Skip to main content
Top
Published in: Langenbeck's Archives of Surgery 7/2020

01-11-2020 | Metastasis | Review Article

Role of lymphadenectomy in resectable pancreatic cancer

Authors: Suna Erdem, Martin Bolli, Sascha A. Müller, Markus von Flüe, Rebekah White, Mathias Worni

Published in: Langenbeck's Archives of Surgery | Issue 7/2020

Login to get access

Abstract

Background

Pancreatic cancer (PC) remains one of the most devastating malignant diseases, predicted to become the second leading cause of cancer-related death by 2030. Despite advances in surgical techniques and in systemic therapy, the 5-year relative survival remains a grim 9% for all stages combined. The extent of lymphadenectomy has been discussed intensively for decades, given that even in early stages of PC, lymph node (LN) metastasis can be detected in approximately 80%.

Purpose

The primary objective of this review was to provide an overview of the current literature evaluating the role of lymphadenectomy in resected PC. For this, we evaluated randomized controlled studies (RCTs) assessing the impact of extent of lymphadenectomy on OS and studies evaluating the prognostic impact of anatomical site of LN metastasis and the impact of the number of resected LNs on OS.

Conclusions

Lymphadenectomy plays an essential part in the multimodal treatment algorithm of PC and is an additional therapeutic tool to increase the chance for surgical radicality and to ensure correct staging for optimal oncological therapy. Based on the literature from the last decades, standard lymphadenectomy with resection of at least ≥ 15 LNs is associated with an acceptable postoperative complication risk and should be recommended to obtain local radicality and accurate staging of the disease. Although radical surgery including appropriate lymphadenectomy of regional LNs remains the only chance for long-term tumor control, future studies specifically assessing the impact of neoadjuvant therapy on extraregional LNs are warranted.
Literature
3.
go back to reference Oettle H, Neuhaus P, Hochhaus A, Hartmann JT, Gellert K, Ridwelski K, Niedergethmann M, Zulke C, Fahlke J, Arning MB, Sinn M, Hinke A, Riess H (2013) Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA 310(14):1473–1481. https://doi.org/10.1001/jama.2013.279201CrossRefPubMed Oettle H, Neuhaus P, Hochhaus A, Hartmann JT, Gellert K, Ridwelski K, Niedergethmann M, Zulke C, Fahlke J, Arning MB, Sinn M, Hinke A, Riess H (2013) Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA 310(14):1473–1481. https://​doi.​org/​10.​1001/​jama.​2013.​279201CrossRefPubMed
4.
go back to reference Neoptolemos JP, Stocken DD, Bassi C, Ghaneh P, Cunningham D, Goldstein D, Padbury R, Moore MJ, Gallinger S, Mariette C, Wente MN, Izbicki JR, Friess H, Lerch MM, Dervenis C, Olah A, Butturini G, Doi R, Lind PA, Smith D, Valle JW, Palmer DH, Buckels JA, Thompson J, McKay CJ, Rawcliffe CL, Buchler MW, European Study Group for Pancreatic C (2010) Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial. JAMA 304(10):1073–1081. https://doi.org/10.1001/jama.2010.1275CrossRefPubMed Neoptolemos JP, Stocken DD, Bassi C, Ghaneh P, Cunningham D, Goldstein D, Padbury R, Moore MJ, Gallinger S, Mariette C, Wente MN, Izbicki JR, Friess H, Lerch MM, Dervenis C, Olah A, Butturini G, Doi R, Lind PA, Smith D, Valle JW, Palmer DH, Buckels JA, Thompson J, McKay CJ, Rawcliffe CL, Buchler MW, European Study Group for Pancreatic C (2010) Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial. JAMA 304(10):1073–1081. https://​doi.​org/​10.​1001/​jama.​2010.​1275CrossRefPubMed
