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Published in: World Journal of Surgery 3/2021

01-03-2021 | Pancreatoduodenostomy | Original Scientific Report

Complete Lymphadenectomy Around the Entire Superior Mesenteric Artery Improves Survival in Artery-First Approach Pancreatoduodenectomy for T3 Pancreatic Ductal Adenocarcinoma

Authors: Shinjiro Kobayashi, Takehito Otsubo, Hiroshi Nakano, Satoshi Koizumi, Kazunari Nakahara

Published in: World Journal of Surgery | Issue 3/2021

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Abstract

Background

Artery-first approach pancreatoduodenectomy (AFA-PD) is an important technique for treating pancreatic ductal adenocarcinoma (PDAC). However, it remains unknown whether performing complete lymphadenectomy around the entire superior mesenteric artery (SMA) is associated with better outcomes. In this retrospective study, we aimed to investigate whether this approach improved overall and recurrence-free survival in patients with PDAC.

Methods

We identified 88 patients with T3 PDAC who underwent PD at St. Marianna University School of Medicine, Kawasaki, Japan, between April 2005 and October 2017. Two groups were defined: an “AFA-PD group” (n = 45) who had undergone AFA-PD in addition to complete lymphadenectomy around the entire SMA, and a “conventional PD group” (n = 43) in whom complete lymphadenectomy had not been performed (conventional group). Univariate and multivariate survival analyses were performed to identify risk factors for overall and disease-free survival.

Results

The AFA-PD group had a longer median survival time (40.3 vs. 22.6 months; p = 0.0140) and a higher 5-year survival rate (40.3% vs. 5.9%, p = 0.005) than the conventional PD group. Multivariate analysis showed that AFA-PD with complete lymphadenectomy around the entire SMA was an independent factor for improved overall survival (p = 0.022). Recurrences around the SMA were significantly less frequent in the AFA-PD group than in the conventional group (22.2% vs. 44.2%, p = 0.041).

