Liver surgery—less is more

The laparoscopic approach to liver surgery has been increasingly utilized since it was first described in 1992 (1). As of 2016, nearly 10,000 cases were reported in the literature establishing laparoscopy as a safe and effective approach to resection of benign and malignant liver tumors (2). Initially reserved for smaller wedge resections in the anterior segments, advances in technology, development of new approaches and improvement in surgeon skill enabled complex laparoscopic approaches for major hepatectomies including challenging posterior segments. In fact, it is estimated that between 30–60% of liver resections are performed laparoscopically at specialty centers (3). International consensus recommends the laparoscopic approach as standard of care for minor resections while major resections are still considered investigational. This substantial progress exemplifies the importance of short and long-term data reporting, international collaboration and consensus publication (3-5).

There is a large body of literature establishing the laparoscopic approach for curative management of benign and malignant liver tumors. Not only has it been proven to be safe in skilled hands, the current evidence finds the laparoscopic approach to be advantageous for patients compared to open surgery in the short term while achieving comparable long-term oncologic outcomes (6-15). Laparoscopy affords unique intraoperative benefits including improved visualization of certain segments from a caudal compared to a ventral approach and lower blood loss from the venous tamponade effect by pneumoperitoneum and reverse Trendelenburg positioning. The article from Dr. Andreou and colleagues published in 2018 in Surgical Oncology complements this body of literature with a large propensity-matched comparison of minimally invasive hepatectomy (MIH), which included pure laparoscopic surgery, single-incision laparoscopic surgery (SILS), and the hybrid technique (HYB), versus open hepatectomy (OH) for hepatocellular carcinoma (HCC) (16).

Their cohort included 407 consecutive patients who underwent OH or MIH for HCC between 2005 and 2016 at two centers, with 56 (14%) of them undergoing MIH. The MIH cohort incorporated range of resections, consisting mostly of segmentectomies or wedge resections (n=31), but also several lobectomies (n=8) and bi-segmentectomies (n=16). After propensity score matching based on patient demographics, resection extent, underlying liver characteristics, and tumor number and size, 112 patients were compared between the MIH and OH cohorts. Their analysis demonstrated a statistically significant reduction in length of hospital stay, major and minor complications at 90 days, liver failure rate, and 90-day mortality in the MIH cohort. Aside from longer operative time, MIH did not result in any negative oncologic or perioperative outcomes such as increased percentage of positive surgical margins, prolonged ICU stay, or higher red blood cell transfusions. The authors compared oncologic outcomes after a median follow-up time of 51 months demonstrating MIH to have a comparable 5-year overall survival (54% vs. 41% for OH, P=0.151) and 5-year disease free survival rate (50% vs. 38% for OH, P=0.956). There are a few limitations of this matched retrospective series to acknowledge. First, the majority of MIH was performed during the last 2 years of the 11-year study period and advances in perioperative care and implementation of Early Recovery After Surgery (ERAS) protocols likely directly influenced perioperative outcomes such as length of stay. There was no mention of incidence of conversion to OH or if the MIH outcomes were recorded for an intention-to-treat assessment. Finally, limited information was provided on complexity of the case type as all segments are not created equal. Recognizing these limitations, their findings do mirror the current evidence and further establish the short and long-term efficacy of MIH while controlling for selection bias in a large, matched cohort.

The liver surgeon today is afforded with numerous technical approaches to tumor resection including conventional laparotomy, laparoscopic and robot-assisted laparoscopic techniques. Several randomized control trials are being conducted to better control for patient selection and compare these different modalities (Table 1). Published laparoscopic techniques include pure laparoscopic liver surgery (PLAP), SILS, hand-assisted laparoscopic surgery (HALS) and a HYB (17), which utilizes PLAP for liver mobilization and a mini-laparotomy for parenchymal transection and hilar dissection. Numerous factors influence selection of surgical approach including tumor location, size, extent of resection, parenchymal characteristics, and surgeon or regional preference. PLAP was originally reserved for peripherally accessible lesions while a hybrid or hand-assisted technique for lobectomies and larger formal resections, however as surgeon skill improves the application of these techniques has significantly broadened (18,19). The recent publication of the Southampton Consensus has provided important guidelines for liver surgeons in choosing an approaching a variety of indications, complex diseases, and operations (3).

