Robotic versus laparoscopic liver resection for huge (≥10 cm) liver tumors: an international multicenter propensity-score matched cohort study of 799 cases
Original Article

Robotic versus laparoscopic liver resection for huge (≥10 cm) liver tumors: an international multicenter propensity-score matched cohort study of 799 cases

Tan-To Cheung1, Rong Liu2, Federica Cipriani3, Xiaoying Wang4, Mikhail Efanov5, David Fuks6, Gi-Hong Choi7, Nicholas L. Syn8, Charing C. N. Chong9, Fabrizio Di Benedetto10, Ricardo Robles-Campos11, Vincenzo Mazzaferro12, Fernando Rotellar13,14, Santiago Lopez-Ben15, James O. Park16, Alejandro Mejia17, Iswanto Sucandy18, Adrian K. H. Chiow19, Marco V. Marino20,21, Mikel Gastaca22, Jae Hoon Lee23, T. Peter Kingham24, Mathieu D’Hondt25, Sung Hoon Choi26, Robert P. Sutcliffe27, Ho-Seong Han28, Chung-Ngai Tang29, Johann Pratschke30, Roberto I. Troisi31, Go Wakabayashi32, Daniel Cherqui33, Felice Giuliante34, Davit L. Aghayan35, Bjorn Edwin35, Olivier Scatton36, Atsushi Sugioka37, Tran Cong Duy Long38, Constantino Fondevila39, Mohammad Abu Hilal40,41, Andrea Ruzzenente42, Alessandro Ferrero43, Paulo Herman44, Kuo-Hsin Chen45, Luca Aldrighetti3, Brian K. P. Goh46,47; International robotic and laparoscopic liver resection study group investigators*

1Department of Surgery, Queen Mary Hospital, The University of Hong Kong, Hong Kong SAR, China; 2Faculty of Hepatopancreatobiliary Surgery, The First Medical Center of Chinese People’s Liberation Army (PLA) General Hospital, Beijing, China; 3Hepatobiliary Surgery Division, IRCCS San Raffaele Hospital, Milan, Italy; 4Department of Liver Surgery and Transplantation, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai, China; 5Department of Hepato-Pancreato-Biliary Surgery, Moscow Clinical Scientific Center, Moscow, Russia; 6Department of Digestive, Oncologic and Metabolic Surgery, Institute Mutualiste Montsouris, Universite Paris Descartes, Paris, France; 7Division of Hepatopancreatobiliary Surgery, Department of Surgery, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea; 8Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore; 9Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong SAR, China; 10HPB Surgery and Liver Transplant Unit, University of Modena and Reggio Emilia, Modena, Italy; 11Department of General, Visceral and Transplantation Surgery, Clinic and University Hospital Virgen de la Arrixaca, IMIB-ARRIXACA, Murcia, Spain; 12HPB Surgery, Hepatology and Liver Transplantation, Fondazione IRCCS Istituto Nazionale Tumori di Milano, Milan, Italy; 13HPB and Liver Transplant Unit, Department of General Surgery, Clinica Universidad de Navarra, Universidad de Navarra, Pamplona, Spain; 14Institute of Health Research of Navarra (IdisNA), Pamplona, Spain; 15Hepatobiliary and Pancreatic Surgery Unit, Department of Surgery, Dr. Josep Trueta Hospital, IdIBGi, Girona, Spain; 16Hepatobiliary Surgical Oncology, Department of Surgery, University of Washington Medical Center, Seattle, WA, USA; 17The Liver Institute, Methodist Dallas Medical Center, Dallas, TX, USA; 18AdventHealth Tampa, Digestive Health Institute, Tampa, FL, USA; 19Hepatopancreatobiliary Unit, Department of Surgery, Changi General Hospital, Singapore, Singapore; 20General Surgery Department, Azienda Ospedaliera Ospedali Riuniti Villa Sofia-Cervello, Palermo, Italy; 21Oncologic Surgery Department, P. Giaccone University Hospital, Palermo, Italy; 22Hepatobiliary Surgery and Liver Transplantation Unit, Biocruces Bizkaia Health Research Institute, Cruces University Hospital, University of the Basque Country, Bilbao, Spain; 23Division of Hepato-Biliary and Pancreatic Surgery, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea; 24Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA; 25Department of Digestive and Hepatobiliary/Pancreatic Surgery, Groeninge Hospital, Kortrijk, Belgium; 26Department of General Surgery, CHA Bundang Medical Center, CHA University School of Medicine, Seongnam, Korea; 27Department of Hepatopancreatobiliary and Liver Transplant Surgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK; 28Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Korea; 29Department of Surgery, Pamela Youde Nethersole Eastern Hospital, Hong Kong SAR, China; 30Department of Surgery, Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany; 31Division of HPB, Minimally Invasive and Robotic Surgery, Department of Clinical Medicine and Surgery, Federico II University Hospital Naples, Naples, Italy; 32Center for Advanced Treatment of Hepatobiliary and Pancreatic Diseases, Ageo Central General Hospital, Saitama, Japan; 33Department of Hepatobiliary Surgery, Assistance Publique Hopitaux de Paris, Centre Hepato-Biliaire, Paul-Brousse Hospital, Villejuif, France; 34Hepatobiliary Surgery Unit, Fondazione Policlinic Universitario A. Gemelli, IRCCS, Catholic University of the Sacred Heart, Rome, Italy; 35The Intervention Centre, Institute of Clinical Medicine and Department of Hepato-Pancreato-Biliary Surgery, Oslo University Hospital, Oslo, Norway; 36Department of Digestive, HBP and Liver Transplantation, Hopital Pitie-Salpetriere, APHP, Sorbonne Université, Paris, France; 37Department of Surgery, Fujita Health University School of Medicine, Aichi, Japan; 38Department of Hepatopancreatobiliary Surgery, University Medical Center, University of Medicine and Pharmacy, Ho Chi Minh City, Vietnam; 39General and Digestive Surgery, Hospital Clinic, IDIBAPS, CIBERehd, University of Barcelona, Barcelona, Spain; 40Department of Surgery, University Hospital Southampton, Southampton, UK; 41Department of Surgery, Fondazione Poliambulanza, Brescia, Italy; 42General and Hepatobiliary Surgery, Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, GB Rossi Hospital, Verona, Italy; 43Department of General and Oncological Surgery, Mauriziano Hospital, Turin, Italy; 44Liver Surgery Unit, Department of Gastroenterology, University of Sao Paulo School of Medicine, Sao Paulo, Brazil; 45Division of General Surgery, Department of Surgery, Far Eastern Memorial Hospital, New Taipei City; 46Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and National Cancer Centre Singapore, Singapore, Singapore; 47Duke-National University of Singapore Medical School, Singapore, Singapore

