Abstract
Both robotic and laparoscopic right anterior sectionectomy and central hepatectomy can be performed safely in expert centres, with excellent outcomes. The robotic approach was associated with statistically significant less blood loss compared with laparoscopy, although the clinical relevance of this finding remains unclear.
Introduction
The role of minimally invasive major hepatectomy today is a hotly debated topic. It is viewed as an innovative procedure that should be performed only by experienced surgeons in specialist centres1–4. Right anterior sectionectomy and central hepatectomy for centrally located tumours are traditionally viewed as complex and technically demanding procedures with a higher perioperative morbidity rate, especially via a minimally invasive approach5,6. This post hoc analysis of databases (2010–2020) aimed to establish outcome data.
Results
Of a total of 9293 patients, 233 (2.5 per cent) underwent minimally invasive right anterior sectionectomy or central hepatectomy (48 robotic and 185). See Supplementary methods, Tables S1–S3 and Figs S1–S5 for methods, definitions, surgical technique, inclusion criteria, definitions, and statistical methods7–9. Baseline clinicopathological characteristics and perioperative outcomes for both cohorts are summarized in Tables 1 and 2. Although hepatocellular carcinoma was the most common indication overall, patients undergoing robotic surgery were more likely to have other pathology (perhaps indicating selection). The distribution of minimally invasive resections was stable over time (Figs S6–S8).
Table 1.
Comparison of baseline clinicopathological characteristics in patients undergoing robotic versus laparoscopic right anterior sectionectomy and central hepatectomy
| Unmatched cohort | 1 : 2 propensity-matched cohort | 1 : 1 propensity-matched cohort | |||||||
|---|---|---|---|---|---|---|---|---|---|
| R-RAS/CH (n = 48) | L-RAS/CH (n = 185) | P† | R-RAS/CH (n = 34) | L-RAS/CH (n = 68) | P‡ | R-RAS/CH (n = 40) | L-RAS/CH (n = 40) | P§ | |
| Age (years)* | 60 (51–67) | 63 (56–70) | 0.034 | 61 (54–70) | 62 (55–68) | 0.712 | 62 (55–68) | 62 (54–72) | 0.630 |
| Men | 37 of 48 (77.1) | 142 of 185 (76.8) | 0.962 | 28 of 34 (82.4) | 57 of 68 (83.8) | 0.855 | 32 of 40 (80.0) | 33 of 40 (82.5) | 0.901 |
| ASA grade | 0.587 | 0.888 | 0.881 | ||||||
| I | 8 of 48 (16.7) | 19 of 185 (10.3) | 4 of 34 (11.8) | 9 of 68 (13.2) | 5 of 40 (12.5) | 5 of 40 (12.5) | |||
| II | 29 of 48 (60.4) | 125 of 185 (67.6) | 20 of 34 (58.8) | 42 of 68 (61.8) | 24 of 40 (60.0) | 22 of 40 (55.0) | |||
| III | 11 of 48 (22.9) | 40 of 185 (21.6) | 10 of 34 (29.4) | 17 of 68 (25.0) | 11 of 40 (27.5) | 13 of 40 (32.5) | |||
| IV | 0 of 48 (0) | 1 of 185 (0.5) | 0 of 34 (0) | 0 of 68 (0) | 0 of 40 (0) | 0 of 40 (0) | |||
| Right anterior sectionectomy | 36 of 48 (75.0) | 118 of 185 (63.8) | 0.144 | 26 of 34 (76.5) | 52 of 68 (76.5) | 1.000 | 30 of 40 (75.0) | 32 of 40 (80.0) | 0.800 |
