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Conversion surgery for initially unresectable pancreatic cancer: current status and unresolved issues

  • Hideyuki YoshitomiEmail author
  • Shigetsugu Takano
  • Katsunori Furukawa
  • Tsukasa Takayashiki
  • Satoshi Kuboki
  • Masayuki Ohtsuka
Review Article
  • 72 Downloads

Abstract

Pancreatic cancer is one of the most lethal of all malignancies. One of the reasons for the dismal prognosis is that most diagnoses are made when the disease is either locally advanced or metastatic. Recent advances in chemotherapy and chemoradiotherapy (CRT) enable “conversion surgery” to be performed for selected patients with initially unresectable pancreatic cancer following favorable responses to preoperative treatment. Using FOLFIRINOX as preoperative treatment, the resection rate was reported as 6–44% of patients with locally advanced cancer and the prognosis of these patients was favorable. Even for metastasized cancer, recent reports show the effectiveness of conversion surgery, which has achieved 27–56 months of median overall survival. However, there are many unanswered questions about conversion surgery. The optimal regimen and duration of preoperative treatment remain unclear and there is still debate regarding the safety and effectiveness of vascular resection, which is often required for curative resection of locally advanced cancer. Accumulation of more data on conversion surgery is required to establish the safety and effectiveness of this treatment. In this review, we summarize the current status and unresolved issues about conversion surgery for initially unresectable pancreatic cancer.

Keywords

Conversion surgery Unresectable pancreatic cancer Preoperative therapy 

Notes

Acknowledgements

We thank all members of the Department of General Surgery, Chiba University, Graduate School of Medicine for their support and suggestions.

Compliance with ethical standards

Conflict of interest

Hideyuki Yoshitomi and his co-authors have no conflicts of interest to declare.

References

  1. 1.
    The editorial board of the cancer statistics in Japan. Cancer statistics in Japan-2017. Foundation for promotion of cancer research (FPCR); 2018.Google Scholar
  2. 2.
    Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68:7–30.CrossRefGoogle Scholar
  3. 3.
    Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74:2913–21.CrossRefGoogle Scholar
  4. 4.
    Imamura M, Doi R, Imaizumi T, Funakoshi A, Wakasugi H, Sunamura M, et al. A randomized multicenter trial comparing resection and radiochemotherapy for resectable locally invasive pancreatic cancer. Surgery. 2004; 136: 1003–11.Google Scholar
  5. 5.
    Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet. 2011;378:607–20.CrossRefGoogle Scholar
  6. 6.
    Burris HA 3rd, 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. 1997;15:2403–13.CrossRefGoogle Scholar
  7. 7.
    Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364:1817–25.CrossRefGoogle Scholar
  8. 8.
    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.CrossRefGoogle Scholar
  9. 9.
    Badiyan SN, Molitoris JK, Chuong MD, Regine WF, Kaiser A. The role of radiation therapy for pancreatic cancer in the adjuvant and neoadjuvant settings. Surg Oncol Clin N Am. 2017;26:431–53.CrossRefGoogle Scholar
  10. 10.
    Oettle H, Neuhaus P, Hochhaus A, Hartmann JT, Gellert K, Ridwelski K, et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA. 2013;310:1473–81.CrossRefGoogle Scholar
  11. 11.
    Uesaka K, Boku N, Fukutomi A, Okamura Y, Konishi M, Matsumoto I, et al. Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: a phase 3, open-label, randomised, non-inferiority trial (JASPAC 01). Lancet. 2016;388:248–57.CrossRefGoogle Scholar
  12. 12.
    Dhir M, Malhotra GK, Sohal DPS, Hein NA, Smith LM, O'Reilly EM, et al. Neoadjuvant treatment of pancreatic adenocarcinoma: a systematic review and meta-analysis of 5520 patients. World J Surg Oncol. 2017;15:183.CrossRefGoogle Scholar
  13. 13.
    Satoi S, Yamaue H, Kato K, Takahashi S, Hirono S, Takeda S, et al. Role of adjuvant surgery for patients with initially unresectable pancreatic cancer with a long-term favorable response to non-surgical anti-cancer treatments: results of a project study for pancreatic surgery by the Japanese Society of Hepato-Biliary-Pancreatic Surgery. J Hepatobiliary Pancreat Sci. 2013;20:590–600.CrossRefGoogle Scholar
  14. 14.