5.
go back to reference Uesaka K, Boku N, Fukutomi A, Okamura Y, Konishi M, Matsumoto I, Kaneoka Y, Shimizu Y, Nakamori S, Sakamoto H, Morinaga S, Kainuma O, Imai K, Sata N, Hishinuma S, Ojima H, Yamaguchi R, Hirano S, Sudo T, Ohashi Y, Group JS (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(10041):248–257. https://doi.org/10.1016/S0140-6736(16)30583-9CrossRefPubMed Uesaka K, Boku N, Fukutomi A, Okamura Y, Konishi M, Matsumoto I, Kaneoka Y, Shimizu Y, Nakamori S, Sakamoto H, Morinaga S, Kainuma O, Imai K, Sata N, Hishinuma S, Ojima H, Yamaguchi R, Hirano S, Sudo T, Ohashi Y, Group JS (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(10041):248–257. https://​doi.​org/​10.​1016/​S0140-6736(16)30583-9CrossRefPubMed
6.
go back to reference Neoptolemos JP, Palmer DH, Ghaneh P, Psarelli EE, Valle JW, Halloran CM, Faluyi O, O'Reilly DA, Cunningham D, Wadsley J, Darby S, Meyer T, Gillmore R, Anthoney A, Lind P, Glimelius B, Falk S, Izbicki JR, Middleton GW, Cummins S, Ross PJ, Wasan H, McDonald A, Crosby T, Ma YT, Patel K, Sherriff D, Soomal R, Borg D, Sothi S, Hammel P, Hackert T, Jackson R, Buchler MW, European Study Group for Pancreatic C (2017) 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 389(10073):1011–1024. https://doi.org/10.1016/S0140-6736(16)32409-6CrossRefPubMed Neoptolemos JP, Palmer DH, Ghaneh P, Psarelli EE, Valle JW, Halloran CM, Faluyi O, O'Reilly DA, Cunningham D, Wadsley J, Darby S, Meyer T, Gillmore R, Anthoney A, Lind P, Glimelius B, Falk S, Izbicki JR, Middleton GW, Cummins S, Ross PJ, Wasan H, McDonald A, Crosby T, Ma YT, Patel K, Sherriff D, Soomal R, Borg D, Sothi S, Hammel P, Hackert T, Jackson R, Buchler MW, European Study Group for Pancreatic C (2017) 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 389(10073):1011–1024. https://​doi.​org/​10.​1016/​S0140-6736(16)32409-6CrossRefPubMed
7.
go back to reference Sinn M, Bahra M, Liersch T, Gellert K, Messmann H, Bechstein W, Waldschmidt D, Jacobasch L, Wilhelm M, Rau BM, Grutzmann R, Weinmann A, Maschmeyer G, Pelzer U, Stieler JM, Striefler JK, Ghadimi M, Bischoff S, Dorken B, Oettle H, Riess H (2017) CONKO-005: Adjuvant chemotherapy with gemcitabine plus erlotinib versus gemcitabine alone in patients after R0 resection of pancreatic cancer: a multicenter randomized phase III trial. J Clin Oncol 35(29):3330–3337. https://doi.org/10.1200/JCO.2017.72.6463CrossRefPubMed Sinn M, Bahra M, Liersch T, Gellert K, Messmann H, Bechstein W, Waldschmidt D, Jacobasch L, Wilhelm M, Rau BM, Grutzmann R, Weinmann A, Maschmeyer G, Pelzer U, Stieler JM, Striefler JK, Ghadimi M, Bischoff S, Dorken B, Oettle H, Riess H (2017) CONKO-005: Adjuvant chemotherapy with gemcitabine plus erlotinib versus gemcitabine alone in patients after R0 resection of pancreatic cancer: a multicenter randomized phase III trial. J Clin Oncol 35(29):3330–3337. https://​doi.​org/​10.​1200/​JCO.​2017.​72.​6463CrossRefPubMed