Contributions: (I) Conception and design: TT Cheung, R Liu, KH Chen, L Aldrighetti, BKP Goh; (II) Administrative support: TT Cheung, R Liu, BKP Goh; (III) Provision of study material or patients: All authors; (IV) Collection and assembly of data: All authors; (V) Data analysis and interpretation: TT Cheung, R Liu, NL Syn, BKP Goh; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

*International robotic and laparoscopic liver resection study group investigators: Chung-Yip Chan, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital, Singapore, Singapore; Mizelle D’Silva, Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Korea; Henri Schotte, Department of Digestive and Hepatobiliary/Pancreatic Surgery, Groeninge Hospital, Kortrijk, Belgium; Celine De Meyere, Department of Digestive and Hepatobiliary/Pancreatic Surgery, Groeninge Hospital, Kortrijk, Belgium; Eric C. H. Lai, Department of Surgery, Pamela Youde Nethersole Eastern Hospital, Hong Kong SAR, China; Felix Krenzien, Department of Surgery, Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany; Moritz Schmelzle, Department of Surgery, Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany; Prashant Kadam, Department of Hepatopancreatobiliary and Liver Transplant Surgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK; Roberto Montalti, Division of HPB, Minimally Invasive and Robotic Surgery, Department of Clinical Medicine and Surgery, Federico II University Hospital Naples, Naples, Italy; Mariano Giglio, Division of HPB, Minimally Invasive and Robotic Surgery, Department of Clinical Medicine and Surgery, Federico II University Hospital Naples, Naples, Italy; Qu Liu, Faculty of Hepatopancreatobiliary Surgery, the First Medical Center of Chinese People’s Liberation Army (PLA) General Hospital, Beijing, China; Kit-Fai Lee, Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong SAR, China; Diana Salimgereeva, Department of Hepato-Pancreato-Biliary Surgery, Moscow Clinical Scientific Center, Moscow, Russia; Ruslan Alikhanov, Department of Hepato-Pancreato-Biliary Surgery, Moscow Clinical Scientific Center, Moscow, Russia; Lip-Seng Lee, Hepatopancreatobiliary Unit, Department of Surgery, Changi General Hospital, Singapore, Singapore; Mikel Prieto, Hepatobiliary Surgery and Liver Transplantation Unit, Biocruces Bizkaia Health Research Institute, Cruces University Hospital, University of the Basque Country, Bilbao, Spain; Jae Young Jang, Department of General Surgery, CHA Bundang Medical Center, CHA University School of Medicine, Seongnam, Korea; Victor Lopez-Lopez, Department of Surgery, Virgen de la Arrixaca University Hospital, Murcia, Spain; Paolo Magistri, HPB Surgery and Liver Transplant Unit, University of Modena and Reggio Emilia, Modena, Italy; Margarida Casellas I. Robert, Department of Surgery, Virgen de la Arrixaca University Hospital, Murcia, Spain; Chetana Lim, Department of Digestive, HBP and Liver Transplantation, Hopital Pitie-Salpetriere, APHP, Sorbonne Université, Paris, France; Kevin P. Labadie, Hepatobiliary Surgical Oncology, Department of Surgery, University of Washington Medical Center, Seattle, WA, USA; Phan Phuoc Nghia, University Medical Center, Ho Chi Minh City, Vietnam; Masayuki Kojima, Department of Surgery, Fujita Health University School of Medicine, Aichi, Japan; Yutaro Kato, Department of Surgery, Fujita Health University School of Medicine, Aichi, Japan; Kohei Mishima, Center for Advanced Treatment of Hepatobiliary and Pancreatic Diseases, Ageo Central General Hospital, Saitama, Japan; Mansour Saleh, Department of Hepatobiliary Surgery, Assistance Publique Hopitaux de Paris, Centre Hepato-Biliaire, Paul-Brousse Hospital, Villejuif, France; Franco Pascual, Department of Hepatobiliary Surgery, Assistance Publique Hopitaux de Paris, Centre Hepato-Biliaire, Paul-Brousse Hospital, Villejuif, France; Fabricio Ferreira Coelho, Liver Surgery Unit, Department of Gastroenterology, University of Sao Paulo School of Medicine, Sao Paulo, Brazil; Jaime Arthur Pirola Kruger, Liver Surgery Unit, Department of Gastroenterology, University of Sao Paulo School of Medicine, Sao Paulo, Brazil; Astmund Avdem Fretland, The Intervention Centre, Institute of Clinical Medicine and Department of Hepato-Pancreato-Biliary Surgery, Oslo University Hospital, Oslo, Norway; Jacob Ghotbi, The Intervention Centre, Institute of Clinical Medicine and Department of Hepato-Pancreato-Biliary Surgery, Oslo University Hospital, Oslo, Norway; Bernardo Dalla Valle, General and Hepatobiliary Surgery, Department of Surgery, Dentistry, Gynecology and Pediatrics, University of Verona, GB Rossi Hospital, Verona, Italy; Amal Suhool, Department of Surgery, University Hospital Southampton, UK and Department of Surgery, Fondazione Poliambulanza, Brescia, Italy; Ugo Giustizieri, HPB Surgery, Hepatology and Liver Transplantation, Fondazione IRCCS Istituto Nazionale Tumori di Milano, Milan, Italy; Davide Citterio, HPB Surgery, Hepatology and Liver Transplantation, Fondazione IRCCS Istituto Nazionale Tumori di Milano, Milan, Italy; Simone Vani, Hepatobiliary Surgery Unit, Fondazione Policlinic Universitario A. Gemelli, IRCCS, Catholic University of the Sacred Heart, Rome, Italy; Tiing Foong Siow, Division of General Surgery, Far Eastern Memorial Hospital, Taipei; Fabio Forchino, Department of General and Oncological Surgery, Mauriziano Hospital, Turin, Italy.