    Opendro SS, Satoi S, Yanagimoto H, Yamamoto T, Toyokawa H, Hirooka S, et al. Role of adjuvant surgery in initially unresectable pancreatic cancer after long-term chemotherapy or chemoradiation therapy: survival benefit? J Hepatobiliary Pancreat Sci. 2014;21:695–702.CrossRefGoogle Scholar
  15. 15.
    Wanebo HJ, Glicksman AS, Vezeridis MP, Clark J, Tibbetts L, Koness RJ, et al. Preoperative chemotherapy, radiotherapy, and surgical resection of locally advanced pancreatic cancer. Arch Surg. 2000;135:81–7.CrossRefGoogle Scholar
  16. 16.
    Strobel O, Berens V, Hinz U, Hartwig W, Hackert T, Bergmann F, et al. Resection after neoadjuvant therapy for locally advanced, “unresectable” pancreatic cancer. Surgery. 2012;152:S33–42.CrossRefGoogle Scholar
  17. 17.
    Ueno H, Ioka T, Ikeda M, Ohkawa S, Yanagimoto H, Boku N, et al. Randomized phase III study of gemcitabine plus S-1, S-1 alone, or gemcitabine alone in patients with locally advanced and metastatic pancreatic cancer in Japan and Taiwan: GEST study. J Clin Oncol. 2013;31:1640–8.CrossRefGoogle Scholar
  18. 18.
    Marthey L, Sa-Cunha A, Blanc JF, Gauthier M, Cueff A, Francois E, et al. FOLFIRINOX for locally advanced pancreatic adenocarcinoma: results of an AGEO multicenter prospective observational cohort. Ann Surg Oncol. 2015;22:295–301.CrossRefGoogle Scholar
  19. 19.
    Suker M, Beumer BR, Sadot E, Marthey L, Faris JE, Mellon EA, et al. FOLFIRINOX for locally advanced pancreatic cancer: a systematic review and patient-level meta-analysis. Lancet Oncol. 2016;17:801–10.CrossRefGoogle Scholar
  20. 20.
    Okusaka T, Ikeda M, Fukutomi A, Ioka T, Furuse J, Ohkawa S, et al. Phase II study of FOLFIRINOX for chemotherapy-naive Japanese patients with metastatic pancreatic cancer. Cancer Sci. 2014;105:1321–6.CrossRefGoogle Scholar
  21. 21.
    Ueno H, Ikeda M, Ueno M, Mizuno N, Ioka T, Omuro Y, et al. Phase I/II study of nab-paclitaxel plus gemcitabine for chemotherapy-naive Japanese patients with metastatic pancreatic cancer. Cancer Chemother Pharmacol. 2016;77:595–603.CrossRefGoogle Scholar
  22. 22.
    Tempero M. NCCN Guidelines version 2.2018 Pancreatic adenocarcinoma. https://www.nccn.org/professionals/physician_gls/default.aspx Accessed 1 Nov 2018
  23. 23.
    Yamaguchi K, Okusaka T, Shimizu K, Furuse J, Ito Y, Hanada K, et al. Clinical practice guidelines for pancreatic cancer 2016 from the Japan pancreas society: a synopsis. Pancreas. 2017;46:595–604.CrossRefGoogle Scholar
  24. 24.
    Sudo K, Yamaguchi T, Ishihara T, Nakamura K, Hara T, Denda T, et al. Phase II study of oral S-1 and concurrent radiotherapy in patients with unresectable locally advanced pancreatic cancer. Int J Radiat Oncol Biol Phys. 2011;80:119–25.CrossRefGoogle Scholar
  25. 25.
    Shinchi H, Maemura K, Mataki Y, Kurahara H, Sakoda M, Ueno S, et al. A phase II study of oral S-1 with concurrent radiotherapy followed by chemotherapy with S-1 alone for locally advanced pancreatic cancer. J Hepatobiliary Pancreat Sci. 2012;19:152–8.CrossRefGoogle Scholar
  26. 26.