| Central hepatectomy | 12 of 48 (25.0) | 67 of 185 (36.2) | 8 of 34 (23.5) | 16 of 68 (23.5) | 10 of 40 (25.0) | 8 of 40 (20.0) | |||
| Previous abdominal surgery | 12 of 48 (25.0) | 60 of 185 (32.4) | 0.321 | 10 of 24 (29.4) | 20 of 68 (29.4) | 1.000 | 11 of 40 (27.5) | 13 of 40 (32.5) | 0.683 |
| Previous liver surgery | 3 of 48 (6.3) | 13 of 185 (7.0) | 0.850 | 3 of 34 (8.8) | 3 of 68 (4.4) | 0.396 | 3 of 40 (7.5) | 2 of 40 (5.0) | 0.655 |
| Malignant pathology | 41 of 48 (85.4) | 181 of 185 (97.8) | < 0.001 | 33 of 34 (97.1) | 66 of 68 (97.1) | 1.000 | 38 of 40 (95.0) | 38 of 40 (95.0) | 1.000 |
| Pathological type | 0.003 | 0.786 | 0.896 | ||||||
| HCC | 26 of 48 (54.2) | 125 of 185 (67.6) | 23 of 34 (67.7) | 47 of 68 (69.1) | 25 of 40 (62.5) | 27 of 40 (67.5) | |||
| CRM | 7 of 48 (14.6) | 39 of 185 (21.1) | 6 of 34 (17.7) | 14 of 68 (20.6) | 7 of 40 (17.5) | 6 of 40 (15.0) | |||
| Others | 15 of 48 (31.3) | 21 of 185 (11.4) | 5 of 34 (14.7) | 7 of 68 (10.3) | 8 of 40 (20.0) | 7 of 40 (17.5) | |||
| Cirrhosis | 19 of 48 (39.6) | 81 of 185 (43.8) | 0.600 | 15 of 34 (44.1) | 31 of 68 (45.6) | 0.892 | 18 of 40 (45.0) | 19 of 40 (47.5) | 0.869 |
| Child–Pugh grade | 0.058 | 0.892 | 0.974 | ||||||
| No cirrhosis | 29 of 48 (60.4) | 104 of 185 (56.2) | 19 of 34 (55.9) | 37 of 68 (54.4) | 22 of 40 (55.0) | 21 of 40 (52.5) | |||
| A | 16 of 48 (33.3) | 79 of 185 (42.7) | 15 of 34 (44.1) | 31 of 68 (45.6) | 16 of 40 (40.0) | 17 of 40 (42.5) | |||
| B | 3 of 48 (6.3) | 2 of 185 (1.1) | 0 of 34 (0) | 0 of 68 (0) | 2 of 40 (5.0) | 2 of 40 (5.0) | |||
| Portal hypertension | 4 of 48 (8.3) | 14 of 185 (7.6) | 0.859 | 1 of 34 (2.9) | 5 of 68 (7.4) | 0.403 | 3 of 40 (7.5) | 3 of 40 (7.5) | 1.000 |
| Tumour size (mm)* | 40 (30–50) | 34 (26–50) | 0.221 | 38 (29–47) | 35 (30–51) | 0.649 | 38 (30–49) | 35 (30–50) | 0.524 |
| Multiple tumours | 9 of 48 (18.8) | 45 of 185 (24.3) | 0.415 | 6 of 34 (17.6) | 16 of 68 (23.5) | 0.507 | 7 of 40 (17.5) | 10 of 40 (25.0) | 0.467 |
| Multiple resections | 0 of 48 (0) | 14 of 185 (7.6) | 0.049 | 0 of 34 (0) | 0 of 68 (0) | 1.000 | 0 of 40 (0) | 0 of 40 (0) | 1.000 |
| Concomitant operation, not cholecystectomy | 7 of 48 (14.6) | 10 of 185 (5.4) | 0.029 | 2 of 34 (5.9) | 6 of 68 (8.8) | 0.489 | 5 of 40 (12.5) | 6 of 40 (15.0) | 0.763 |
| Iwate score | 0.291 | 0.865 | 0.628 | ||||||
| Low | 0 of 48 (0) | 0 of 185 (0) | 0 of 34 (0) | 0 of 68 (0) | 0 of 40 (0) | 0 of 40 (0) | |||
| Intermediate | 0 of 48 (0) | 0 of 185 (0) | 0 of 34 (0) | 0 of 68 (0) | 0 of 40 (0) | 0 of 40 (0) | |||
| High | 8 of 48 (16.7) | 44 of 185 (23.8) | 7 of 34 (20.6) | 15 of 68 (22.1) | 8 of 32 (20.0) | 4 of 40 (10.0) | |||
| Expert | 40 of 48 (83.3) | 141 of 185 (76.2) | 27 of 34 (79.4) | 53 of 68 (77.9) | 32 of 40 (80.0) | 36 of 40 (90.0) | |||
