Hepatobiliary and pancreatic (HBP) surgery is one of the most challenging aspects in the field of surgery. Introduction of laparoscopy has increased the technical difficulty further. Laparoscopic liver resection (LLR) with all its hurdles has gone a long way from small tumorectomy in the anterior-lateral area to major hepatectomy including donor hepatectomy.
With the advantages of 3D visibility, increased degrees of freedom, and reduced physiologic tremor, robotic surgery is gaining popularity. However, the high cost, loss of haptic feedback and few definite advantages over laparoscopic surgery have limited its use (1). Studies have shown that robotic liver resection (RLR) has acceptable conversion and complication rates and shows good overall safety with outcomes similar to laparoscopic and open surgery (2,3).
Gallbladder cancer (GBC) is a controversial subject in the field of minimal invasive HBP surgery. The advent of minimal invasive surgery (MIS) in GBC has started a dispute among hepato-biliary surgeons. Concerns ranging from port site recurrence, bile spillage causing cancer dissemination, to inadequate evidence of safety were prevalent among HBP surgeons. Not just the concern of oncological outcomes but the issue of patient safety associated with the technical difficulty in LLR has prevented the adoption of the minimal invasive approach for GBC. Another issue is the steep learning curve associated with safe lymph node dissection around the hepatoduodenal ligament (4). However, there have been increasing reports highlighting the advantages of MIS while maintaining patient safety. Reports on acceptable long-term oncological outcomes prompted a slow shift towards MIS (5). MIS in GBC is gradually being adopted at a number of centers recently. There is still skeptism on MIS in GBC in patients requiring liver resection. With increasing expertise in LLR, high volume centers have begun extending indications of laparoscopic GBC. There is still very limited data on minimal invasive liver resection in GBC with most data including retrospective studies and cases reports. In GBC, the aim of liver resection is to achieve a negative hepatic parenchymal resection margin as well as minimize recurrence by removing microscopic metastases in the liver (6). With experience these aims can be fulfilled even with MIS.
LLR in GBC
The ﬁrst prospective study on laparoscopic surgery for suspected early GBC was conducted from 2004 to 2007 by our team. 30 patients were selected based on a preoperative endoscopic ultrasound and intra-operative laparoscopic ultrasound done to rule out any liver invasion. The complication rate was 16.7% and no patient developed recurrence after a median follow up of 27 months (7).
A recent paper published by Jang et al. compared outcomes in T2 stage GBC between laparoscopic and open groups. Data of patients over 13 years was presented. Median follow up time was 35.2 months. There was no statistical difference between the 2 groups in terms of overall survival. Disease free survival was significantly higher in the laparoscopic group (at 5 years laparoscopic surgery vs. open surgery: 78% vs. 62.4%; P=0.0171). There was no case of port site recurrence reported in the laparoscopic surgery group (8). Agarwal et al. retrospectively compared outcomes of 24 cases of laparoscopic radical cholecystectomy and 46 cases of open radical cholecystectomy, showing no signiﬁcant difference in terms of postoperative morbidity, mortality, number of lymph nodes collected, and recurrence rate (9). Itano et al. reviewed 19 laparoscopic and 14 open cases of suspected T2 GBC, and showed no signiﬁcant difference in postoperative morbidity, mortality, number of lymph nodes collected, and recurrence rate (10).
The first prospective study did not include patients with LLR. The extent of liver resection has been a topic of debate. Still wedge resection or IVb and V resection is recommended for T2 GBC. There are reports that thin liver resection without wedge resection gives good results in T2 GBC (5). Lee et al. showed that there is no clear benefit of liver resection in selected patients with peritoneal side GBC (11).
There are several reports showing no difference in overall survival between wedge resection and IVb and V segmentectomy in GBC. Similar outcomes have been achieved with both surgeries (12,13). Wedge resection of the liver is technically easier than anatomical IV b and V resection therefore laparoscopic wedge resection can be easily performed.
In a recent consensus meeting involving 9 experts to discuss the role of laparoscopic surgery in GBC, the overall value of laparoscopic extended cholecystectomy for GBC was considered equivalent to open surgery (4).
Seven retrospective studies evaluating the outcomes of laparoscopic radical cholecystectomy including either wedge resection of the liver, segment IV b and V segmentectomy or major hepatic resections have been published (Table 1). All the reports show acceptable outcomes with laparoscopic surgery, some papers also showed results similar to those of open surgery.
The most recent retrospective study involving the largest cohort of patients was recently published online by Nag et al. They compared 30 patients of laparoscopic extended cholecystectomy with bi-segmentectomy, with 38 patients of open surgery. Mean blood loss (P=0.006) was significantly lower while mean hospital stay (P=0.0001) significantly shorter in the laparoscopic group. Median number of lymph nodes excised, post-operative complication rate, recurrence free and overall survival were similar in both groups. They concluded that laparoscopy can improve perioperative outcomes with similar oncological efficacy (20).