9.
go back to reference Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, Adenis A, Raoul JL, Gourgou-Bourgade S, de la Fouchardiere C, Bennouna J, Bachet JB, Khemissa-Akouz F, Pere-Verge D, Delbaldo C, Assenat E, Chauffert B, Michel P, Montoto-Grillot C, Ducreux M, Groupe Tumeurs Digestives of U, Intergroup P (2011) FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 364(19):1817–1825. https://doi.org/10.1056/NEJMoa1011923CrossRefPubMed Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, Adenis A, Raoul JL, Gourgou-Bourgade S, de la Fouchardiere C, Bennouna J, Bachet JB, Khemissa-Akouz F, Pere-Verge D, Delbaldo C, Assenat E, Chauffert B, Michel P, Montoto-Grillot C, Ducreux M, Groupe Tumeurs Digestives of U, Intergroup P (2011) FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 364(19):1817–1825. https://​doi.​org/​10.​1056/​NEJMoa1011923CrossRefPubMed
10.
go back to reference Conroy T, Hammel P, Hebbar M, Ben Abdelghani M, Wei AC, Raoul JL, Chone L, Francois E, Artru P, Biagi JJ, Lecomte T, Assenat E, Faroux R, Ychou M, Volet J, Sauvanet A, Breysacher G, Di Fiore F, Cripps C, Kavan P, Texereau P, Bouhier-Leporrier K, Khemissa-Akouz F, Legoux JL, Juzyna B, Gourgou S, O'Callaghan CJ, Jouffroy-Zeller C, Rat P, Malka D, Castan F, Bachet JB, Canadian Cancer Trials G, the Unicancer GIPG (2018) FOLFIRINOX or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med 379(25):2395–2406. https://doi.org/10.1056/NEJMoa1809775CrossRefPubMed Conroy T, Hammel P, Hebbar M, Ben Abdelghani M, Wei AC, Raoul JL, Chone L, Francois E, Artru P, Biagi JJ, Lecomte T, Assenat E, Faroux R, Ychou M, Volet J, Sauvanet A, Breysacher G, Di Fiore F, Cripps C, Kavan P, Texereau P, Bouhier-Leporrier K, Khemissa-Akouz F, Legoux JL, Juzyna B, Gourgou S, O'Callaghan CJ, Jouffroy-Zeller C, Rat P, Malka D, Castan F, Bachet JB, Canadian Cancer Trials G, the Unicancer GIPG (2018) FOLFIRINOX or gemcitabine as adjuvant therapy for pancreatic cancer. N Engl J Med 379(25):2395–2406. https://​doi.​org/​10.​1056/​NEJMoa1809775CrossRefPubMed
11.
go back to reference Von Hoff DD, Ervin T, Arena FP, Chiorean EG, Infante J, Moore M, Seay T, Tjulandin SA, Ma WW, Saleh MN, Harris M, Reni M, Dowden S, Laheru D, Bahary N, Ramanathan RK, Tabernero J, Hidalgo M, Goldstein D, Van Cutsem E, Wei X, Iglesias J, Renschler MF (2013) Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med 369(18):1691–1703. https://doi.org/10.1056/NEJMoa1304369CrossRef Von Hoff DD, Ervin T, Arena FP, Chiorean EG, Infante J, Moore M, Seay T, Tjulandin SA, Ma WW, Saleh MN, Harris M, Reni M, Dowden S, Laheru D, Bahary N, Ramanathan RK, Tabernero J, Hidalgo M, Goldstein D, Van Cutsem E, Wei X, Iglesias J, Renschler MF (2013) Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med 369(18):1691–1703. https://​doi.​org/​10.​1056/​NEJMoa1304369CrossRef
12.
21.
24.
26.