Conclusions

AFA-PD with complete lymphadenectomy around the entire SMA can prevent recurrences around the SMA and may prolong overall survival in patients with PDAC.
Literature
1.
go back to reference Weitz J, Rahbari N, Koch M et al (2010) The “artery first” approach for resection of pancreatic head cancer. J Am Coll Surg 210:e1-4CrossRef Weitz J, Rahbari N, Koch M et al (2010) The “artery first” approach for resection of pancreatic head cancer. J Am Coll Surg 210:e1-4CrossRef
2.
go back to reference Ironside N, Barreto SG, Loveday B et al (2018) Meta-analysis of an artery-first approach versus standard pancreatoduodenectomy on perioperative outcomes and survival. Br J Surg 105:628–636CrossRef Ironside N, Barreto SG, Loveday B et al (2018) Meta-analysis of an artery-first approach versus standard pancreatoduodenectomy on perioperative outcomes and survival. Br J Surg 105:628–636CrossRef
3.
go back to reference Jiang X, Yu Z, Ma Z et al (2020) Superior mesenteric artery first approach can improve the clinical outcomes of pancreaticoduodenectomy: a meta-analysis. Int J Surg 73:14–24CrossRef Jiang X, Yu Z, Ma Z et al (2020) Superior mesenteric artery first approach can improve the clinical outcomes of pancreaticoduodenectomy: a meta-analysis. Int J Surg 73:14–24CrossRef
4.
go back to reference Pedrazzoli S, DiCarlo V, Dionigi R et al (1998) 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 228:508–517CrossRef Pedrazzoli S, DiCarlo V, Dionigi R et al (1998) 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 228:508–517CrossRef
5.
go back to reference Nimura Y, Nagino M, Takao S et al (2012) 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 19:230–241CrossRef Nimura Y, Nagino M, Takao S et al (2012) 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 19:230–241CrossRef
6.
go back to reference Jang JY, Kang MJ, Heo JS et al (2014) A prospective randomized controlled study comparing outcomes of standard resection and extended resection, including dissection of the nerve plexus and various lymph nodes, in patients with pancreatic head cancer. Ann Surg 259:656–664CrossRef Jang JY, Kang MJ, Heo JS et al (2014) A prospective randomized controlled study comparing outcomes of standard resection and extended resection, including dissection of the nerve plexus and various lymph nodes, in patients with pancreatic head cancer. Ann Surg 259:656–664CrossRef
7.
go back to reference Yeo CJ, Cameron JL, Sohn TA et al (1999) Pancreaticoduodenectomy with or without extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma: comparison of morbidity and mortality and short-term outcome. Ann Surg 229:613–622 (discussion 622-614)CrossRef Yeo CJ, Cameron JL, Sohn TA et al (1999) Pancreaticoduodenectomy with or without extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma: comparison of morbidity and mortality and short-term outcome. Ann Surg 229:613–622 (discussion 622-614)CrossRef
8.
go back to reference Farnell MB, Pearson RK, Sarr MG et al (2005) A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery 138:618–628 (discussion 628-630)CrossRef Farnell MB, Pearson RK, Sarr MG et al (2005) A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery 138:618–628 (discussion 628-630)CrossRef
9.
go back to reference Japan Pancreas Society (2016) Lymph node metastases. In: General rules for the study of pancreatic cancer, 7th edn. Kanahara Publishing, Tokyo, pp 34–47 Japan Pancreas Society (2016) Lymph node metastases. In: General rules for the study of pancreatic cancer, 7th edn. Kanahara Publishing, Tokyo, pp 34–47
10.
go back to reference Kurosaki I, Minagawa M, Takano K et al (2011) Left posterior approach to the superior mesenteric vascular pedicle in pancreaticoduodenectomy for cancer of the pancreatic head. JOP 12:220–229PubMed Kurosaki I, Minagawa M, Takano K et al (2011) Left posterior approach to the superior mesenteric vascular pedicle in pancreaticoduodenectomy for cancer of the pancreatic head. JOP 12:220–229PubMed
11.
go back to reference Verbeke CS, Leitch D, Menon KV et al (2006) Redefining the R1 resection in pancreatic cancer. Br J Surg 93:1232–1237CrossRef Verbeke CS, Leitch D, Menon KV et al (2006) Redefining the R1 resection in pancreatic cancer. Br J Surg 93:1232–1237CrossRef
12.
go back to reference Chang DK, Johns AL, Merrett ND et al (2009) Margin clearance and outcome in resected pancreatic cancer. J clin oncol 27:2855–2862CrossRef Chang DK, Johns AL, Merrett ND et al (2009) Margin clearance and outcome in resected pancreatic cancer. J clin oncol 27:2855–2862CrossRef
13.
go back to reference Hartwig W, Hackert T, Hinz U et al (2011) Pancreatic cancer surgery in the new millennium: better prediction of outcome. Ann Surg 254:311–319CrossRef Hartwig W, Hackert T, Hinz U et al (2011) Pancreatic cancer surgery in the new millennium: better prediction of outcome. Ann Surg 254:311–319CrossRef
14.
go back to reference Konstantinidis IT, Warshaw AL, Allen JN et al (2013) Pancreatic ductal adenocarcinoma: is there a survival difference for R1 resections versus locally advanced unresectable tumors? what is a “true” R0 resection? Ann Surg 257:731–736CrossRef Konstantinidis IT, Warshaw AL, Allen JN et al (2013) Pancreatic ductal adenocarcinoma: is there a survival difference for R1 resections versus locally advanced unresectable tumors? what is a “true” R0 resection? Ann Surg 257:731–736CrossRef
