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Surgical Endoscopy

, Volume 30, Issue 5, pp 1999–2010 | Cite as

Safety and feasibility of laparoscopic liver resection with associated lymphadenectomy for intrahepatic cholangiocarcinoma: a propensity score-based case-matched analysis from a single institution

  • Francesca RattiEmail author
  • Federica Cipriani
  • Riccardo Ariotti
  • Annalisa Gagliano
  • Michele Paganelli
  • Marco Catena
  • Luca Aldrighetti
Article

Abstract

Background

Intrahepatic cholangiocarcinoma (ICC) is still a relatively uncommon indication for laparoscopic surgery because of technical challenges related to the frequent need for major hepatectomies and the necessity to perform formal regional lymphadenectomy. The aim of the present case-matched study was to compare laparoscopic and open resections for ICC.

Methods

In a case-matched retrospective analysis, 20 consecutive patients who had undergone laparoscopic resection for ICC (LPS group) were compared with 60 of 83 patients who had undergone open surgery (open group) in the same institution. The groups were matched in a ratio of 1:3 using propensity scores based on covariates representing relevant patient characteristics and severity of disease. The main endpoints were short- and long-term outcomes and impact and adequacy of laparoscopic lymphadenectomy.

Results

The groups were well matched in terms of patient and disease characteristics. The laparoscopic approach resulted in less blood loss (200 vs. 350 mL, p = 0.040) despite less extensive use of the Pringle maneuver. There was no difference in perioperative morbidity and mortality rates; however, the laparoscopic approach was associated with faster functional recovery (median 3 vs. 4 days, p = 0.050). After a mean follow-up of 39 months, disease-free and overall survivals were 33 and 51 months, respectively, for the LPS and 36 and 63, respectively, for the open group (p ns). The number of harvested nodes was comparable between groups.

Conclusions

Compared with open surgery, laparoscopic resection of ICC is feasible and safe, providing short-term benefits without negatively affecting oncologic adequacy in terms of rate of R0 resections, depth of margins, and long-term overall and disease-free survivals. Laparoscopic regional lymphadenectomy is technically possible but should be the object of future focused studies.

Keywords

Laparoscopy Minimally invasive Intrahepatic cholangiocarcinoma Lymphadenectomy New technique Liver resection 

Abbreviations

ICC

Intrahepatic cholangiocarcinoma

LPS

Laparoscopic

LND

Lymphadenectomy

ASA

American Society of Anesthesiology

CT

Computed tomography

MRI

Magnetic resonance imaging

CEA

Carcinoembryonic antigen

OS

Overall survival

DFS

Disease-free survival

Notes

Acknowledgments

English language revision was made by Edanz Group Global Ltd.

Author contribution

Study design: Ratti, Aldrighetti; acquisition of data: Ariotti, Gagliano; analysis and interpretation: Ratti, Aldrighetti; manuscript drafted by: Ratti, Ariotti; revision: Cipriani, Catena, Paganelli, Gagliano; statistical advice: Paganelli, Catena.

Compliance with ethical standard

Disclosure

The material has not been previously published or submitted elsewhere for publication and will not be sent to another journal until a decision is made concerning publication. All listed authors have participated in the study and have approved the final manuscript. Francesca Ratti, Riccardo Ariotti, Annalisa Gagliano, Federica Cipriani, Michele Paganelli, Marco Catena, and Luca Aldrighetti have no personal conflicts of interest or financial disclosure.