    Ikeda M, Ioka T, Ito Y, Yonemoto N, Nagase M, Yamao K, et al. A multicenter phase II trial of S-1 with concurrent radiation therapy for locally advanced pancreatic cancer. Int J Radiat Oncol Biol Phys. 2013;85:163–9.CrossRefGoogle Scholar
  27. 27.
    Nakachi K, Furuse J, Kinoshita T, Kawashima M, Ishii H, Ikeda M, et al. A phase II study of induction chemotherapy with gemcitabine plus S-1 followed by chemoradiotherapy for locally advanced pancreatic cancer. Cancer Chemother Pharmacol. 2010;66:527–34.CrossRefGoogle Scholar
  28. 28.
    Goldstein D, Spry N, Cummins MM, Brown C, van Hazel GA, Carroll S, et al. The GOFURTGO Study: AGITG Phase II Study of fixed dose rate gemcitabine–oxaliplatin integrated with concomitant 5FU and 3-D conformal radiotherapy for the treatment of localised pancreatic cancer. Br J Cancer. 2011;106:61–9.CrossRefGoogle Scholar
  29. 29.
    Schellenberg D, Kim J, Christman-Skieller C, Chun CL, Columbo LA, Ford JM, et al. Single-fraction stereotactic body radiation therapy and sequential gemcitabine for the treatment of locally advanced pancreatic cancer. Int J Radiat Oncol Biol Phys. 2011;81:181–8.CrossRefGoogle Scholar
  30. 30.
    Ben-Josef E, Schipper M, Francis IR, Hadley S, Ten-Haken R, Lawrence T, et al. A phase I/II trial of intensity modulated radiation (IMRT) dose escalation with concurrent fixed-dose rate gemcitabine (FDR-G) in patients with unresectable pancreatic cancer. Int J Radiat Oncol Biol Phys. 2012;84:1166–71.CrossRefGoogle Scholar
  31. 31.
    Kawashiro S, Yamada S, Okamoto M, Ohno T, Nakano T, Shinoto M, et al. Multi-institutional study of carbon-ion radiotherapy for locally advanced pancreatic cancer: Japan carbon-ion radiation oncology study group (J-CROS) study 1403 pancreas. Int J Radiat Oncol Biol Phys. 2018;101:1212–21.CrossRefGoogle Scholar
  32. 32.
    Hammel P, Huguet F, van Laethem JL, Goldstein D, Glimelius B, Artru P, et al. Effect of chemoradiotherapy vs chemotherapy on survival in patients with locally advanced pancreatic cancer controlled after 4 Months of gemcitabine with or without erlotinib: The LAP07 randomized clinical trial. JAMA. 2016;315:1844–53.CrossRefGoogle Scholar
  33. 33.
    Gillen S, Schuster T, Meyer Zum Buschenfelde C, Friess H, Kleeff J. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med. 2010; 7: e1000267.Google Scholar
  34. 34.
    Bickenbach KA, Gonen M, Tang LH, O'Reilly E, Goodman K, Brennan MF, et al. Downstaging in pancreatic cancer: a matched analysis of patients resected following systemic treatment of initially locally unresectable disease. Ann Surg Oncol. 2012;19:1663–9.CrossRefGoogle Scholar
  35. 35.
    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.CrossRefGoogle Scholar
  36. 36.
    Hosein PJ, Macintyre J, Kawamura C, Maldonado JC, Ernani V, Loaiza-Bonilla A, et al. A retrospective study of neoadjuvant FOLFIRINOX in unresectable or borderline-resectable locally advanced pancreatic adenocarcinoma. BMC Cancer. 2012;12:199.CrossRefGoogle Scholar
  37. 37.
    Faris JE, Blaszkowsky LS, McDermott S, Guimaraes AR, Szymonifka J, Huynh MA, et al. FOLFIRINOX in locally advanced pancreatic cancer: the Massachusetts General Hospital Cancer Center experience. Oncologist. 2013;18:543–8.CrossRefGoogle Scholar
  38. 38.