Correspondence to: Professor Brian K. P. Goh, MBBS, MMed, MSc, FRCSEd. Senior Consultant and Professor, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and National Cancer Centre Singapore, Level 5, 20 College Road, Academia, Singapore 169856, Singapore. Email: bsgkp@hotmail.com; Professor Tan To Cheung, MS, MD, FRCS. Department of Surgery, Queen Mary Hospital, University of Hong Kong, Hong Kong SAR, China. Email: tantocheung@hotmail.com.

Background: The use of laparoscopic (LLR) and robotic liver resections (RLR) has been safely performed in many institutions for liver tumours. A large scale international multicenter study would provide stronger evidence and insight into application of these techniques for huge liver tumours ≥10 cm.

Methods: This was a retrospective review of 971 patients who underwent LLR and RLR for huge (≥10 cm) tumors at 42 international centers between 2002–2020.

Results: One hundred RLR and 699 LLR which met study criteria were included. The comparison between the 2 approaches for patients with huge tumors were performed using 1:3 propensity-score matching (PSM) (73 vs. 219). Before PSM, LLR was associated with significantly increased frequency of previous abdominal surgery, malignant pathology, liver cirrhosis and increased median blood. After PSM, RLR and LLR was associated with no significant difference in key perioperative outcomes including media operation time (242 vs. 290 min, P=0.286), transfusion rate rate (19.2% vs. 16.9%, P=0.652), median blood loss (200 vs. 300 mL, P=0.694), open conversion rate (8.2% vs. 11.0%, P=0.519), morbidity (28.8% vs. 21.9%, P=0.221), major morbidity (4.1% vs. 9.6%, P=0.152), mortality and postoperative length of stay (6 vs. 6 days, P=0.435).

Conclusions: RLR and LLR can be performed safely for selected patients with huge liver tumours with excellent outcomes. There was no significant difference in perioperative outcomes after RLR or LLR.

Keywords: Laparoscopic liver resection (LLR); robotic liver resection (RLR); hepatocellular carcinoma; colorectal liver metastases; huge

Submitted Jul 09, 2022. Accepted for publication Oct 15, 2022. Published online Mar 17, 2023.

doi: 10.21037/hbsn-22-283

Highlight box

Key findings

• Both robotic and laparoscopic liver resections can be performed safely for selected patients with huge liver tumours with excellent outcomes. There was no significant difference in perioperative outcomes after RLR or LLR.

What is known and what is new?