go back to reference Showalter TN, Winter KA, Berger AC, Regine WF, Abrams RA, Safran H, Hoffman JP, Benson AB, MacDonald JS, Willett CG (2011) The influence of total nodes examined, number of positive nodes, and lymph node ratio on survival after surgical resection and adjuvant chemoradiation for pancreatic cancer: a secondary analysis of RTOG 9704. Int J Radiat Oncol Biol Phys 81(5):1328–1335. https://doi.org/10.1016/j.ijrobp.2010.07.1993CrossRefPubMed Showalter TN, Winter KA, Berger AC, Regine WF, Abrams RA, Safran H, Hoffman JP, Benson AB, MacDonald JS, Willett CG (2011) The influence of total nodes examined, number of positive nodes, and lymph node ratio on survival after surgical resection and adjuvant chemoradiation for pancreatic cancer: a secondary analysis of RTOG 9704. Int J Radiat Oncol Biol Phys 81(5):1328–1335. https://​doi.​org/​10.​1016/​j.​ijrobp.​2010.​07.​1993CrossRefPubMed
27.
go back to reference Morales-Oyarvide V, Rubinson DA, Dunne RF, Kozak MM, Bui JL, Yuan C, Qian ZR, Babic A, Da Silva A, Nowak JA, Khalaf N, Brais LK, Welch MW, Zellers CL, Ng K, Chang DT, Miksad RA, Bullock AJ, Tseng JF, Swanson RS, Clancy TE, Linehan DC, Findeis-Hosey JJ, Doyle LA, Hornick JL, Ogino S, Fuchs CS, Hezel AF, Koong AC, Wolpin BM (2017) Lymph node metastases in resected pancreatic ductal adenocarcinoma: predictors of disease recurrence and survival. Br J Cancer 117(12):1874–1882. https://doi.org/10.1038/bjc.2017.349CrossRefPubMedPubMedCentral Morales-Oyarvide V, Rubinson DA, Dunne RF, Kozak MM, Bui JL, Yuan C, Qian ZR, Babic A, Da Silva A, Nowak JA, Khalaf N, Brais LK, Welch MW, Zellers CL, Ng K, Chang DT, Miksad RA, Bullock AJ, Tseng JF, Swanson RS, Clancy TE, Linehan DC, Findeis-Hosey JJ, Doyle LA, Hornick JL, Ogino S, Fuchs CS, Hezel AF, Koong AC, Wolpin BM (2017) Lymph node metastases in resected pancreatic ductal adenocarcinoma: predictors of disease recurrence and survival. Br J Cancer 117(12):1874–1882. https://​doi.​org/​10.​1038/​bjc.​2017.​349CrossRefPubMedPubMedCentral
31.
go back to reference Warschkow R, Tsai C, Kohn N, Erdem S, Schmied B, Nussbaum DP, Gloor B, Muller SA, Blazer D 3rd, Worni M (2020) Role of lymphadenectomy, adjuvant chemotherapy, and treatment at high-volume centers in patients with resected pancreatic cancer-a distinct view on lymph node yield. Langenbecks Arch Surg 405(1):43–54. https://doi.org/10.1007/s00423-020-01859-2CrossRefPubMed Warschkow R, Tsai C, Kohn N, Erdem S, Schmied B, Nussbaum DP, Gloor B, Muller SA, Blazer D 3rd, Worni M (2020) Role of lymphadenectomy, adjuvant chemotherapy, and treatment at high-volume centers in patients with resected pancreatic cancer-a distinct view on lymph node yield. Langenbecks Arch Surg 405(1):43–54. https://​doi.​org/​10.​1007/​s00423-020-01859-2CrossRefPubMed
32.
go back to reference Yeo CJ, Cameron JL, Lillemoe KD, Sohn TA, Campbell KA, Sauter PK, Coleman J, Abrams RA, Hruban RH (2002) 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 236(3):355–366; discussion 366-358. https://doi.org/10.1097/00000658-200209000-00012CrossRefPubMedPubMedCentral Yeo CJ, Cameron JL, Lillemoe KD, Sohn TA, Campbell KA, Sauter PK, Coleman J, Abrams RA, Hruban RH (2002) 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 236(3):355–366; discussion 366-358. https://​doi.​org/​10.​1097/​00000658-200209000-00012CrossRefPubMedPubMedCentral
33.