In addition to traditional laparoscopy, robot surgical systems are increasingly being used for liver surgery since the system was approved by the US Food and Drug Administration (FDA) in 2000. An international consensus statement on robotic hepatectomy was published in 2018 to promote development of standardization of robotic hepatectomy and improve patient safety (20). In this statement, seven recommendations establishing safety and feasibility were based on low to very low levels of evidence (grade 2C and 2D), highlighting the need for higher quality investigations examining robot liver surgery in comparison to conventional techniques. The importance of prospective studies is further reinforced by the recent FDA warning regarding the safety and effectiveness of robot-assisted surgeries for early cervical and breast cancers (21). One randomized control trial is ongoing comparing robotic-assisted versus open surgery for complicated hepatolithiasis, and the hepatobiliary community looks forward to the results of this and other analyses.

Data examining the short and long-term differences in minimally invasive surgical approaches are limited and many are hampered by selection bias in retrospective series. No single approach has been identified as superior, although the hybrid approach has been encouraged as a technical bridge to pure laparoscopy. Fiorentini and colleagues recently reported the first propensity-matched analysis of pure laparoscopic versus hand-assisted/hybrid major hepatectomies at two centers (22). Comparing PLAP to HALS and HYB after 1:1 propensity matching, the two cohorts had comparable rate of open conversion, length of ICU stay, red blood cell transfusion, and postoperative morbidity or mortality. Operative time for PLAP and HALS were comparable while HYB approach reduced operative time by 100 minutes. Tsung et al. conducted a matched comparison of robotic and laparoscopic hepatectomy, demonstrating comparable safety and feasibility in 57 robotic to 114 laparoscopic hepatic resections (23). Several systematic reviews and meta-analyses comparing approaches demonstrate no proven advantage of any minimally invasive technique (24,25). Based on current evidence, multiple forms of MIH appear to achieve the same goals for our patients and we would predict that utilization of these techniques will be dependent upon surgeon skills, preference and institutional resources.

New and exciting technologies accompanying minimally invasive liver surgery are continuously being developed to improve pre-operative planning and intra-operative decision making (26). Although still mostly in exploratory phase, image-guided liver surgery, surgical resection maps, indocyanine green fluorescence with near-infrared fluorescent imaging and 3D modeling were developed to assist the surgeon and surgical trainee. Recent advances in virtual and augmented reality have been applied to liver surgery, with systems developed to help with surgical navigation. A recent report from our group has demonstrated the feasibility of rendering pre-operative axial imaging in three-dimensions on the robotic surgical console to guide liver resection in a porcine model (27). With technological advances and innovation in minimally invasive liver surgery, we hope to see continued improvement in surgical outcomes.

Faced with many choices, it can be challenging for liver surgeons to determine the optimal surgical approach for a given patient. With important contributions by Dr. Andreou et al. and others, there is mounting evidence that in skilled hands and in select patients, a minimally invasive approach is advantageous in liver surgery and should be offered.

Acknowledgments

Due to space limitation, we apologize for not citing other studies in this commentary.

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the editorial office, Laparoscopic Surgery. The article did not undergo external peer review.

Conflicts of Interest: The authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/ls.2019.05.01). The authors have no 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/.