• The use of laparoscopic and robotic liver resections has been widely adopted and safely performed in many institutions. Information on the application of the minimally-invasive approach for huge (≥10 cm) tumours remains limited.

• This study provides new data demonstrating the safety and feasibility of performing laparoscopic and robotic liver resections for huge tumours.

What is the implication, and what should change now?

• Minimally-invasive surgery should be used even for huge liver tumors when performed by experienced surgeons. Future prospective studies with long-term outcomes are needed to determine its oncological safety in comparison with the open approach and to compare between the robotic and laparoscopic approach.

Introduction

The minimally invasive approach to liver resection (MILR) for liver tumours has been proven to be safe and effective especially for minor liver resection (LR) (1-3). The short-term advantages over open surgery include less blood loss, less transfusion requirement, shorter hospital stays and less morbidities (3). The number of laparoscopic and robotic minor LR performed worldwide has proliferated in recent years. Nonetheless, most major and complex hepatectomies today are still performed via the traditional open approach (1-5). The slow development of major and complex LR by the minimally invasive approach is not surprising as the learning curve for this approach is long and steep (6-9).

A growing body of literature has demonstrated that MILR can be safely carried out in expert centers, and indications for MILR have been expanding. In Asia, for example, MILR for donor hepatectomy has been adopted cautiously in several high-volume centers (10). In a similar vein, resection of huge (≥10 cm) tumours—which were previously considered a contraindication to MILR (11)—was recently reported in a small single-surgeon study, which suggested that if surgeons can overcome the technical difficulties of resecting huge tumours via the minimally-invasive approach, the benefits of minimally invasive surgery could still be maintained (12). Given the paucity of data and potential biases inherent in small single-center studies, a large scale international multicenter study would provide stronger evidence and insight into MILR for huge tumours.

As some recent studies have suggested that robotic liver resections (RLR) may be associated with advantages over laparoscopic liver resections (LLR), we performed the present study with the primary objective of comparing the outcomes between LLR and RLR for huge liver tumours to determine if robotic assistance may be advantageous in this subset of patients. To the best of our knowledge, this study represents the largest series to date focusing on the application of LLR and RLR in this group of patients. We present the following article in accordance with the STROBE reporting checklist (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-22-283/rc).

Methods

This was a retrospective review of 971 patients who underwent MILR for huge (≥10 cm) tumors at 42 international centers between 2002 and 2020. All institutions obtained their respective approvals according to their local center’s requirements. This retrospective study on anonymized patient data was approved by the Singapore General Hospital Institution Review Board (No. 2020/2802) and the need for any further board review and patient consent was waived. The anonymized data were collected in the individual centers. These were collated and analyzed centrally at the Singapore General Hospital. The study was performed in accordance with the Declaration of Helsinki (as revised in 2013).

After exclusion of patients who underwent hepatectomy with bilio-enteric anastomoses, resection of cysts and cystic tumors such as cystadenoma, gallbladder carcinoma and intrahepatic stones; there were 853 cases. A further 24 cases of laparoscopic-assisted (hybrid) resections were excluded. Of the 829 cases, there were 699 pure LLR, 100 RLR and 30 hand-assisted laparoscopic (HAL)-LR. The 30 HAL were excluded from further analyses.

Definitions

LR were defined according to the 2000 Brisbane classification (13). Major resections were classified as resection of 3 or more contiguous segments. Additionally, right anterior and right posterior sectionectomies were also considered major resections in this study (14-16). This is due to the wide surface area for parenchymal transection associated with these resections (14-16).

Portal hypertension was defined based on clinical criteria such as the presence of ascites, varices or splenomegaly with a platelet count of less than 100,000/µL as portal pressure was not routinely measured in most centers. Diameter of the largest lesion was used in the cases of multiple tumors. Huge tumors were defined as tumors with a size ≥10 cm based on histology. Post-operative complications were classified according to the Clavien-Dindo classification and recorded for up to 30 days or during the same hospitalization (17). Difficulty of resections were graded according to the Iwate score and Institute Mutualiste Montsouris (IMM) score (18,19).

Statistical analyses

The comparisons between the robotic and laparoscopic approaches for patients with huge tumors were accomplished using propensity-score matching (PSM). Propensity-scores were developed using Firth logit modelling of all baseline characteristics shown in Table 1. This included variables such as age, year of surgery, gender, American Society of Anesthesiologists (ASA), previous abdominal surgery or previous liver surgery, patho, Child-Pugh status, portal hypertension, tumor size, multifocal, multiple resections, concomitant other surgery, major resection, Iwate score and IMM difficulty grade. This model exhibited excellent discrimination [area under the curve (AUC) =0.827, bias-corrected 95% confidence interval (CI): 0.788–0.866] and good calibration (P=0.512 from Hosmer-Lemeshow test with 10 deciles) (Figures S1,S2). PSM was performed using 1:3 greedy matching algorithm without replacement and with a caliper of 0.20*standard deviations of the linear predictor (i.e., log odds of the propensity score). Propensity-score distributions and covariates were well-balanced after matching (Figures S3-S5). As there was minimal missing data, complete cases analysis with no imputation was performed.

Table 1

Comparison between baseline clinicopathological characteristics of RLR vs. LLR for huge (≥10 cm) tumors

Baseline characteristics Overall (n=799) Unmatched cohort 1:3 propensity-score matched cohort
RLR (n=100) LLR (n=699) P value RLR (n=73) LLR (n=219) P value
Median age [IQR], years 60 [46–61) 54 [41–66] 60 [46–71] 0.004 54 [40–66] 55 [42–68] 0.544
Year of surgery, n (%) 0.001 0.846
   2002–2010 75 (9.4) 0 (0.0) 75 (10.7) 0 (0.0) 1 (0.5)
   2011–2015 175 (21.9) 20 (20.0) 155 (22.2) 17 (23.3) 51 (23.3)
   2016–2020 549 (68.7) 80 (80.0) 469 (67.1) 56 (76.7) 167 (76.3)
Male sex, n (%) 412/798 (51.6) 48/100 (48.0) 364/698 (52.1) 0.437 34 (46.6) 105 (47.9) 0.839
ASA score, n (%) 0.938 0.649
   I/II 609/798 (75.3) 75/100 (75.0) 526/698 (75.4) 51 (69.9) 159 (72.6)
   III/IV 197/798 (24.7) 25/100 (25.0) 172/698 (24.6) 22 (30.1) 60 (27.4)
Median BMI, [IQR] kg/m2 24.7 [22.3–27.5] 25.0 [23.0–28.5] 24.7 [22.1–27.4] 0.209 25.0 [22.6–28.5] 24.0 [21.6–27.3] 0.123
Previous abdominal surgery, n (%) 256 (32.0) 20 (20.0) 236 (33.8) 0.006 16 (21.9) 52 (23.7) 0.750
Previous liver surgery, n (%) 48 (6.0) 2 (2.0) 46 (6.6) 0.071 1 (1.4) 3 (1.4) 1.000
Malignant pathology, n (%) 560 (70.1) 59 (59.0) 501 (71.7) 0.010 41 (56.2) 140 (63.9) 0.232
Pathology type, n/n (%) 0.026 0.840
   HCC 296/798 (37.1) 36/100 (36.0) 260/698 (37.2) 24 (32.9) 82 (37.4)
   Intrahepatic cholangiocarcinoma 83/798 (10.4) 12/100 (12.0) 71/698 (10.2) 8 (11.0) 26 (11.9)
   CRM and other metastases 168/798 (21.1) 10/100 (10.0) 158/698 (22.6) 8 (11.0) 29 (13.2)
   FNH/adenoma/hemangioma 223/798 (27.9) 37/100 (37.0) 186/698 (26.6) 30 (41.1) 75 (34.2)
   Others 28/798 (3.5) 5/100 (5.0) 23/68 (3.3) 3 (4.1) 7 (3.2)
Cirrhosis, n (%) 150 (18.8) 13 (13.0) 137 (19.6) 0.114 10 (13.7) 33 (15.1) 0.774
Child-Pugh score, n (%) 0.047 0.795
   No cirrhosis 651 (81.5) 87 (87.0) 564 (80.7) 63 (86.3) 186 (84.9)
   A 131 (16.4) 9 (9.0) 122 (17.5) 8 (11.0) 29 (13.2)
   B 17 (2.1) 4 (4.0) 13 (1.9) 2 (2.7) 4 (1.8)
Portal hypertension, n (%) 15/795 (1.9) 4/100 (4.0) 11/698 (1.6) 0.097 2 (2.7) 6 (2.7) 1.000
Median tumor size, mm [IQR] 110 [100–134] 115 [100–132] 110 [100–135] 0.585 115 [100–135] 110 [100–130] 0.340
Multiple tumors, n (%) 140 (17.5) 11 (11.0) 129 (18.5) 0.067 10 (13.7) 31 (14.2) 0.922
Multiple resections, n (%) 49 (6.1) 3 (3.0) 46 (6.6) 0.163 3 (4.1) 15 (6.8) 0.411
Concomitant operation excluding cholecystectomy, n (%) 94 (11.8) 10 (10.0) 84 (12.0) 0.558 8 (11.0) 21 (9.6) 0.733
Major resection (minimally-invasive criteria), n (%) 466 (58.3) 61 (61.0) 405 (57.9) 0.562 46 (63.0) 137 (62.6) 0.945
Iwate score, n (%) 0.278 0.989
   Low 21/797 (2.6) 1/100 (1.0) 20/697 (2.9) 1 (1.4) 4 (1.8)
   Intermediate 241/797 (30.2) 24/100 (24.0) 217/697 (31.1) 16 (21.9) 50 (22.8)
   High 154/797 (19.3) 23/100 (23.0) 131/697 (18.8) 15 (20.6) 46 (21.0)
   Expert 381/797 (47.8) 52/100 (52.0) 329/697 (47.2) 41 (56.2) 119 (54.3)
IMM difficulty, n (%) 0.353 0.742
   I 254 (31.8) 26 (26.0) 228 (32.6) 16 (21.9%) 51 (23.3)
   II 11 (23.9) 28 (28.0) 163 (23.3) 17 (23.3%) 59 (26.9)
   III 354 (44.3) 46 (46.0) 308 (44.1) 40 (54.8%) 109 (49.8)
Type of resection, n (%) 0.070 0.993
   Wedge anterolateral 46 (5.8) 4 (4.0) 42 (6.0) 4 (5.5) 15 (6.8)
   Wedge posterosuperior 25 (3.1) 8 (8.0) 17 (2.4) 3 (4.1) 12 (5.5)
   Left lateral sectionectomy 183 (22.9) 14 (14.0) 169 (24.2) 9 (12.3) 24 (11.0)
   Segmentectomy anterolateral 53 (6.6) 8 (8.0) 45 (6.4) 6 (8.2) 23 (10.5)
   Left hepatectomy 139 (17.4) 20 (20.0) 119 (17.0) 11 (15.1) 37 (16.9)
   Segmentectomy posterosuperior 27 (3.4) 5 (5.0) 22 (3.1) 5 (6.8) 8 (3.7)
   Right hepatectomy 228 (28.5) 27 (27.0) 201 (28.8) 23 (31.5) 66 (30.1)
   Extended right hepatectomy 31 (3.9) 3 (3.0) 28 (4.0) 3 (4.1) 9 (4.1)
   Right posterior sectionectomy 43 (5.4) 7 (7.0) 36 (5.2) 6 (8.2) 16 (7.3)
   Right anterior sectionectomy/central hepatectomy 13 (1.6) 3 (3.0) 10 (1.4) 2 (2.7) 7 (3.2)
   Extended left hepatectomy 11 (1.4) 1 (1.0) 10 (1.4) 1 (1.4) 2 (0.9)