Robotic surgery in GBC
There are fewer published reports of robotic radical cholecystectomy (RRC) as compared to laparoscopic robotic cholecystectomy in GBC (Table 2). However, these reports on RRC show acceptable long term and short-term outcomes as well.
A study conducted in Italy evaluated the outcomes of completion cholecystectomy using both the robotic and laparoscopic approach. Three patients were present in each group. Segment IVb and V resection including lymphadenectomy was carried out with results similar to other studies and no recurrence after 32 months of follow-up. They thus concluded that radicalization of cholecystectomy can be achieved without compromising outcomes using MIS approach (24).
Goel et al. studied the outcomes in 27 patients after RRC. All patients underwent IV b and V segmentectomy. Only one patient had complications post operatively clavien dindo 3b. After a median follow up of 9 months, 2 patients had a recurrence (23).
Case reports on LLR and RLR
In conclusion, at present MIS can be recognized as a safe alternative to open surgery in GBC. Centers with expertise in both MIS surgery and hepatobiliary surgery can extend their MIS indications in GBC to include liver resection. With increasing experience there may come a day when this minimal access approach will become the standard of care in patients with GBC.
Provenance and Peer Review: This article was commissioned by the Guest Editor (Giammauro Berardi) for the series “Minimally Invasive Resections for Liver Malignancies: Among Certainties and Controversies” published in Laparoscopic Surgery. The article has undergone external peer review.
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/ls-20-51). The series “Minimally Invasive Resections for Liver Malignancies: Among Certainties and Controversies” was commissioned by the editorial office without any funding or sponsorship. The authors have no other conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
- Ocuin LM, Tsung A. Robotic liver resection for malignancy: Current status, oncologic outcomes, comparison to laparoscopy, and future applications. J Surg Oncol 2015;112:295-301. [Crossref] [PubMed]
- Tsilimigras DI, Moris D, Vagios S, et al. Safety and oncologic outcomes of robotic liver resections: A systematic review. J Surg Oncol 2018;117:1517-30. [Crossref] [PubMed]
- Morel P, Jung M, Cornateanu S, et al. Robotic versus open liver resections: A case-matched comparison. Int J Med Robot 2017; [Crossref] [PubMed]
- Yoon YS, Han HS, Agarwal A, et al. Survey results of the expert meeting on laparoscopic surgery for gallbladder cancer and a review of relevant literature. Dig Surg 2019;36:7-12. [Crossref] [PubMed]
- Yoon YS, Han HS, Cho JY, et al. Is laparoscopy contraindicated for gallbladder cancer? A 10-year prospective cohort study. J Am Coll Surg 2015;221:847-53. [Crossref] [PubMed]
- Han HS, Yoon YS, Agarwal AK, et al. Laparoscopic surgery for gallbladder cancer: An expert consensus statement. Dig Surg 2019;36:1-6. [Crossref] [PubMed]
- Cho JY, Han HS, Yoon YS, et al. Laparoscopic Approach for Suspected Early-Stage Gallbladder Carcinoma. Arch Surg 2010;145:128-33. [Crossref] [PubMed]
- Jang JY, Han HS, Yoon YS, et al. Retrospective comparison of outcomes of laparoscopicand open surgery for T2 gallbladder cancer - Thirteen-year experience. Surg Oncol 2019;29:142-7. [Crossref] [PubMed]
- Agarwal AK, Javed A, Kalayarasan R, et al. Minimally invasive vs. the conventional open surgical approach of a radical cholecystectomy for gallbladder cancer: A retrospective comparative study. HPB 2015;17:536-41. [Crossref] [PubMed]
- Itano O, Oshima G, Minagawa T, et al. Novel strategy for laparoscopic treatment of pT2 gallbladder carcinoma. Surg Endosc 2015;29:3600-7. [Crossref] [PubMed]
- Lee H, Choi DW, Park JY, et al. Surgical Strategy for T2 Gallbladder Cancer According to Tumor Location. Ann Surg Oncol 2015;22:2779-86. [Crossref] [PubMed]
- Yu LH, Yuan B, Fu XH, et al. Does anatomic resection get more benefits than wedge hepatectomy on the prognosis for pT3 unsuspected gallbladder cancer? J Laparoendosc Adv Surg Tech A 2019;29:1414-8. [Crossref] [PubMed]