    Boone BA, Steve J, Krasinskas AM, Zureikat AH, Lembersky BC, Gibson MK, et al. Outcomes with FOLFIRINOX for borderline resectable and locally unresectable pancreatic cancer. J Surg Oncol. 2013;108:236–41.CrossRefGoogle Scholar
  39. 39.
    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.CrossRefGoogle Scholar
  40. 40.
    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.CrossRefGoogle Scholar
  41. 41.
    Nitsche U, Wenzel P, Siveke JT, Braren R, Holzapfel K, Schlitter AM, et al. Resectability after first-line FOLFIRINOX in initially unresectable locally advanced pancreatic cancer: a single-center experience. Ann Surg Oncol. 2015;22(Suppl 3):S1212–S12201220.CrossRefGoogle Scholar
  42. 42.
    Khushman M, Dempsey N, Maldonado JC, Loaiza-Bonilla A, Velez M, Carcas L, et al. Full dose neoadjuvant FOLFIRINOX is associated with prolonged survival in patients with locally advanced pancreatic adenocarcinoma. Pancreatology. 2015;15:667–73.CrossRefGoogle Scholar
  43. 43.
    Wagner M, Antunes C, Pietrasz D, Cassinotto C, Zappa M, Sa Cunha A, et al. CT evaluation after neoadjuvant FOLFIRINOX chemotherapy for borderline and locally advanced pancreatic adenocarcinoma. Eur Radiol. 2017;27:3104–16.CrossRefGoogle Scholar
  44. 44.
    Lakatos G, Petranyi A, Szucs A, Nehez L, Harsanyi L, Hegyi P, et al. Efficacy and safety of FOLFIRINOX in locally advanced pancreatic cancer. A single center experience. Pathol Oncol Res. 2017; 23: 753-9.Google Scholar
  45. 45.
    Michelakos T, Pergolini I, Castillo CF, Honselmann KC, Cai L, Deshpande V, et al. Predictors of resectability and survival in patients with borderline and locally advanced pancreatic cancer who underwent neoadjuvant treatment with FOLFIRINOX. Ann Surg. 2017.  https://doi.org/10.1097/SLA.0000000000002600.Google Scholar
  46. 46.
    Marchegiani G, Todaro V, Boninsegna E, Negrelli R, Sureka B, Bonamini D, et al. Surgery after FOLFIRINOX treatment for locally advanced and borderline resectable pancreatic cancer: increase in tumour attenuation on CT correlates with R0 resection. Eur Radiol. 2018;28:4265–73.CrossRefGoogle Scholar
  47. 47.
    Barenboim A, Lahat G, Geva R, Nachmany I, Nakache R, Goykhman Y, et al. Neoadjuvant FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer: An intention to treat analysis. Eur J Surg Oncol. 2018;44:1619–23.CrossRefGoogle Scholar
  48. 48.
    Chapman BC, Gleisner A, Rigg D, Messersmith W, Paniccia A, Meguid C, et al. Perioperative and survival outcomes following neoadjuvant FOLFIRINOX versus gemcitabine abraxane in patients with pancreatic adenocarcinoma. JOP. 2018;19:75–85.Google Scholar
  49. 49.
    Takahashi H, Akita H, Tomokuni A, Kobayashi S, Ohigashi H, Fijiwara Y, et al. Preoperative gemcitabine-based chemoradiation therapy for borderline resectable pancreatic cancer: impact of venous and arterial involvement status on surgical outcome and pattern of recurrence. Ann Surg. 2016;264:1091–7.CrossRefGoogle Scholar
  50. 50.
    Jang JY, Han Y, Lee H, Kim SW, Kwon W, Lee KH, et al. Oncological benefits of neoadjuvant chemoradiation with gemcitabine versus upfront surgery in patients with borderline resectable pancreatic cancer: a prospective, randomized, open-label, multicenter phase 2/3 trial. Ann Surg. 2018;268:215–22.CrossRefGoogle Scholar
  51. 51.
    Strobel O, Neoptolemos J, Jager D, Bucheler MW. Optimizing the outcomes of pancreatic cancer surgery. Nat Rev Clin Oncol. 2019;16:11–26.CrossRefGoogle Scholar
  52. 52.