RLR, robotic liver resection; LLR, laparoscopic liver resection; IQR, interquartile range; ASA, American Society of Anesthesiologists; BMI, body mass index; HCC, hepatocellular carcinoma; CRM, colorectal metastases; FNH, focal nodular hyperplasia; IMM, Institute Mutualiste Montsouris.

In the unmatched cohorts, comparisons of patient characteristics and peri-operative outcomes between patients were performed using the Mann-Whitney U test and Pearson’s χ2 test for continuous and categorical variables respectively. Comparisons in the matched cohorts took into account the paired nature of the data; hence, mixed-effects quantile regression (with a random-effects denoting matched sets) and conditional logit regression were used in 1:3 matched analyses of continuous and binary data respectively. Statistical analyses were done in Stata version 16.0 (StataCorp), and nominal P<0.05 were considered to indicate statistical significance.

Results

Comparison between RLR vs. LLR for huge tumors in the entire unmatched and matched cohort

Seven hundred and ninety-nine cases met study selection criteria of which 100 underwent RLR and 699 underwent LLR during the study period. LLR group patient was associated with significantly more previous abdominal surgery (P=0.006), more malignant pathology (P=0.010), more liver cirrhosis (P=0.047) and more median blood loss (300 vs. 200 mL, P=0.018) (Tables 1,2).

Table 2

Comparison between perioperative outcomes of RLR vs. LLR for huge (≥10 cm) tumors

Perioperative outcomes Unmatched cohort 1:3 propensity-score matching
Overall (n=799) RLR (n=100) LLR (n=699) P value RLR (n=73) LLR (n=219) P value
Median operating time [IQR], min 270 [190–346] 236 [176–337] 270 [193–349] 0.256 242 [197–359] 290 [210–360] 0.286
Median blood loss [IQR], mL 300 [150–300] 200 [100–500] 300 [150–500] 0.018 200 [100–500] 300 [110–500] 0.694
Blood loss (categories), n/n (%), mL 0.720 0.511
   <500 536/742 (72.2) 73/99 (73.7) 463/643 (72.0) 50/72 (69.4) 149/204 (73.0)
   ≥500 206/742 (27.8) 26/99 (26.3) 180/643 (28.0) 22/72 (30.6) 55/204 (27.0)
Intraoperative blood transfusion, n/n (%) 140/797 (17.6) 15/100 (15.0) 125/697 (17.9) 0.471 14/73 (19.2) 37/219 (16.9) 0.652
Pringle maneuver applied, n/n (%) 424/769 (55.1) 56/100 (56.0) 368/669 (55.0) 0.852 40/73 (54.8) 131/212 (61.8) 0.264
Median Pringle duration when applied [IQR], min 40 [24–60] 40 [20–60] 40 [24–60] 0.738 45 [26–60] 45 [30–61] 0.745
Open conversion, n (%) 105 (13.1) 8 (8.0) 97 (13.9) 0.104 6/73 (8.2) 24/219 (11.0) 0.519
Median postoperative stay [IQR], days 6 [4–8] 6 [4–8] 6 [4–8] 0.505 6 [4–9] 6 [4–7] 0.435
30-day readmission, n/n (%) 40/789 (5.1) 3/100 (3.0) 37/689 (5.4) 0.313 2/73 (2.7) 17/217 (7.8) 0.133
Postoperative morbidity, n (%) 190 (23.8) 26 (26.0%) 164 (23.5) 0.577 21/73 (28.8) 48/219 (21.9) 0.221
Major morbidity (Clavien-Dindo grade >2), n (%) 72 (9.0) 4 (4.0) 68 (9.7) 0.061 3/73 (4.1) 21/219 (9.6) 0.152
Reoperation, n (%) 17 (2.1) 0 (0.0) 17 (2.4) 0.115 0/73 (0.0) 3/219 (1.4) 0.576
In-hospital mortality, n (%) 11 (1.4) 0 (0.0) 11 (1.6) 0.207 0/73 (0.0) 4/219 (1.8) 0.575
90-day mortality, n (%) 16 (2.0) 0 (0.0) 16 (2.3) 0.126 0/73 (0.0) 6/219 (2.7) 0.342
Close/involved margins (≤1 mm) for malignancies, n/n (%) 88/557 (15.8) 9/59 (15.3) 79/498 (15.9) 0.935 7/41 (17.1) 31/139 (22.3) 0.654

RLR, robotic liver resection; LLR, laparoscopic liver resection; IQR, interquartile range.

PSM and inverse probability of treatment-weighting (IPTW) were performed using the same demographic data criteria as mentioned above to develop propensity-scores. After 1:3 PSM with 73 patients in the RLR arm and 219 patients in the LLR arm, both groups had comparable preoperative co morbid condition, liver function, tumour size, numbers and stage of disease.

RLR and LLR were associated with no significant difference in median operation time (242 vs. 290 min, P=0.286), transfusion rate (19.2% vs. 16.9%, P=0.652), median blood loss (200 vs. 300 mL, P=0.694), morbidity (28.8% vs. 21.9%, P=0.221), major morbidity (4.1% vs. 9.6%, P=0.152), frequency of Pringle maneuver application (54.8% vs. 61.8%, P=0.264) and postoperative length of stay (6 vs. 6 days, P=0.435).

There were 4 in-hospital mortalities in the LLR group (1.8%) and 0 hospital mortality in the RLR group (P=0.57). The major morbidity rate (Clavien-Dindo grade >2) was 9.6% vs. 4.1% respectively (P=0.152). The most common major morbidities in the LLR group included bile leak (n=19), postoperative collection (n=13), pulmonary complications (n=14), postoperative liver failure (n=6), postoperative bleeding (n=5) and wound complications (n=2). The major morbidities in the RLR group included bile leak (n=2) and postoperative collection (n=2). All these results are summarized in Tables 1,2.

Discussion

In the current analysis after 1:3 PSM, we observed no significant difference with regards to the key perioperative outcomes such as open conversion rate, blood loss, blood transfusion rate, morbidity, major morbidity and postoperative stay between RLR and LLR for huge liver tumors.

We had previously published an international multicenter study on the application of MILR for huge liver tumours showed that with careful patient selection, MILR could be performed safely in this subset of patients. Many participating specialized centers with expertise had demonstrated the feasibility and safety of resecting huge liver tumours by the minimally invasive approach (20). In the study, comparison between MILR for 174 huge tumors with 174 large (3–9.9 cm) tumors demonstrated not unexpectedly poorer outcomes in terms of blood loss, major morbidity and length of stay. However, the perioperative outcomes of MILR for huge tumors compared favourably with previous studies reporting on open LR for huge tumours (20).

More recently, the use of the robotic platform to facilitate LR has been advocated by several centers. It has been suggested that the use of robotic assistance may decrease the learning curve and increase the application of minimally invasive approach for LR (21-26). Hence with these results in mind, we performed the present analysis to determine if RLR was associated with any advantages over LLR in the subset patients with huge liver tumors.

LR for huge tumors larger than 10 cm was traditionally considered a contraindication for the minimally invasive approach. However as demonstrated in this study; with increasing experience, expert centers have now pushed the limits and MILR for huge tumors is no longer a rarity. Over 75% of the patients in this study were classified as of high or expert difficulty according to the Iwate system. The potential advantages of the minimally invasive approach are illustrated in the current analysis as shown by the low blood transfusion, morbidity and mortality rate. During conventional open LR, a large muscle-cutting upper abdominal wound is required in order to provide adequate exposure for meticulous dissection and haemostasis especially for huge tumours. During the minimally invasive approach, some may argue that a generous incision is still required for specimen delivery. However, the surgical incision may be transferred from an upper abdominal to a lower abdominal incision (Pfannenstiel or lower midline) resulting in less pain and better cosmesis. This may also potentially result in a reduction in pulmonary complications (8).

During MILR, it is well-known that pneumoperitoneum may reduce blood loss especially from the hepatic vein tributaries. This was supported in the present study, whereby the median blood loss after MILR for huge tumours was only 300 mL. This finding compared favorably with a recent publication on open hepatectomy for huge tumours (27).