Values in parentheses are percentages unless indicated otherwise; *values are median (i.q.r.). R-RAS/CH, robotic right anterior sectionectomy/central hepatectomy; L-RAS/CH, laparoscopic right anterior sectionectomy/central hepatectomy; HCC, hepatocellular carcinoma; CRM, colorectal cancer metastases. †From unpaired analyses i.e. Mann-Whitney U test and Pearson's chi-square test; ‡From Wilcoxon signed rank test and McNemar's chi-square test; §From mixed-effects quantile regression (in which a random-effects parameter was used to denote the 1:2 matched data structure), conditional logistic, or mixed-effects ordinal logistic regression.
Table 2.
Comparison of perioperative outcomes after robotic versus laparoscopic right anterior sectionectomy and central hepatectomy
| Entire unmatched cohort | 1 : 2 propensity-matched cohort | 1 : 1 propensity-matched cohort | |||||||
|---|---|---|---|---|---|---|---|---|---|
| R-RAS/CH (n = 48) | L-RAS/CH (n = 185) | P† | R-RAS/CH (n = 34) | L-RAS/CH (n = 68) | P‡ | R-RAS/CH (n = 40) | L-RAS/CH (n = 40) | P§ | |
| Duration of operation (min)* | 307 (209–496) | 315 (231–435) | 0.776 | 355 (248–530) | 285 (210–365) | 0.047 | 339 (228–505) | 298 (210–358) | 0.133 |
| Blood loss (ml)* | 200 (100–500) | 371 (200–650) | < 0.001 | 200 (100–500) | 300 (192–700) | 0.020 | 200 (100–500) | 350 (200–725) | 0.019 |
| Intraoperative blood transfusion | 5 of 48 (10.4) | 31 of 185 (16.8) | 0.279 | 4 of 34 (11.8) | 12 of 68 (17.6) | 0.418 | 4 of 40 (10.0) | 9 of 40 (22.5) | 0.166 |
| Pringle manoeuvre applied | 29 of 48 (60.4) | 123 of 185 (66.5) | 0.431 | 18 of 34 (52.9) | 47 of 68 (69.1) | 0.082 | 21 of 40 (52.5) | 32 of 40 (80.0) | 0.131 |
| Median duration of Pringle manoeuvre when applied (min)* | 60 (38–82) | 60 (30–98) | 0.902 | 75 (50–89) | 60 (30–100) | 0.582 | 61 (50–84) | 63 (53–98) | 0.853 |
| Conversion to open surgery | 2 of 48 (4.2) | 11 of 185 (5.9) | 0.632 | 2 of 34 (5.9) | 3 of 68 (4.4) | 0.753 | 2 of 40 (5.0) | 2 of 40 (5.0) | 1.000 |
| Duration of postoperative hospital stay (days)* | 7 (5–10) | 8 (6–12) | 0.217 | 8 (6–11) | 7 (6–10) | 0.580 | 7 (6–11) | 8 (5–10) | 0.853 |
| 30-day readmission | 2 of 48 (4.2) | 7 of 184 (3.8) | 0.908 | 1 of 34 (2.9) | 3 of 68 (4.4) | 0.726 | 1 of 40 (2.5) | 4 of 40 (10.0) | 0.180 |
| Postoperative morbidity | 9 of 48 (18.8) | 62 of 185 (33.5) | 0.048 | 8 of 34 (23.5) | 20 of 68 (29.4) | 0.548 | 8 of 40 (20.0) | 14 of 40 (35.0) | 0.201 |
| Major morbidity (Clavien–Dindo grade > II) | 3 of 48 (6.3) | 13 of 185 (7.0) | 0.850 | 2 of 34 (5.9) | 2 of 68 (2.9) | 0.488 | 2 of 40 (5.0) | 2 of 40 (5.0) | 1.000 |
| Reoperation | 1 of 48 (2.1) | 2 of 185 (1.1) | 0.583 | 1 of 34 (2.9) | 0 of 68 (0) | 0.155 | 1 of 40 (2.5) | 0 of 40 (0) | 0.317 |
| 30-day mortality | 1 of 48 (2.1) | 1 of 185 (0.5) | 0.302 | 1 of 34 (2.9) | 0 of 68 (0) | 0.155 | 1 of 40 (2.5) | 0 of 40 (0) | 0.317 |
| In-hospital mortality | 1 of 48 (2.1) | 1 of 185 (0.5) | 0.302 | 1 of 34 (2.9) | 0 of 68 (0) | 0.155 | 1 of 40 (2.5) | 0 of 40 (0) | 0.317 |
| 90-day mortality | 2 of 48 (4.2) | 2 of 185 (1.1) | 0.143 | 2 of 34 (5.9) | 0 of 68 (0) | 0.109 | 2 of 40 (5.0) | 1 of 40 (0) | 0.157 |