References

  1. 1.
    Nakeeb A, Pitt HA, Sohn TA, Coleman J, Abrams RA, Piantadosi S, Hruban RH, Lillemoe KD, Yeo CJ, Cholangiocarcinoma Cameron JL (1996) A spectrum of intrahepatic, perihilar, and distal tumors. Ann Surg 224(4):463–473CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Khan SA, Toledano MB, Taylor-Robinson SD (2008) Epidemiology, risk factors, and pathogenesis of cholangiocarcinoma. HPB (Oxford) 10(2):77–82CrossRefGoogle Scholar
  3. 3.
    Ribero D, Pinna AD, Guglielmi A, Ponti A, Nuzzo G, Giulini SM, Aldrighetti L, Calise F, Gerunda GE, Tomatis M, Amisano M, Berloco P, Torzilli G, Capussotti L, Italian Intrahepatic Cholangiocarcinoma Study Group (2012) Surgical approach for long-term survival of patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis of 434 patients. Arch Surg 147(12):1107–1113CrossRefPubMedGoogle Scholar
  4. 4.
    de Jong MC, Nathan H, Sotiropoulos GC, Paul A, Alexandrescu S, Marques H, Pulitano C, Barroso E, Clary BM, Aldrighetti L, Ferrone CR, Zhu AX, Bauer TW, Walters DM, Gamblin TC, Nguyen KT, Turley R, Popescu I, Hubert C, Meyer S, Schulick RD, Choti MA, Gigot JF, Mentha G, Pawlik TM (2011) Intrahepatic cholangiocarcinoma: an international multi-institutional analysis of prognostic factors and lymph node assessment. J Clin Oncol 29(23):3140–3145CrossRefPubMedGoogle Scholar
  5. 5.
    Bridgewater J, Galle PR, Khan SA, Llovet JM, Park JW, Patel T, Pawlik TM, Gores GJ (2014) Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. J Hepatol 60(6):1268–1289CrossRefPubMedGoogle Scholar
  6. 6.
    Amini N, Ejaz A, Spolverato G, Maithel SK, Kim Y, Pawlik TM (2014) Management of lymph nodes during resection of hepatocellular carcinoma and intrahepatic cholangiocarcinoma: a systematic review. J Gastrointest Surg 18(12):2136–2148CrossRefPubMedGoogle Scholar
  7. 7.
    Brown KM, Parmar AD, Geller DA (2014) Intrahepatic cholangiocarcinoma. Surg Oncol Clin N Am 23(2):231–246CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Mavros MN, Economopoulos KP, Alexiou VG, Pawlik TM (2014) Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: systematic review and meta-analysis. JAMA Surg. doi: 10.1001/jamasurg.2013.5137 PubMedGoogle Scholar
  9. 9.
    Spolverato G, Ejaz A, Kim Y, Sotiropoulos GC, Pau A, Alexandrescu S, Marques H, Pulitano C, Barroso E, Clary BM, Aldrighetti L, Bauer TW, Walters DM, Groeschl R, Gamblin TC, Marsh W, Nguyen KT, Turley R, Popescu I, Hubert C, Meyer S, Gigot JF, Mentha G, Pawlik TM (2014) Tumor size predicts vascular invasion and histologic grade among patients undergoing resection of intrahepatic cholangiocarcinoma. J Gastrointest Surg 18(7):1284–1291CrossRefPubMedGoogle Scholar
  10. 10.
    Uchiyama K, Yamamoto M, Yamaue H, Ariizumi S, Aoki T, Kokudo N, Ebata T, Nagino M, Ohtsuka M, Miyazaki M, Tanaka E, Kondo S, Uenishi T, Kubo S, Yoshida H, Unno M, Imura S, Shimada M, Ueno M, Takada T (2011) Impact of nodal involvement on surgical outcomes of intrahepatic cholangiocarcinoma: a multicenter analysis by the Study Group for Hepatic Surgery of the Japanese Society of Hepato-Biliary-Pancreatic Surgery. J Hepatobiliary Pancreat Sci 18(3):443–452CrossRefPubMedGoogle Scholar
  11. 11.
    Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Conci S, Valdegamberi A, Sandri M, Iacono C (2011) Prognostic significance of lymph node ratio after resection of peri-hilar cholangiocarcinoma. HPB (Oxford) 13(4):240–245CrossRefGoogle Scholar
  12. 12.
    Nguyen KT, Steel J, Vanounou T, Tsung A, Marsh JW, Geller DA, Gamblin TC (2009) Initial presentation and management of hilar and peripheral cholangiocarcinoma: is a node-positive status or potential margin-positive result a contraindication to resection? Ann Surg Oncol 16(12):3308–3315CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Ruys AT, Kate FJ, Busch OR, Engelbrecht MR, Gouma DJ, van Gulik TM (2011) Metastatic lymph nodes in hilar cholangiocarcinoma: does size matter? HPB (Oxford) 13(12):881–886CrossRefGoogle Scholar
  14. 14.
    Nguyen KT, Gamblin TC, Geller DA (2009) World review of laparoscopic liver resection-2,804 patients. Ann Surg 250(5):831–841CrossRefPubMedGoogle Scholar
  15. 15.
    Aldrighetti L, Cipriani F, Ratti F, Casciola L, Calise F, on behalf of the Italian National Survey Study Group (2013) The Italian experience in minimally invasive surgery of the liver: A national survey. In: Calise F, Casciola L (eds) minimally invasive surgery of the liver. Springer, Italia, pp 295–312CrossRefGoogle Scholar
  16. 16.
    Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS, World Consensus Conference on Laparoscopic Surgery (2009) The international position on laparoscopic liver surgery: the Louisville Statement, 2008. Ann Surg 250(5):825–830CrossRefPubMedGoogle Scholar
  17. 17.
    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, O’Rourke N, Tanabe M, Koffron AJ, Tsung A, Soubrane O, Machado MA, Gayet B, Troisi RI, Pessaux P, Van Dam RM, Scatton O, Abu Hilal M, Belli G, Kwon CH, Edwin B, Choi GH, Aldrighetti LA, Cai X, Cleary S, Chen KH, Schön MR, Sugioka A, Tang CN, Herman P, Pekolj J, Chen XP, Dagher I, Jarnagin W, Yamamoto M, Strong R, Jagannath P, Lo CM, Clavien PA, Kokudo N, Barkun J, Strasberg SM (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261(4):619–629PubMedGoogle Scholar
  18. 18.
    Belghiti J, Clavien PA, Gadzijev E (2000) The Brisbane 2000 terminology of liver anatomy and resections. HPB 2:333–339Google Scholar
  19. 19.
    Aldrighetti L, Pulitanò C, Arru M, Catena M, Guzzetti E, Casati M, Ferla G (2008) Ultrasonic-mediated laparoscopic liver transection. Am J Surg 195(2):270–272CrossRefPubMedGoogle Scholar
  20. 20.
    Gumbs AA, Jarufe N, Gayet B (2013) Minimally invasive approaches to extrapancreatic cholangiocarcinoma. Surg Endosc 27(2):406–414CrossRefPubMedGoogle Scholar
  21. 21.
    Edge SB (2009) Intrahepatic bile ducts. In: Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (eds) AJCC cancer staging manual, 7th edn. Springer, New York, pp 201–210Google Scholar
  22. 22.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Aldrighetti L, Guzzetti E, Pulitanò C, Cipriani F, Catena M, Paganelli M, Ferla G (2010) Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol 102(1):82–86CrossRefPubMedGoogle Scholar
  24. 24.
    Pulitanò C, Aldrighetti L (2008) The current role of laparoscopic liver resection for the treatment of liver tumors. Nat Clin Pract Gastroenterol Hepatol 5(11):648–654CrossRefPubMedGoogle Scholar
  25. 25.
    Pulitanò C, Catena M, Arru M, Guzzetti E, Comotti L, Ferla G, Aldrighetti L (2008) Laparoscopic liver resection without portal clamping: a prospective evaluation. Surg Endosc 22(10):2196–2200CrossRefPubMedGoogle Scholar
  26. 26.
    Pulitanò C, Catena M, Finazzi R, Aldrighetti L (2008) Efficacy of methylprednisolone in reducing ischemia-reperfusion injury in steatosic liver. Am J Surg 195(3):418CrossRefPubMedGoogle Scholar
  27. 27.