go back to reference Farnell MB, Pearson RK, Sarr MG, DiMagno EP, Burgart LJ, Dahl TR, Foster N, Sargent DJ, Pancreas Cancer Working G (2005) A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery 138(4):618–628; discussion 628-630. https://doi.org/10.1016/j.surg.2005.06.044CrossRefPubMed Farnell MB, Pearson RK, Sarr MG, DiMagno EP, Burgart LJ, Dahl TR, Foster N, Sargent DJ, Pancreas Cancer Working G (2005) A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery 138(4):618–628; discussion 628-630. https://​doi.​org/​10.​1016/​j.​surg.​2005.​06.​044CrossRefPubMed
34.
go back to reference Tol JA, Gouma DJ, Bassi C, Dervenis C, Montorsi M, Adham M, Andren-Sandberg A, Asbun HJ, Bockhorn M, Buchler MW, Conlon KC, Fernandez-Cruz L, Fingerhut A, Friess H, Hartwig W, Izbicki JR, Lillemoe KD, Milicevic MN, Neoptolemos JP, Shrikhande SV, Vollmer CM, Yeo CJ, Charnley RM, International Study Group on Pancreatic S (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(3):591–600. https://doi.org/10.1016/j.surg.2014.06.016CrossRefPubMed Tol JA, Gouma DJ, Bassi C, Dervenis C, Montorsi M, Adham M, Andren-Sandberg A, Asbun HJ, Bockhorn M, Buchler MW, Conlon KC, Fernandez-Cruz L, Fingerhut A, Friess H, Hartwig W, Izbicki JR, Lillemoe KD, Milicevic MN, Neoptolemos JP, Shrikhande SV, Vollmer CM, Yeo CJ, Charnley RM, International Study Group on Pancreatic S (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(3):591–600. https://​doi.​org/​10.​1016/​j.​surg.​2014.​06.​016CrossRefPubMed
35.
go back to reference Pedrazzoli S, Beger HG, Obertop H, Andren-Sandberg A, Fernandez-Cruz L, Henne-Bruns D, Luttges J, Neoptolemos JP (1999) A surgical and pathological based classification of resective treatment of pancreatic cancer. Summary of an international workshop on surgical procedures in pancreatic cancer. Dig Surg 16(4):337–345. https://doi.org/10.1159/000018744CrossRefPubMed Pedrazzoli S, Beger HG, Obertop H, Andren-Sandberg A, Fernandez-Cruz L, Henne-Bruns D, Luttges J, Neoptolemos JP (1999) A surgical and pathological based classification of resective treatment of pancreatic cancer. Summary of an international workshop on surgical procedures in pancreatic cancer. Dig Surg 16(4):337–345. https://​doi.​org/​10.​1159/​000018744CrossRefPubMed
36.
go back to reference Isaji SMY, Kishiwada M (2018) New Japanese classification of pancreatic cancer Pancreatic cancer 7 ed Springer: p. 1021–1037 Isaji SMY, Kishiwada M (2018) New Japanese classification of pancreatic cancer Pancreatic cancer 7 ed Springer: p. 1021–1037
37.
go back to reference Society JP (2003) Classification of pancreatic carcinoma (2nd English ed.). Kanehara & Co Ltd, Tokyo Society JP (2003) Classification of pancreatic carcinoma (2nd English ed.). Kanehara & Co Ltd, Tokyo
38.
go back to reference Ducreux M, Cuhna AS, Caramella C, Hollebecque A, Burtin P, Goere D, Seufferlein T, Haustermans K, Van Laethem JL, Conroy T, Arnold D, Committee EG (2015) Cancer of the pancreas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 26(Suppl 5):v56–v68. https://doi.org/10.1093/annonc/mdv295CrossRefPubMed Ducreux M, Cuhna AS, Caramella C, Hollebecque A, Burtin P, Goere D, Seufferlein T, Haustermans K, Van Laethem JL, Conroy T, Arnold D, Committee EG (2015) Cancer of the pancreas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 26(Suppl 5):v56–v68. https://​doi.​org/​10.​1093/​annonc/​mdv295CrossRefPubMed
40.