    Shrikhande SV, Kleeff J, Reiser C, Weitz J, Hinz U, Esposito I, et al. Pancreatic resection for M1 pancreatic ductal adenocarcinoma. Ann Surg Oncol. 2007;14:118–27.CrossRefGoogle Scholar
  53. 53.
    Gleisner AL, Assumpcao L, Cameron JL, Wolfgang CL, Choti MA, Herman JM, et al. Is resection of periampullary or pancreatic adenocarcinoma with synchronous hepatic metastasis justified? Cancer. 2007;110:2484–92.CrossRefGoogle Scholar
  54. 54.
    Dunschede F, Will L, von Langsdorf C, Mohler M, Galle PR, Otto G, et al. Treatment of metachronous and simultaneous liver metastases of pancreatic cancer. Eur Surg Res. 2010;44:209–13.CrossRefGoogle Scholar
  55. 55.
    Tachezy M, Gebauer F, Janot M, Uhl W, Zerbi A, Montorsi M, et al. Synchronous resections of hepatic oligometastatic pancreatic cancer: disputing a principle in a time of safe pancreatic operations in a retrospective multicenter analysis. Surgery. 2016;160:136–44.CrossRefGoogle Scholar
  56. 56.
    Bellon E, Gebauer F, Tachezy M, Izbicki JR, Bockhorn M. Pancreatic cancer and liver metastases: state of the art. Updates Surg. 2016;68:247–51.CrossRefGoogle Scholar
  57. 57.
    Sohal DPS, Kennedy EB, Khorana A, Copur MS, Crane CH, Garrido-Laguna I, et al. Metastatic pancreatic cancer: ASCO clinical practice guideline update. J Clin Oncol. 2018;36:2545–56.CrossRefGoogle Scholar
  58. 58.
    Sohal DP, Mangu PB, Khorana AA, Shah MA, Philip PA, O'Reilly EM, et al. Metastatic pancreatic cancer: American society of clinical oncology clinical practice guideline. J Clin Oncol. 2016;34:2784–96.CrossRefGoogle Scholar
  59. 59.
    Schneitler S, Kropil P, Riemer J, Antoch G, Knoefel WT, Haussinger D, et al. Metastasized pancreatic carcinoma with neoadjuvant FOLFIRINOX therapy and R0 resection. World J Gastroenterol. 2015;21:6384–90.CrossRefGoogle Scholar
  60. 60.
    Shimura M, Mizuma M, Hayashi H, Mori A, Tachibana T, Hata T, et al. A long-term survival case treated with conversion surgery following chemotherapy after diagnostic metastasectomy for pancreatic cancer with synchronous liver metastasis. Surg Case Rep. 2017;3:132.CrossRefGoogle Scholar
  61. 61.
    Wright GP, Poruk KE, Zenati MS, Steve J, Bahary N, Hogg ME, et al. Primary tumor resection following favorable response to systemic chemotherapy in stage IV pancreatic adenocarcinoma with synchronous metastases: a bi-institutional analysis. J Gastrointest Surg. 2016;20:1830–5.CrossRefGoogle Scholar
  62. 62.
    Frigerio I, Regi P, Giardino A, Scopelliti F, Girelli R, Bassi C, et al. Downstaging in stage IV pancreatic cancer: a new population eligible for surgery? Ann Surg Oncol. 2017;24:2397–403.CrossRefGoogle Scholar
  63. 63.
    Satoi S, Fujii T, Yanagimoto H, Motoi F, Kurata M, Takahara N, et al. Multicenter phase II study of intravenous and intraperitoneal paclitaxel with S-1 for pancreatic ductal adenocarcinoma patients with peritoneal metastasis. Ann Surg. 2017;265:397–401.CrossRefGoogle Scholar
  64. 64.
    Ielpo B, Duran H, Diaz E, Fabra I, Caruso R, Ferri V, et al. Preoperative treatment with gemcitabine plus nab-paclitaxel is a safe and effective chemotherapy for pancreatic adenocarcinoma. Eur J Surg Oncol. 2016;42:1394–400.CrossRefGoogle Scholar
  65. 65.