| Close/involved margins (≤ 1 mm) for malignancies | 6 of 48 (12.5) | 31 of 185 (16.8) | 0.472 | 6 of 33 (18.2) | 13 of 66 (19.7) | 0.850 | 6 of 38 (15.8) | 8 of 38 (21.1) | 0.791 |
Values in parentheses are percentages unless indicated otherwise; *values are median (i.q.r.). R-RAS/CH, robotic right anterior sectionectomy/central hepatectomy; L-RAS/CH, laparoscopic right anterior sectionectomy/central hepatectomy. †From unpaired analyses i.e. Mann-Whitney U test and Pearson's chi-square test; ‡From Wilcoxon signed rank test and McNemar's chi-square test; §From mixed-effects quantile regression (in which a random-effects parameter was used to denote the 1:2 matched data structure), conditional logistic, or mixed-effects ordinal logistic regression.
Patients suitable for robotic surgery had less blood loss and morbidity than those having other approaches, but a similar duration of hospital stay, and rates of conversion and reoperation. Blood loss was lower with robotic surgery, even with propensity score matching, but it was not a clinically significant difference. No differences in transfusion requirements were observed as a result.
Discussion
A steep learning curve has proven to be a major stumbling block in widespread application of minimally invasive liver resection10–12. There is some evidence that robotic platforms may be beneficial at the expense of higher costs13–18. Right anterior and central resections are two of the most technically demanding owing to wide parenchymal planes with close proximity to critical structures and major vessels5,6,19. Those suitable for minimal access approaches have less blood loss, a shorter postoperative hospital stay, and lower morbidity, but longer operating times5,6,19. Both procedures were associated with a relatively low volume of blood loss in the present study, and it was better in the robotic group. It is likely that experienced surgeons with a special interest would have performed the robotic resections in selected patients20.
There is an inherent risk of confounding bias with a relatively small sample size in this study. The relatively long time period inevitably confounds results, given the rapid and significant improvements in surgical technology and perioperative care over time. Nonetheless, there was no significant difference in the proportion of robotic versus laparoscopic approaches performed over time. There was no patient selection or operative standardization, but the multicentre study provides validity to the results.
Supplementary Material
Disclosure
B.K.P.G. has received travel grants and honoraria from Johnson and Johnson and Transmedic, the local distributor for the Da Vinci® robot. M.V.M. is a consultant for CAVA Robotics. J.P. reports a research grant from Intuitive Surgical Deutschland, and personal fees or non-financial support from Johnson & Johnson, Medtronic, AFS Medical, Astellas, CHG Meridian, Chiesi, