Skip to main content
Log in

Is It Time to Consider Laparoscopic Hepatectomy for Intrahepatic Cholangiocarcinoma? A Meta-Analysis

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery

Abstract

Objectives

The role of laparoscopic hepatectomy (LH) for intrahepatic cholangiocarcinoma (ICC) remains indefinite, though the utilization of this minimally invasive approach has been increasing for ICC. We herein performed a meta-analysis to investigate this issue.

Methods

Six retrospective studies including 384 patients who had undergone LH and 2147 patients who had undergone open hepatectomy (OH) for ICC were included. The fixed-effects or random-effects models were utilized for data analysis.

Results

Compared with patients who had undergone OH for ICC, patients who had undergone LH for ICC experienced more R0 resections (81.6 versus 73.8%, risk ratio (RR) = 1.08, 95% confidence interval (CI) 1.02–1.14; P = 0.008) but less major hepatectomies (37.7 versus 54.2%, RR = 0.69, 95% CI 0.60–0.79; P < 0.0001), less lymph node dissections (38.0 versus 61.5%, RR = 0.62, 95% CI 0.54–0.70; P < 0.0001), and smaller tumor size resected (4.14 versus 4.94 cm, weighted mean difference = − 0.80 cm, 95% CI − 1.38 to − 0.22 cm; P = 0.007). No significant difference was observed in other perioperative results (all P > 0.05) or overall survival (hazard ratio (HR) = 1.38, 95% CI 0.63–3.02; P = 0.43).

Conclusions

LH has comparable safety, feasibility, and oncological efficacy to that of OH for ICC and has superiority in R0 resection over OH. It may be time to consider LH for ICC only if a more thorough effort on lymph node dissection is undertaken in selective patients at experienced centers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Razumilava N, Gores GJ. Cholangiocarcinoma. The Lancet 2014; 383: 2168–2179.

    Article  Google Scholar 

  2. Banales JM, Cardinale V, Carpino G, et al. Expert consensus document: Cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European Network for the Study of Cholangiocarcinoma (ENS-CCA). Nat Rev Gastroenterol Hepatol 2016; 13: 261–280.

    Article  Google Scholar 

  3. Sirica AE, Gores GJ, Groopman JD, et al. Intrahepatic Cholangiocarcinoma: Continuing Challenges and Translational Advances. Hepatology 2018; 69:1803–1815.

    Article  Google Scholar 

  4. Ransome E, Tong L, Espinosa J, et al. Trends in surgery and disparities in receipt of surgery for intrahepatic cholangiocarcinoma in the US: 2005-2014. J Gastrointest Oncol 2019; 10: 339–347.

    Article  Google Scholar 

  5. Antwi SO, Mousa OY, Patel T. Racial, Ethnic, and Age Disparities in Incidence and Survival of Intrahepatic Cholangiocarcinoma in the United States; 1995-2014. Ann Hepatol 2018; 17: 274–285.

    Article  Google Scholar 

  6. Chan KM, Tsai CY, Yeh CN, et al. Characterization of intrahepatic cholangiocarcinoma after curative resection: outcome, prognostic factor, and recurrence. BMC Gastroenterology 2018;18:180.

    Article  Google Scholar 

  7. Choi SB, Kim KS, Choi JY, et al. The prognosis and survival outcome of intrahepatic cholangiocarcinoma following surgical resection: association of lymph node metastasis and lymph node dissection with survival. Ann Surg Oncol 2009; 16: 3048–3056.

    Article  Google Scholar 

  8. Uchiyama K, Yamamoto M, Yamaue H, et al. 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 2011; 18: 443–452.

    Article  Google Scholar 

  9. Lurje G, Bednarsch J, Czigany Z, et al. The prognostic role of lymphovascular invasion and lymph node metastasis in perihilar and intrahepatic cholangiocarcinoma. Eur J Surg Oncol 2019; 45:1468-1478.

  10. Mahul B. Amin, Stephen Edge, Frederick Greene, et al. AJCC Cancer Staging Manual, 8th edition. Springer International Publishing 2017; 297–299Hardcover ISBN. 978-3-319-40617-6.

  11. Zhang XF, Chakedis J, Bagante F, et al. Trends in use of lymphadenectomy in surgery with curative intent for intrahepatic cholangiocarcinoma. Br J Surg 2018; 105: 857–866.

  12. Kim SH, Han DH, Choi GH, et al. Oncologic Impact of Lymph Node Dissection for Intrahepatic Cholangiocarcinoma: a Propensity Score-Matched Study. J Gastrointest Surg 2018; 23:538–544.

    Article  Google Scholar 

  13. Li DY, Zhang HB, Yang N, et al. Routine lymph node dissection may be not suitable for all intrahepatic cholangiocarcinoma patients: Results of a monocentric series. World J Gastroenterol 2013; 19:9084–9091.

    Article  Google Scholar 

  14. Zhou R, Lu D, Li W, et al. Is lymph node dissection necessary for resectable intrahepatic cholangiocarcinoma? A systematic review and meta-analysis. HPB (Oxford) 2019; 21:784–792.

    Article  Google Scholar 

  15. Ciria R, Cherqui D, Geller DA, et al. Comparative Short-term Benefits of Laparoscopic Liver Resection: 9000 Cases and Climbing. Ann Surg 2016; 263: 761–777.

    Article  Google Scholar 

  16. Xiangfei M, Yinzhe X, Yingwei P, et al. Open versus laparoscopic hepatic resection for hepatocellular carcinoma: a systematic review and meta-analysis. Surg Endosc 2019; 33:2396–2418.

    Article  Google Scholar 

  17. Uy BJ, Han HS, Yoon YS, et al. Laparoscopic Liver Resection for Intrahepatic Cholangiocarcinoma. J Laparoendosc Adv Surg Tech A 2015; 25:272–277.

  18. Ratti F, Cipriani F, Ariotti R, et al. Safety and feasibility of laparoscopic liver resection with associated lymphadenectomy for intrahepatic cholangiocarcinoma: a propensity score-based case-matched analysis from a single institution. Surg Endosc 2016; 30: 1999–2010.

  19. Lee W, Park JH, Kim JY, et al. Comparison of perioperative and oncologic outcomes between open and laparoscopic liver resection for intrahepatic cholangiocarcinoma. Surg Endosc 2016; 30: 4835–4840.

  20. Wei F, Lu C, Cai L, et al. Can laparoscopic liver resection provide a favorable option for patients with large or multiple intrahepatic cholangiocarcinomas? Surg Endosc 2017; 31: 3646–3655.

    Article  Google Scholar 

  21. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62:1006–1012.

    Article  Google Scholar 

  22. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000; 283:2008–2012.

    Article  CAS  Google Scholar 

  23. Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. [Cited 1 Jun 2019.] Available from URL: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

  24. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005; 5:13.

    Article  Google Scholar 

  25. Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 2007; 8:16.

    Article  Google Scholar 

  26. Kinoshita M, Kanazawa A, Takemura S, et al. Indications for laparoscopic liver resection of mass-forming intrahepatic cholangiocarcinoma. Asian J Endosc Surg. 2019 Mar 28. https://doi.org/10.1111/ases.12703. [Epub ahead of print]

  27. Martin SP, Drake J, Wach MM, et al. Laparoscopic Approach to Intrahepatic Cholangiocarcinoma is Associated with an Exacerbation of Inadequate Nodal Staging. Ann Surg Oncol 2019;26:1851–1857.

    Article  Google Scholar 

  28. Ratti F, Fiorentini G, Cipriani F, et al. Perioperative and Long-Term Outcomes of Laparoscopic Versus Open Lymphadenectomy for Biliary Tumors: A Propensity-Score-Based, Case-Matched Analysis. Ann Surg Oncol 2019;26:564–575.

    Article  Google Scholar 

  29. Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 2009;250:825–830.

    Article  Google Scholar 

  30. Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 2015; 261:619–629.

    PubMed  Google Scholar 

  31. Jiang S, Wang Z, Ou M, et al. Laparoscopic Versus Open Hepatectomy in Short- and Long-Term Outcomes of the Hepatocellular Carcinoma Patients with Cirrhosis: A Systematic Review and Meta-Analysis. J Laparoendosc Adv Surg Tech A; 2019 Jan 31. https://doi.org/10.1089/lap.2018.0588. [Epub ahead of print].

  32. Ciria R, Ocaña S, Gomez-Luque I, et al. A systematic review and meta-analysis comparing the short- and long-term outcomes for laparoscopic and open liver resections for liver metastases from colorectal cancer. Surg Endosc. 2019 Apr 15. https://doi.org/10.1007/s00464-019-06774-2.

  33. Harimoto N, Shimada M, Tsujita E, et al. Laparoscopic hepatectomy and dissection of lymph nodes for intrahepatic cholangiocarcinoma. Case report. Surg Endosc 2002; 16:1806.

  34. Abu Hilal M, Badran A, Di Fabio F, et al. Pure Laparoscopic En Bloc Left Hemihepatectomy and Caudate Lobe Resection in Patients with Intrahepatic Cholangiocarcinoma. J Laparoendosc Adv Surg Tech A 2011;21:845–849.

    Article  Google Scholar 

  35. Takahashi M, Wakabayashi G, Nitta H, et al. Pure laparoscopic right hepatectomy by anterior approach with hanging maneuver for large intrahepatic cholangiocarcinoma. Surg Endosc 2013; 27:4732–4733.

    Article  Google Scholar 

  36. Saito Y, Yamada S, Imura S, et al. A learning curve for laparoscopic liver resection: an effective training system and standardization of technique. Transl Gastroenterol Hepatol 2018; 3:45.

    Article  Google Scholar 

  37. Jia C, Li H, Wen N, et al. Laparoscopic liver resection: a review of current indications and surgical techniques. Hepatobiliary Surg Nutr 2018; 7:277–288.

    Article  Google Scholar 

  38. Ogiso S, Nomi T, Araki K, et al. Laparoscopy-Specific Surgical Concepts for Hepatectomy Based on the Laparoscopic Caudal View: A Key to Reboot Surgeons’ Minds. Annals of Surgical Oncology 2015; 22: S327–333.

    Article  Google Scholar 

  39. Nomi T, Hokuto D, Yoshikawa T, et al. A Novel Navigation for Laparoscopic Anatomic Liver Resection Using Indocyanine Green Fluorescence. Ann Surg Oncol 2018; 25: 3982.

  40. Aoki T, Murakami M, Koizumi T, et al. Determination of the surgical margin in laparoscopic liver resections using infrared indocyanine green fluorescence. Langenbecks Arch Surg 2018; 403: 671–680.

    Article  Google Scholar 

  41. Wu L, Tsilimigras DI, Paredes AZ, et al. Trends in the Incidence, Treatment and Outcomes of Patients with Intrahepatic Cholangiocarcinoma in the USA: Facility Type is Associated with Margin Status, Use of Lymphadenectomy and Overall Survival. World J Surg 2019; 43: 1777–1787.

  42. Zhang XF, Lv Y, Weiss M, et al. Should Utilization of Lymphadenectomy Vary According to Morphologic Subtype of Intrahepatic Cholangiocarcinoma? Ann Surg Oncol 2019; 26: 2242–2250.

    Article  Google Scholar 

  43. Morine Y, Shimada M. The value of systematic lymph node dissection for intrahepatic cholangiocarcinoma from the viewpoint of liver lymphatics. J Gastroenterol 2015; 50:913–927.

  44. Lendoire JC, Gil L, Imventarza O. Intrahepatic cholangiocarcinoma surgery: the impact of lymphadenectomy. Chin Clin Oncol 2018; 7: 53.

    Article  Google Scholar 

  45. Bagante F, Spolverato G, Weiss M, et al. Surgical Management of Intrahepatic Cholangiocarcinoma in Patients with Cirrhosis: Impact of Lymphadenectomy on Peri-Operative Outcomes. World J Surg. 2018;42:2551–2560.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

FQ Wei conceived and designed the study. G Wang, JY Ding, and TN Yu acquired and analyzed the data. CW Dou and CW Zhang interpreted the data. FQ Wei wrote the manuscript. G Wang helped to revise the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Fangqiang Wei.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethics Approval and Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Table S1

Meta-analysis of baseline characteristics. (DOCX 97 kb)

Figure S1

Flowchart of included studies. (PNG 69 kb)

High Resolution Image (TIF 562 kb)

Figure S2

Results of the meta-analysis on perioperative outcomes: (A) The mean difference of operation time in minutes in laparoscopic hepatectomy (LH) in comparison with open hepatectomy (OH); (B) The mean difference of blood loss in milliliter in LH in comparison with OH; (C) The T1 stage tumors rate in LH in comparison with OH; (D)The well differentiation tumors rate in LH in comparison with OH; (E) The morbidity rate in LH in comparison with OH; (F) The mean difference of hospital stay in days in LH in comparison with OH. (PNG 469 kb)

High Resolution Image (TIF 5187 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, F., Wang, G., Ding, J. et al. Is It Time to Consider Laparoscopic Hepatectomy for Intrahepatic Cholangiocarcinoma? A Meta-Analysis. J Gastrointest Surg 24, 2244–2250 (2020). https://doi.org/10.1007/s11605-019-04404-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-019-04404-9

Keywords

Navigation