    Ielpo B, Caruso R, Duran H, Diaz E, Fabra I, Malave L, et al. A comparative study of neoadjuvant treatment with gemcitabine plus nab-paclitaxel versus surgery first for pancreatic adenocarcinoma. Surg Oncol. 2017;26:402–10.CrossRefGoogle Scholar
  66. 66.
    Dhir M, Zenati MS, Hamad A, Singhi AD, Bahary N, Hogg ME, et al. FOLFIRINOX versus gemcitabine/nab-Paclitaxel for neoadjuvant treatment of resectable and borderline resectable pancreatic head adenocarcinoma. Ann Surg Oncol. 2018.  https://doi.org/10.1245/s10434-018-6512-8.Google Scholar
  67. 67.
    Rombouts SJ, Walma MS, Vogel JA, van Rijssen LB, Wilmink JW, Mohammad NH, et al. Systematic review of resection rates and clinical outcomes after FOLFIRINOX-based treatment in patients with locally advanced pancreatic cancer. Ann Surg Oncol. 2016;23:4352–60.CrossRefGoogle Scholar
  68. 68.
    Kim SS, Nakakura EK, Wang ZJ, Kim GE, Corvera CU, Harris HW, et al. Preoperative FOLFIRINOX for borderline resectable pancreatic cancer: is radiation necessary in the modern era of chemotherapy? J Surg Oncol. 2016;114:587–96.CrossRefGoogle Scholar
  69. 69.
    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;147:753–60.CrossRefGoogle Scholar
  70. 70.
    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;10:511–8.CrossRefGoogle Scholar
  71. 71.
    Eguchi H, Yamada D, Iwagami Y, Gotoh K, Kawamoto K, Wada H, et al. Prolonged neoadjuvant therapy for locally advanced pancreatic cancer. Dig Surg. 2018;35:70–6.CrossRefGoogle Scholar
  72. 72.
    Asano T, Hirano S, Nakamura T, Okamura K, Tsuchikawa T, Noji T, et al. Survival benefit of conversion surgery for patients with initially unresectable pancreatic cancer who responded favorably to nonsurgical treatment. J Hepatobiliary Pancreat Sci. 2018;25:342–50.CrossRefGoogle Scholar
  73. 73.
    Gemenetzis G, Groot VP, Blair AB, Laheru DA, Zheng L, Narang AK, et al. Survival in locally advanced pancreatic cancer after neoadjuvant therapy and surgical resection. Ann Surg. 2018.Google Scholar
  74. 74.
    Duwe G, Knitter S, Pesthy S, Beierle AS, Bahra M, Schmelzle M, et al. Hepatotoxicity following systemic therapy for colorectal liver metastases and the impact of chemotherapy-associated liver injury on outcomes after curative liver resection. Eur J Surg Oncol. 2017;43:1668–811.CrossRefGoogle Scholar
  75. 75.
    Almadi MA, Barkun A, Martel M. Plastic vs. self-Expandable metal stents for palliation in malignant biliary obstruction: a series of meta-analyses. Am J Gastroenterol. 2017; 112: 260-73.Google Scholar
  76. 76.
    Crippa S, Cirocchi R, Partelli S, Petrone MC, Muffatti F, Renzi C, et al. Systematic review and meta-analysis of metal versus plastic stents for preoperative biliary drainage in resectable periampullary or pancreatic head tumors. Eur J Surg Oncol. 2016;42:1278–85.CrossRefGoogle Scholar
  77. 77.
    Kitahata Y, Kawai M, Tani M, Hirono S, Okada K, Miyazawa M, et al. Preoperative cholangitis during biliary drainage increases the incidence of postoperative severe complications after pancreaticoduodenectomy. Am J Surg. 2014;208:1–10.CrossRefGoogle Scholar
  78. 78.
    Abou-Khalil J, Rocha FG. Surgical strategies and novel therapies for locally advanced pancreatic cancer. J Surg Oncol. 2017;116:16–24.CrossRefGoogle Scholar
  79. 79.
    Miyazaki M, Itoh H, Kaiho T, Ambiru S, Togawa A, Sasada K, et al. Portal vein reconstruction at the hepatic hilus using a left renal vein graft. J Am Coll Surg. 1995;180:497–8.Google Scholar
  80. 80.
    Suzuki T, Yoshidome H, Kimura F, Shimizu H, Ohtsuka M, Kato A, et al. Renal function is well maintained after use of left renal vein graft for vascular reconstruction in hepatobiliary-pancreatic surgery. J Am Coll Surg. 2006;202:87–92.CrossRefGoogle Scholar
  81. 81.
    Yoshitomi H, Kato A, Shimizu H, Ohtsuka M, Furukawa K, Takayashiki T, et al. Tips and tricks of surgical technique for pancreatic cancer: portal vein resection and reconstruction (with videos). J Hepatobiliary Pancreat Sci. 2014;21:E69–74.CrossRefGoogle Scholar
  82. 82.
    Smoot RL, Christein JD, Farnell MB. An innovative option for venous reconstruction after pancreaticoduodenectomy: the left renal vein. J Gastrointest Surg. 2007;11:425–31.CrossRefGoogle Scholar
  83. 83.
    Choi SH, Hwang HK, Kang CM, Lee WJ. Potential use of left renal vein graft in pancreaticoduodenectomy combined with long segmental resection of the superior mesenteric-splenic-portal vein confluence. JOP. 2011;12:234–40.Google Scholar
  84. 84.
    Tran TB, Mell MW, Poultsides GA. An untapped resource: left renal vein interposition graft for portal vein reconstruction during pancreaticoduodenectomy. Dig Dis Sci. 2017;62:68–71.CrossRefGoogle Scholar
  85. 85.
    Nakao A, Takeda S, Inoue S, Nomoto S, Kanazumi N, Sugimoto H, et al. Indications and techniques of extended resection for pancreatic cancer. World J Surg. 2006;30:976–82.CrossRefGoogle Scholar
  86. 86.
    Bockhorn M, Burdelski C, Bogoevski D, Sgourakis G, Yekebas EF, Izbicki JR. Arterial en bloc resection for pancreatic carcinoma. Br J Surg. 2011;98:86–92.CrossRefGoogle Scholar
  87. 87.
    Mollberg N, Rahbari NN, Koch M, Hartwig W, Hoeger Y, Buchler MW, et al. Arterial resection during pancreatectomy for pancreatic cancer: a systematic review and meta-analysis. Ann Surg. 2011;254:882–93.CrossRefGoogle Scholar
  88. 88.
    Jegatheeswaran S, Baltatzis M, Jamdar S, Siriwardena AK. Superior mesenteric artery (SMA) resection during pancreatectomy for malignant disease of the pancreas: a systematic review. HPB (Oxford). 2017;19:483–90.CrossRefGoogle Scholar
  89. 89.
    Hirano S, Kondo S, Hara T, Ambo Y, Tanaka E, Shichinohe T, et al. Distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic body cancer: long-term results. Ann Surg. 2007;246:46–51.CrossRefGoogle Scholar
  90. 90.
    Klompmaker S, de Rooij T, Korteweg JJ, van Dieren S, van Lienden KP, van Gulik TM, et al. Systematic review of outcomes after distal pancreatectomy with coeliac axis resection for locally advanced pancreatic cancer. Br J Surg. 2016;103:941–9.CrossRefGoogle Scholar
  91. 91.
    Baumgartner JM, Krasinskas A, Daouadi M, Zureikat A, Marsh W, Lee K, et al. Distal pancreatectomy with en bloc celiac axis resection for locally advanced pancreatic adenocarcinoma following neoadjuvant therapy. J Gastrointest Surg. 2012;16:1152–9.CrossRefGoogle Scholar
  92. 92.
    Nakamura T, Hirano S, Noji T, Asano T, Okamura K, Tsuchikawa T, et al. Distal pancreatectomy with en bloc celiac axis resection (modified appleby procedure) for locally advanced pancreatic body cancer: a single-center review of 80 consecutive patients. Ann Surg Oncol. 2016;23:969–75.CrossRefGoogle Scholar
  93. 93.
    Amano R, Kimura K, Nakata B, Yamazoe S, Motomura H, Yamamoto A, et al. Pancreatectomy with major arterial resection after neoadjuvant chemoradiotherapy gemcitabine and S-1 and concurrent radiotherapy for locally advanced unresectable pancreatic cancer. Surgery. 2015;158:191–200.CrossRefGoogle Scholar
  94. 94.
    Glebova NO, Hicks CW, Tosoian JJ, Piazza KM, Abularrage CJ, Schulick RD, et al. Outcomes of arterial resection during pancreatectomy for tumor. J Vasc Surg. 2016;63:722–9.CrossRefGoogle Scholar
  95. 95.
    Perinel J, Nappo G, El Bechwaty M, Walter T, Hervieu V, Valette PJ, et al. Locally advanced pancreatic duct adenocarcinoma: pancreatectomy with planned arterial resection based on axial arterial encasement. Langenbecks Arch Surg. 2016;401:1131–42.CrossRefGoogle Scholar
  96. 96.
    Hartwig W, Gluth A, Hinz U, Koliogiannis D, Strobel O, Hackert T, et al. Outcomes after extended pancreatectomy in patients with borderline resectable and locally advanced pancreatic cancer. Br J Surg. 2016;103:1683–94.CrossRefGoogle Scholar
  97. 97.
    Miyazaki M, Yoshitomi H, Takano S, Shimizu H, Kato A, Yoshidome H, et al. Combined hepatic arterial resection in pancreatic resections for locally advanced pancreatic cancer. Langenbecks Arch Surg. 2017.Google Scholar
  98. 98.
    Bachellier P, Addeo P, Faitot F, Nappo G, Dufour P. Pancreatectomy with arterial resection for pancreatic adenocarcinoma: how can it be done safely and with which outcomes?: a single institution's experience with 118 patients. Ann Surg. 2018.  https://doi.org/10.1097/SLA.0000000000003010.Google Scholar
  99. 99.
    Cassinotto C, Cortade J, Belleannee G, Lapuyade B, Terrebonne E, Vendrely V, et al. An evaluation of the accuracy of CT when determining resectability of pancreatic head adenocarcinoma after neoadjuvant treatment. Eur J Radiol. 2013;82:589–93.CrossRefGoogle Scholar
  100. 100.
    Reni M, Zanon S, Balzano G, Nobile S, Pircher CC, Chiaravalli M, et al. Selecting patients for resection after primary chemotherapy for non-metastatic pancreatic adenocarcinoma. Ann Oncol. 2017;28:2786–92.CrossRefGoogle Scholar
  101. 101.
    Williams JL, Kadera BE, Nguyen AH, Muthusamy VR, Wainberg ZA, Hines OJ, et al. CA19-9 normalization during pre-operative treatment predicts longer survival for patients with locally progressed pancreatic cancer. J Gastrointest Surg. 2016;20:1331–422.CrossRefGoogle Scholar
  102. 102.
    Akita H, Takahashi H, Ohigashi H, Tomokuni A, Kobayashi S, Sugimura K, et al. FDG-PET predicts treatment efficacy and surgical outcome of pre-operative chemoradiation therapy for resectable and borderline resectable pancreatic cancer. Eur J Surg Oncol. 2017;43:1061–7.CrossRefGoogle Scholar
  103. 103.
    Barreto SG, Loveday B, Windsor JA, Pandanaboyana S. Detecting tumour response and predicting resectability after neoadjuvant therapy for borderline resectable and locally advanced pancreatic cancer. ANZ J Surg. 2018.  https://doi.org/10.1111/ans.14764.Google Scholar
  104. 104.
    Kim SS, Ko AH, Nakakura EK, Wang ZJ, Corvera CU, Harris HW, et al. Comparison of tumor regression grading of residual pancreatic ductal adenocarcinoma following neoadjuvant chemotherapy without radiation: would fewer tier-stratification be favorable toward standardization? Am J Surg Pathol. 2018.  https://doi.org/10.1097/PAS.0000000000001152.Google Scholar
  105. 105.
    He J, Blair AB, Groot VP, Javed AA, Burkhart RA, Gemenetzis G, et al. Is a pathological complete response following neoadjuvant chemoradiation associated with prolonged survival in patients with pancreatic cancer? Ann Surg. 2018.  https://doi.org/10.1097/SLA.0000000000002672.Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Department of General SurgeryChiba University, Graduate School of MedicineChibaJapan

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