15.
go back to reference Orci LA, Meyer J, Combescure C et al (2015) A meta-analysis of extended versus standard lymphadenectomy in patients undergoing pancreatoduodenectomy for pancreatic adenocarcinoma. HPB (Oxford) 17:565–572CrossRef Orci LA, Meyer J, Combescure C et al (2015) A meta-analysis of extended versus standard lymphadenectomy in patients undergoing pancreatoduodenectomy for pancreatic adenocarcinoma. HPB (Oxford) 17:565–572CrossRef
16.
go back to reference Michalski CW, Kleeff J, Wente MN et al (2007) Systematic review and meta-analysis of standard and extended lymphadenectomy in pancreaticoduodenectomy for pancreatic cancer. Br J Surg 94:265–273CrossRef Michalski CW, Kleeff J, Wente MN et al (2007) Systematic review and meta-analysis of standard and extended lymphadenectomy in pancreaticoduodenectomy for pancreatic cancer. Br J Surg 94:265–273CrossRef
17.
go back to reference Hartwig W, Vollmer CM, Fingerhut A et al (2014) Extended pancreatectomy in pancreatic ductal adenocarcinoma: definition and consensus of the International Study Group for Pancreatic Surgery (ISGPS). Surgery 156:1–14CrossRef Hartwig W, Vollmer CM, Fingerhut A et al (2014) Extended pancreatectomy in pancreatic ductal adenocarcinoma: definition and consensus of the International Study Group for Pancreatic Surgery (ISGPS). Surgery 156:1–14CrossRef
18.
go back to reference Tomlinson JS, Jain S, Bentrem DJ et al (2007) Accuracy of staging node-negative pancreas cancer: a potential quality measure. Arch Surg 142:767–723 (discussion 773-764)CrossRef Tomlinson JS, Jain S, Bentrem DJ et al (2007) Accuracy of staging node-negative pancreas cancer: a potential quality measure. Arch Surg 142:767–723 (discussion 773-764)CrossRef
19.
go back to reference Slidell MB, Chang DC, Cameron JL et al (2008) Impact of total lymph node count and lymph node ratio on staging and survival after pancreatectomy for pancreatic adenocarcinoma: a large, population-based analysis. Ann Surg Oncol 15:165–217CrossRef Slidell MB, Chang DC, Cameron JL et al (2008) Impact of total lymph node count and lymph node ratio on staging and survival after pancreatectomy for pancreatic adenocarcinoma: a large, population-based analysis. Ann Surg Oncol 15:165–217CrossRef
20.
go back to reference Jamieson NB, Foulis AK, Oien KA et al (2010) Positive mobilization margins alone do not influence survival following pancreatico-duodenectomy for pancreatic ductal adenocarcinoma. Ann Surg 251:1003–1010CrossRef Jamieson NB, Foulis AK, Oien KA et al (2010) Positive mobilization margins alone do not influence survival following pancreatico-duodenectomy for pancreatic ductal adenocarcinoma. Ann Surg 251:1003–1010CrossRef
21.
go back to reference Kanda M, Fujii T, Nagai S et al (2011) Pattern of lymph node metastasis spread in pancreatic cancer. Pancreas 40:951–955CrossRef Kanda M, Fujii T, Nagai S et al (2011) Pattern of lymph node metastasis spread in pancreatic cancer. Pancreas 40:951–955CrossRef
22.
go back to reference Hirono S, Tani M, Kawai M et al (2012) Identification of the lymphatic drainage pathways from the pancreatic head guided by indocyanine green fluorescence imaging during pancreaticoduodenectomy. Dig Surg 29:132–139CrossRef Hirono S, Tani M, Kawai M et al (2012) Identification of the lymphatic drainage pathways from the pancreatic head guided by indocyanine green fluorescence imaging during pancreaticoduodenectomy. Dig Surg 29:132–139CrossRef
23.
go back to reference Tol JA, Gouma DJ, Bassi C et al (2014) Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS). Surgery 156:591–600CrossRef Tol JA, Gouma DJ, Bassi C et al (2014) Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS). Surgery 156:591–600CrossRef
24.
go back to reference Henne-Bruns D, Vogel I, Luttges J et al (2000) Surgery for ductal adenocarcinoma of the pancreatic head: staging, complications, and survival after regional versus extended lymphadenectomy. World J Surg 24:595–601 (discussion 601-592)CrossRef Henne-Bruns D, Vogel I, Luttges J et al (2000) Surgery for ductal adenocarcinoma of the pancreatic head: staging, complications, and survival after regional versus extended lymphadenectomy. World J Surg 24:595–601 (discussion 601-592)CrossRef
25.
go back to reference Sanjay P, Takaori K, Govil S et al (2012) “Artery-first” approaches to pancreatoduodenectomy. Br J Surg 99:1027–1035CrossRef Sanjay P, Takaori K, Govil S et al (2012) “Artery-first” approaches to pancreatoduodenectomy. Br J Surg 99:1027–1035CrossRef
26.
go back to reference Pessaux P, Varma D, Arnaud JP (2006) Pancreaticoduodenectomy: superior mesenteric artery first approach. J Gastrointest Surg 10:607–611CrossRef Pessaux P, Varma D, Arnaud JP (2006) Pancreaticoduodenectomy: superior mesenteric artery first approach. J Gastrointest Surg 10:607–611CrossRef
27.
go back to reference Dumitrascu T, David L, Popescu I (2010) Posterior versus standard approach in pancreatoduodenectomy: a case-match study. Langenbecks Arch Surg 395:677–684CrossRef Dumitrascu T, David L, Popescu I (2010) Posterior versus standard approach in pancreatoduodenectomy: a case-match study. Langenbecks Arch Surg 395:677–684CrossRef