It must be highlighted that performing MILR for huge liver tumours is extremely technically challenging and should only be performed by highly experienced expert surgeons. Numerous challenges resulting from the space-occupying effect of the huge lesion, include distortion of the normal anatomy, compression of the major portal pedicles, compression of hepatic veins leading to higher venous pressure, limited space for manipulation during surgery, development of large collateral vessels supplying the tumor and presence of tumour invasion or adhesions to adjacent structures. These challenges increase the risk of intraoperative complications such as major bleeding, tumor rupture or compromise in surgical margins (20,28).

The adoption of RLR has been increasing in recent years due to its potential advantages such as the seven degrees of freedom of the robotic system which may theoretically overcome the difficulties arising from rigid laparoscopic instruments. Robotic instruments may also facilitate the fine extrahepatic hilar dissection of individual hepatic artery and portal vein in major LR particularly when the anatomy is distorted. It may also enhance the dissection and control of short hepatic veins in the hepatocaval region and allows easier suture plication of bleeders during parenchymal transection (29). In addition, RLR is more ergonomic for the surgeon which may reduce the physical or musculoskeletal stress of surgeons and in the long run may reduce technical error as a result of human fatigue (23,30,31).

Presently, increasing evidence in the literature has demonstrated that RLR is associated with a shorter learning curve compared LLR (32-34) and it may also allow an increased proportion of hepatectomies at advanced difficulty level to be completed via purely minimally invasive approach (21,24,26,32). However, it has to be highlighted that the learning curve is unlikely to be a major confounder in this study as surgeons are less likely to attempt resections for huge tumors during their early experience. The major limitation of robotic surgery compared to laparoscopy include the limited access and availability to the platform and relative high costs of the operation (24,26,32,35). Furthermore, the choice of operating instruments specifically for liver surgery are more limited when compared to laparoscopy. Specifically, the Cavitron Ultrasonic Surgical Aspirator (CUSA) is not available in the robotic platform. However, with the introduction of several new models of surgical robots in the market, it can be anticipated that the barrier to access and cost of the robotic platform would likely decrease (22,23,35).

The main limitation of the current study is its retrospective nature and its associated biases. Despite matching, selection bias may have still have confounded the results observed. Furthermore, since this was a multi-center comparative study, there were differences in the institution or individual surgeon’s MILR experience and surgical techniques deployed during MILR. Unfortunately, detailed information about individual surgeon experience was not available from this database. However, the heterogeneity in the surgical technique adopted by the different centers. enhances the external validity and generalizability of these findings as it reflects current real-world practice.

Conclusions

MILR can be safely performed in selected patients with huge liver tumours with excellent outcomes. There was no significant difference in perioperative outcomes after RLR and LLR for huge liver tumors.

Acknowledgments

Funding: Dr. T. P. Kingham was partially supported by the US National Cancer Institute MSKCC Core Grant number P30 CA00878 for this study.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-22-283/rc

Data Sharing Statement: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-22-283/dss

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-22-283/coif). FR reports speaker fees and support outside the submitted work from Integra, Medtronic, Olympus, Corza, Sirtex and Johnson & Johnson. MVM is a consultant for CAVA robotics LLC. JP reports a research grant from Intuitive Surgical Deutschland GmbH and personal fees or nonfinancial support from Johnson & Johnson, Medtronic, AFS Medical, Astellas, CHG Meridian, Chiesi, Falk Foundation, La Fource Group, Merck, Neovii, NOGGO, pharma-consult Peterson, and Promedicis and serves as the unpaid editorial board member of Hepatobiliary Surgery and Nutrition. BKPG has received travel grants and honorarium from Johnson and Johnson, Olympus and Transmedic the local distributor for the Da Vinci Robot. HSH, MAH and LA serve as the unpaid editorial board members of Hepatobiliary Surgery and Nutrition. The other 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. The study was performed in accordance with the Declaration of Helsinki (as revised in 2013). This retrospective study on anonymized patient data was approved by the Singapore General Hospital Institution Review Board (No. 2020/2802) and the need for any further board review and patient consent was waived.

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/.

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Cite this article as: Cheung TT, Liu R, Cipriani F, Wang X, Efanov M, Fuks D, Choi GH, Syn NL, Chong CCN, Di Benedetto F, Robles-Campos R, Mazzaferro V, Rotellar F, Lopez-Ben S, Park JO, Mejia A, Sucandy I, Chiow AKH, Marino MV, Gastaca M, Lee JH, Kingham TP, D’Hondt M, Choi SH, Sutcliffe RP, Han HS, Tang CN, Pratschke J, Troisi RI, Wakabayashi G, Cherqui D, Giuliante F, Aghayan DL, Edwin B, Scatton O, Sugioka A, Long TCD, Fondevila C, Abu Hilal M, Ruzzenente A, Ferrero A, Herman P, Chen KH, Aldrighetti L, Goh BKP; International robotic and laparoscopic liver resection study group investigators. Robotic versus laparoscopic liver resection for huge (≥10 cm) liver tumors: an international multicenter propensity-score matched cohort study of 799 cases. HepatoBiliary Surg Nutr 2023;12(2):205-215. doi: 10.21037/hbsn-22-283

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