go back to reference Japan Pancreas Society KC, Ltd. Classification of pancreatic carcinoma. 2nd English ed. Tokyo Japan Pancreas Society KC, Ltd. Classification of pancreatic carcinoma. 2nd English ed. Tokyo
42.
go back to reference Nimura Y, Nagino M, Takao S, Takada T, Miyazaki K, Kawarada Y, Miyagawa S, Yamaguchi A, Ishiyama S, Takeda Y, Sakoda K, Kinoshita T, Yasui K, Shimada H, Katoh H (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(3):230–241. https://doi.org/10.1007/s00534-011-0466-6CrossRefPubMed Nimura Y, Nagino M, Takao S, Takada T, Miyazaki K, Kawarada Y, Miyagawa S, Yamaguchi A, Ishiyama S, Takeda Y, Sakoda K, Kinoshita T, Yasui K, Shimada H, Katoh H (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(3):230–241. https://​doi.​org/​10.​1007/​s00534-011-0466-6CrossRefPubMed
43.
go back to reference Jang JY, Kang MJ, Heo JS, Choi SH, Choi DW, Park SJ, Han SS, Yoon DS, Yu HC, Kang KJ, Kim SG, Kim SW (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(4):656–664. https://doi.org/10.1097/SLA.0000000000000384CrossRefPubMed Jang JY, Kang MJ, Heo JS, Choi SH, Choi DW, Park SJ, Han SS, Yoon DS, Yu HC, Kang KJ, Kim SG, Kim SW (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(4):656–664. https://​doi.​org/​10.​1097/​SLA.​0000000000000384​CrossRefPubMed
44.
go back to reference Jang JY, Kang JS, Han Y, Heo JS, Choi SH, Choi DW, Park SJ, Han SS, Yoon DS, Park JS, Yu HC, Kang KJ, Kim SG, Lee H, Kwon W, Yoon YS, Han HS, Kim SW (2017) Long-term outcomes and recurrence patterns of standard versus extended pancreatectomy for pancreatic head cancer: a multicenter prospective randomized controlled study. J Hepatobiliary Pancreat Sci 24(7):426–433. https://doi.org/10.1002/jhbp.465CrossRefPubMed Jang JY, Kang JS, Han Y, Heo JS, Choi SH, Choi DW, Park SJ, Han SS, Yoon DS, Park JS, Yu HC, Kang KJ, Kim SG, Lee H, Kwon W, Yoon YS, Han HS, Kim SW (2017) Long-term outcomes and recurrence patterns of standard versus extended pancreatectomy for pancreatic head cancer: a multicenter prospective randomized controlled study. J Hepatobiliary Pancreat Sci 24(7):426–433. https://​doi.​org/​10.​1002/​jhbp.​465CrossRefPubMed
45.
go back to reference Ignjatovic I, Knezevic S, Knezevic D, Dugalic V, Micev M, Matic S, Ostojic S, Bogdanovic M, Pavlovic I, Jurisic V (2017) Standard versus extended lymphadenectomy in radical surgical treatment for pancreatic head carcinoma. J BUON 22(1):232–238PubMed Ignjatovic I, Knezevic S, Knezevic D, Dugalic V, Micev M, Matic S, Ostojic S, Bogdanovic M, Pavlovic I, Jurisic V (2017) Standard versus extended lymphadenectomy in radical surgical treatment for pancreatic head carcinoma. J BUON 22(1):232–238PubMed
59.
go back to reference van Rijssen LB, Narwade P, van Huijgevoort NC, Tseng DS, van Santvoort HC, Molenaar IQ, van Laarhoven HW, van Eijck CH, Busch OR, Besselink MG, Dutch Pancreatic Cancer G (2016) Prognostic value of lymph node metastases detected during surgical exploration for pancreatic or periampullary cancer: a systematic review and meta-analysis. HPB (Oxford) 18(7):559–566. https://doi.org/10.1016/j.hpb.2016.05.001CrossRef van Rijssen LB, Narwade P, van Huijgevoort NC, Tseng DS, van Santvoort HC, Molenaar IQ, van Laarhoven HW, van Eijck CH, Busch OR, Besselink MG, Dutch Pancreatic Cancer G (2016) Prognostic value of lymph node metastases detected during surgical exploration for pancreatic or periampullary cancer: a systematic review and meta-analysis. HPB (Oxford) 18(7):559–566. https://​doi.​org/​10.​1016/​j.​hpb.​2016.​05.​001CrossRef