28.
go back to reference Nakao A, Takagi H (1993) Isolated pancreatectomy for pancreatic head carcinoma using catheter bypass of the portal vein. Hepatogastroenterology 40:426–429PubMed Nakao A, Takagi H (1993) Isolated pancreatectomy for pancreatic head carcinoma using catheter bypass of the portal vein. Hepatogastroenterology 40:426–429PubMed
29.
go back to reference Iede K, Nakao A, Oshima KS et al (2018) Early ligation of the dorsal pancreatic artery with a mesenteric approach reduces intraoperative blood loss during pancreatoduodenectomy. J Hepatobiliary Pancreat Sci 25:329–334CrossRef Iede K, Nakao A, Oshima KS et al (2018) Early ligation of the dorsal pancreatic artery with a mesenteric approach reduces intraoperative blood loss during pancreatoduodenectomy. J Hepatobiliary Pancreat Sci 25:329–334CrossRef
30.
go back to reference Hirono S, Kawai M, Okada K et al (2017) Mesenteric approach during pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. Ann Gastroenterol Surg 1:208–218CrossRef Hirono S, Kawai M, Okada K et al (2017) Mesenteric approach during pancreaticoduodenectomy for pancreatic ductal adenocarcinoma. Ann Gastroenterol Surg 1:208–218CrossRef
31.
go back to reference Mizuno S, Isaji S, Tanemura A et al (2014) Anterior approach to the superior mesenteric artery by using nerve plexus hanging maneuver for borderline resectable pancreatic head carcinoma. J Gastrointest Surg 18:1209–1215CrossRef Mizuno S, Isaji S, Tanemura A et al (2014) Anterior approach to the superior mesenteric artery by using nerve plexus hanging maneuver for borderline resectable pancreatic head carcinoma. J Gastrointest Surg 18:1209–1215CrossRef
32.
go back to reference Inoue Y, Saiura A, Tanaka M et al (2016) Technical details of an anterior approach to the superior mesenteric artery during pancreaticoduodenectomy. J Gastrointest Surg 20:1769–1777CrossRef Inoue Y, Saiura A, Tanaka M et al (2016) Technical details of an anterior approach to the superior mesenteric artery during pancreaticoduodenectomy. J Gastrointest Surg 20:1769–1777CrossRef
33.
go back to reference Nagakawa Y, Hosokawa Y, Sahara Y et al (2015) A novel “artery first” approach allowing safe resection in laparoscopic pancreaticoduodenectomy: the uncinate process first approach. Hepatogastroenterology 62:1037–1040PubMed Nagakawa Y, Hosokawa Y, Sahara Y et al (2015) A novel “artery first” approach allowing safe resection in laparoscopic pancreaticoduodenectomy: the uncinate process first approach. Hepatogastroenterology 62:1037–1040PubMed
34.
go back to reference Kawabata Y, Tanaka T, Nishi T et al (2012) Appraisal of a total meso-pancreatoduodenum excision with pancreaticoduodenectomy for pancreatic head carcinoma. Eur J Surg Oncol 38:574–579CrossRef Kawabata Y, Tanaka T, Nishi T et al (2012) Appraisal of a total meso-pancreatoduodenum excision with pancreaticoduodenectomy for pancreatic head carcinoma. Eur J Surg Oncol 38:574–579CrossRef
35.
go back to reference Sabater L, Cugat E, Serrablo A et al (2019) Does the artery-first approach improve the rate of R0 resection in pancreatoduodenectomy?: a multicenter, randomized, controlled trial. Ann Surg 270:738–746CrossRef Sabater L, Cugat E, Serrablo A et al (2019) Does the artery-first approach improve the rate of R0 resection in pancreatoduodenectomy?: a multicenter, randomized, controlled trial. Ann Surg 270:738–746CrossRef
36.
go back to reference Hirono S, Kawai M, Okada KI et al (2018) MAPLE-PD trial (mesenteric approach vs. conventional approach for pancreatic cancer during pancreaticoduodenectomy): study protocol for a multicenter randomized controlled trial of 354 patients with pancreatic ductal adenocarcinoma. Trials 19(1):613CrossRef Hirono S, Kawai M, Okada KI et al (2018) MAPLE-PD trial (mesenteric approach vs. conventional approach for pancreatic cancer during pancreaticoduodenectomy): study protocol for a multicenter randomized controlled trial of 354 patients with pancreatic ductal adenocarcinoma. Trials 19(1):613CrossRef
37.
go back to reference Neoptolemos JP, Stocken DD, Friess H et al (2004) A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med 350:1200–1210CrossRef Neoptolemos JP, Stocken DD, Friess H et al (2004) A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med 350:1200–1210CrossRef
38.
go back to reference Uesaka K, Boku N, Fukutomi A et al (2016) Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: a phase 3, open-label, randomised, non-inferiority trial (JASPAC 01). Lancet 388:248–257CrossRef Uesaka K, Boku N, Fukutomi A et al (2016) Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: a phase 3, open-label, randomised, non-inferiority trial (JASPAC 01). Lancet 388:248–257CrossRef
Metadata
Title
Complete Lymphadenectomy Around the Entire Superior Mesenteric Artery Improves Survival in Artery-First Approach Pancreatoduodenectomy for T3 Pancreatic Ductal Adenocarcinoma
Authors
Shinjiro Kobayashi
Takehito Otsubo
Hiroshi Nakano
Satoshi Koizumi
Kazunari Nakahara
Publication date
01-03-2021
Publisher
Springer International Publishing
Published in
World Journal of Surgery / Issue 3/2021
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-020-05856-w

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