References

1. Gagner M, Rheault M, Dubuc J. Laparoscopic partial hepatectomy for liver tumor Surg Endosc 1992;6:99. [abstract].
2. Ciria R, Cherqui D, Geller DA, et al. Comparative Short-term Benefits of Laparoscopic Liver Resection. Ann Surg. 2016;263:761-77. [Crossref] [PubMed]
3. Abu Hilal M, Aldrighetti L, Dagher I, et al. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery. Ann Surg 2018;268:11-8. [Crossref] [PubMed]
4. Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 2009;250:825-30. [Crossref] [PubMed]
5. 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;261:619-29. [PubMed]
6. Berardi G, Van Cleven S, Fretland ÅA, et al. Evolution of Laparoscopic Liver Surgery from Innovation to Implementation to Mastery: Perioperative and Oncologic Outcomes of 2,238 Patients from 4 European Specialized Centers. J Am Coll Surg 2017;225:639-49. [Crossref] [PubMed]
7. Tozzi F, Berardi G, Vierstraete M, et al. Laparoscopic Versus Open Approach for Formal Right and Left Hepatectomy: A Propensity Score Matching Analysis. World J Surg 2018;42:2627-34. [Crossref] [PubMed]
8. Nguyen KT, Gamblin TC, Geller DA. World Review of Laparoscopic Liver Resection—2,804 Patients. Ann Surg 2009;250:831-41. [Crossref] [PubMed]
9. Nguyen KT, Marsh JW, Tsung A, et al. Comparative Benefits of Laparoscopic vs Open Hepatic Resection. Arch Surg 2011;146:348. [Crossref] [PubMed]
10. Han HS, Shehta A, Ahn S, et al. Laparoscopic versus open liver resection for hepatocellular carcinoma: Case-matched study with propensity score matching. J Hepatol 2015;63:643-50. [Crossref] [PubMed]
11. Tzanis D, Shivathirthan N, Laurent A, et al. European experience of laparoscopic major hepatectomy. J Hepatobiliary Pancreat Sci 2013;20:120-4. [Crossref] [PubMed]
12. Tranchart H, Di Giuro G, Lainas P, et al. Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc 2010;24:1170-6. [Crossref] [PubMed]
13. Ratti F, Cipriani F, Ariotti R, et al. Laparoscopic major hepatectomies: current trends and indications. A comparison with the open technique. Updates Surg 2015;67:157-67. [Crossref] [PubMed]
14. Komatsu S, Brustia R, Goumard C, et al. Laparoscopic versus open major hepatectomy for hepatocellular carcinoma: a matched pair analysis. Surg Endosc 2016;30:1965-74. [Crossref] [PubMed]
15. Kasai M, Cipriani F, Gayet B, et al. Laparoscopic versus open major hepatectomy: a systematic review and meta-analysis of individual patient data. Surgery 2018;163:985-95. [Crossref] [PubMed]
16. Andreou A, Struecker B, Raschzok N, et al. Minimal-invasive versus open hepatectomy for hepatocellular carcinoma: Comparison of postoperative outcomes and long-term survivals using propensity score matching analysis. Surg Oncol 2018;27:751-8. [Crossref] [PubMed]
17. Koffron AJ, Kung RD, Auffenberg GB, et al. Laparoscopic liver surgery for everyone: the hybrid method. Surgery 2007;142:463-8; discussion 468.e1-2.
18. Coelho FF, Kruger JAP, Fonseca GM, et al. Laparoscopic liver resection: Experience based guidelines. World J Gastrointest Surg 2016;8:5-26. [Crossref] [PubMed]
19. Fong Y, Jarnagin W, Conlon KC, et al. Hand-Assisted Laparoscopic Liver Resection. Arch Surg 2000;135:854. [Crossref] [PubMed]
20. Liu R, Wakabayashi G, Kim HJ, et al. International consensus statement on robotic hepatectomy surgery in 2018. World J Gastroenterol 2019;25:1432-44. [Crossref] [PubMed]
21. Sancar F. Robotically Assisted Surgical Devices Raise Caution. JAMA 2019;321:1449. [PubMed]
22. Fiorentini G, Swaid F, Cipriani F, et al. Propensity Score-Matched Analysis of Pure Laparoscopic Versus Hand-Assisted/Hybrid Major Hepatectomy at Two Western Centers. World J Surg 2019; [Epub ahead of print]. [Crossref] [PubMed]
23. Tsung A, Geller DA, Sukato DC, et al. Robotic Versus Laparoscopic Hepatectomy. Ann Surg 2014;259:549-55. [Crossref] [PubMed]
24. Jackson NR, Hauch A, Hu T, et al. The safety and efficacy of approaches to liver resection: a meta-analysis. JSLS 2015;19:e2014.00186.
25. Qiu J, Chen S, Chengyou D. A systematic review of robotic-assisted liver resection and meta-analysis of robotic versus laparoscopic hepatectomy for hepatic neoplasms. Surg Endosc 2016;30:862-75. [Crossref] [PubMed]
26. Zygomalas A, Kehagias I. Up-to-date intraoperative computer assisted solutions for liver surgery. World J Gastrointest Surg 2019;11:1. [Crossref] [PubMed]
27. Sullivan KM, Labadie KP, Miller K, et al. Intelligent Imaging in Robotic-Assisted Liver Resection [abstract]. In: Proceedings of the Annual Meeting of Society for American Gastrointestinal and Endoscopic Surgeons. Baltimore, MD; 2019. Available online: https://epostersonline.s3.amazonaws.com/sages2019/sages2019.2e80b6a.NORMAL.pdf