60.
61.
go back to reference Sho M, Murakami Y, Motoi F, Satoi S, Matsumoto I, Kawai M, Honda G, Uemura K, Yanagimoto H, Kurata M, Fukumoto T, Akahori T, Kinoshita S, Nagai M, Nishiwada S, Unno M, Yamaue H, Nakajima Y (2015) Postoperative prognosis of pancreatic cancer with para-aortic lymph node metastasis: a multicenter study on 822 patients. J Gastroenterol 50(6):694–702. https://doi.org/10.1007/s00535-014-1005-4CrossRefPubMed Sho M, Murakami Y, Motoi F, Satoi S, Matsumoto I, Kawai M, Honda G, Uemura K, Yanagimoto H, Kurata M, Fukumoto T, Akahori T, Kinoshita S, Nagai M, Nishiwada S, Unno M, Yamaue H, Nakajima Y (2015) Postoperative prognosis of pancreatic cancer with para-aortic lymph node metastasis: a multicenter study on 822 patients. J Gastroenterol 50(6):694–702. https://​doi.​org/​10.​1007/​s00535-014-1005-4CrossRefPubMed
66.
go back to reference Warschkow R, Widmann B, Beutner U, Marti L, Steffen T, Schiesser M, Schmied BM (2017) The more the better-lower rate of stage migration and better survival in patients with retrieval of 20 or more regional lymph nodes in pancreatic cancer: a population-based propensity score matched and trend SEER analysis. Pancreas 46(5):648–657. https://doi.org/10.1097/MPA.0000000000000784CrossRefPubMed Warschkow R, Widmann B, Beutner U, Marti L, Steffen T, Schiesser M, Schmied BM (2017) The more the better-lower rate of stage migration and better survival in patients with retrieval of 20 or more regional lymph nodes in pancreatic cancer: a population-based propensity score matched and trend SEER analysis. Pancreas 46(5):648–657. https://​doi.​org/​10.​1097/​MPA.​0000000000000784​CrossRefPubMed
68.
70.
75.
go back to reference Malleo G, Maggino L, Capelli P, Gulino F, Segattini S, Scarpa A, Bassi C, Butturini G, Salvia R (2015) Reappraisal of nodal staging and study of lymph node station involvement in pancreaticoduodenectomy with the standard international study group of pancreatic surgery definition of lymphadenectomy for cancer. J Am Coll Surg 221(2):367–379 e364. https://doi.org/10.1016/j.jamcollsurg.2015.02.019CrossRefPubMed Malleo G, Maggino L, Capelli P, Gulino F, Segattini S, Scarpa A, Bassi C, Butturini G, Salvia R (2015) Reappraisal of nodal staging and study of lymph node station involvement in pancreaticoduodenectomy with the standard international study group of pancreatic surgery definition of lymphadenectomy for cancer. J Am Coll Surg 221(2):367–379 e364. https://​doi.​org/​10.​1016/​j.​jamcollsurg.​2015.​02.​019CrossRefPubMed
88.
Metadata
Title
Role of lymphadenectomy in resectable pancreatic cancer
Authors
Suna Erdem
Martin Bolli
Sascha A. Müller
Markus von Flüe
Rebekah White
Mathias Worni
Publication date
01-11-2020
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 7/2020
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-020-01980-2

Other articles of this Issue 7/2020

Langenbeck's Archives of Surgery 7/2020 Go to the issue