    Orci LA, Toso C, Mentha G, Morel P, Majno PE (2013) Systematic review and meta-analysis of the effect of perioperative steroids on ischemia-reperfusion injury and surgical stress response in patients undergoing liver resection. Br J Surg 100(5):600–609CrossRefPubMedGoogle Scholar
  28. 28.
    Zhou YM, Shao WY, Zhao YF, Xu DH, Li B (2011) Meta-analysis of laparoscopic versus open resection for hepatocellular carcinoma. Dig Dis Sci 56(7):1937–1943CrossRefPubMedGoogle Scholar
  29. 29.
    Kluger MD, Cherqui D (2013) Laparoscopic resection of hepatocellular carcinoma. Recent Results Cancer Res 190:111–126CrossRefPubMedGoogle Scholar
  30. 30.
    Coolsen MM, Wong-Lun-Hing EM, van Dam RM, van der Wilt AA, Slim K, Lassen K, Dejong CH (2013) A systematic review of outcomes in patients undergoing liver surgery in an enhanced recovery after surgery pathways. HPB (Oxford) 15(4):245–251CrossRefGoogle Scholar
  31. 31.
    Schultz NA, Larsen PN, Klarskov B, Plum LM, Frederiksen HJ, Christensen BM, Kehlet H, Hillingsǿ JG (2013) Evaluation of a fast-track programme for patients undergoing liver resection. Br J Surg 100(1):138–143CrossRefPubMedGoogle Scholar
  32. 32.
    Poon RT, Fan ST, Lo CM, Liu CL, Lam CM, Yuen WK, Yeung C, Wong J (2004) Improving perioperative outcome expands the role of hepatectomy in management of benign and malignant hepatobiliary diseases: analysis of 1222 consecutive patients from a prospective database. Ann Surg 240(4):698–708PubMedPubMedCentralGoogle Scholar
  33. 33.
    Murakami Y, Kenichiro U, Sudo T, Hashimoto Y, Nakashima A, Sueda T (2012) Intranhepatic cholangiocarcinoma: clinicopathological differences between peripheral type and hilar type. J Gastrointest Surg 16:540–548CrossRefPubMedGoogle Scholar
  34. 34.
    Fretland ÅA, Kazaryan AM, Bjørnbeth BA, Flatmark K, Andersen MH, Tønnessen TI, Bjørnelv GM, Fagerland MW, Kristiansen R, Øyri K, Edwin B (2015) Open versus laparoscopic liver resection for colorectal liver metastases (the Oslo-CoMet study): study protocol for a randomized controlled trial. Trials 16(1):73CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    de’Angelis N, Eshkenazy R, Brunetti F, Valente R, Costa M, Disabato M, Salloum C, Compagnon P, Laurent A, Azoulay D (2015) Laparoscopic versus open resection for colorectal liver metastases: a single-center study with propensity score analysis. J Laparoendosc Adv Surg Tech A 25(1):12–20CrossRefPubMedGoogle Scholar
  36. 36.
    Ikeda O, Sakaguchi Y, Toh Y, Oogaki K, Oki E, Minami K, Okamura T, Baba H (2012) Evaluation of oncological adequacy of laparoscopic distal gastrectomy with special attention to lymph node dissection: a comparison with conventional open gastrectomy. Hepatogastroenterology 59(114):627–632PubMedGoogle Scholar
  37. 37.
    van der Sluis PC, Ruurda JP, van der Horst S, Verhage RJ, Besselink MG, Prins MJ, Haverkamp L, Schippers C, Rinkes IH, Joore HC, Ten Kate FJ, Koffijberg H, Kroese CC, van Leeuwen MS, Lolkema MP, Reerink O, Schipper ME, Steenhagen E, Vleggaar FP, Voest EE, Siersema PD, van Hillegersberg R (2012) Robot-assisted minimally invasive thoraco-laparoscopic esophagectomy versus open transthoracic esophagectomy for resectable esophageal cancer, a randomized controlled trial (ROBOT trial). Trials 13:230CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Francesca Ratti
    • 1
    Email author
  • Federica Cipriani
    • 1
  • Riccardo Ariotti
    • 1
  • Annalisa Gagliano
    • 1
  • Michele Paganelli
    • 1
  • Marco Catena
    • 1
  • Luca Aldrighetti
    • 1
  1. 1.Hepatobiliary Surgery DivisionIRCCS San Raffaele HospitalMilanItaly

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