- Patkar S, Patil V, Rajgopal Acharya M, et al. Achieving margin negative resection—doing less is justified: Oncological outcomes of wedge excision of liver in gallbladder cancer (GBC) surgery. Chin Clin Oncol 2019;8:38. [Crossref] [PubMed]
- Palanisamy S, Patel N, Sabnis S, et al. Laparoscopic radical cholecystectomy for suspected early gall bladder carcinoma: thinking beyond convention. Surg Endosc 2016;30:2442-8. [Crossref] [PubMed]
- Castro CM, Santibañez SP, Rivas TC, et al. Totally Laparoscopic Radical Resection of Gallbladder Cancer: Technical Aspects and Long-Term Results. World J Surg 2018;42:2592-8. [Crossref] [PubMed]
- Piccolo G, Ratti F, Cipriani F, et al. Totally Laparoscopic Radical Cholecystectomy for Gallbladder Cancer: A Single Center Experience. J Laparoendosc Adv Surg Tech A 2019;29:741-6. [Crossref] [PubMed]
- Nag HH, Raj P, Sisodia K. The technique of laparoscopic hepatic bisegmentectomy with regional lymphadenectomy for gallbladder cancer. J Minim Access Surg 2018;14:124-9. [Crossref] [PubMed]
- Gumbs AA, Jarufe N, Gayet B. Minimally invasive approaches to extrapancreatic cholangiocarcinoma. Surg Endosc 2013;27:406-14. [Crossref] [PubMed]
- Elmoghazy W, Cowan J, Tabchouri N, et al. Liver resection for extra-pancreatic biliary cancer: what is the role of laparoscopic approach? Surg Endosc 2019;33:3711-7. [Crossref] [PubMed]
- Nag HH, Sachan A, Nekarakanti PK. Laparoscopic vs. open extended cholecystectomy with bi-segmentectomy (s4b and s5) in patients with gallbladder cancer. J Minim Access Surg 2021;17:21-7. [Crossref] [PubMed]
- Shen BY, Zhan Q, Deng XX, et al. Radical resection of gallbladder cancer: Could it be robotic? Surg Endosc 2012;26:3245-50. [Crossref] [PubMed]
- Khan S, Beard RE, Kingham PT, et al. Long-Term Oncologic Outcomes Following Robotic Liver Resections for Primary Hepatobiliary Malignancies: A Multicenter Study. Ann Surg Oncol 2018;25:2652-60. [Crossref] [PubMed]
- Goel M, Khobragade K, Patkar S, et al. Robotic surgery for gallbladder cancer: Operative technique and early outcomes. J Surg Oncol 2019;119:958-63. [Crossref] [PubMed]
- Sinagra E, Garritano S, Iacopinelli SM, et al. Minimally invasive surgical approach for radicalization of incidental post-cholecystectomy gallbladder carcinoma: safety, feasibility and outcomes. Minim Invasive Ther Allied Technol 2018;27:217-20. [Crossref] [PubMed]
- Chin KM, Chua DWQ, Lee SY, et al. Outcome of minimally invasive liver resection for extrapancreatic biliary malignancies: A single-institutional experience. J Minim Access Surg 2021;17:69-75. [Crossref] [PubMed]
- Chandarana M, Patkar S, Tamhankar A, et al. Robotic resections in hepatobiliary oncology-initial experience with Xi da Vinci system in India. Indian J Cancer 2017;54:52-5. [Crossref] [PubMed]
- Gumbs AA, Milone L, Geha R, et al. Laparoscopic radical cholecystectomy. J Laparoendosc Adv Surg Tech A 2009;19:519-20. [Crossref] [PubMed]
- Goja S, Singh MK, Soin AS. Robotics in hepatobiliary surgery-initial experience, first reported case series from India. Int J Surg Case Rep 2017;33:16-20. [Crossref] [PubMed]
- Kim S, Yoon YS, Han HS, et al. Laparoscopic extended cholecystectomy for T3 gallbladder cancer. Surg Endosc 2018;32:2984-5. [Crossref] [PubMed]
- Muñoz C, Marino C, Morales E. Totally laparoscopic radical cholecystectomy (lymphadenectomy and segment IVb-V liver resection) after incidental gallbladder carcinoma (with video). J Visc Surg 2018;155:243-4. [Crossref] [PubMed]
- Gumbs AA, Hoffman JP. Laparoscopic radical cholecystectomy and Roux-en-Y choledochojejunostomy for gallbladder cancer. Surg Endosc 2010;24:1766-8. [Crossref] [PubMed]
- Machado MA, Makdissi FF, Surjan RC. Totally Laparoscopic Hepatic Bisegmentectomy (s4b+s5) and Hilar Lymphadenectomy for Incidental Gallbladder Cancer. Ann Surg Oncol 2015;22:S336-9. [Crossref] [PubMed]
Cite this article as: D’Silva M, Han HS, Yoon YS, Cho JY. Minimally invasive liver resection for gallbladder cancer. Laparosc Surg 2021;5:25.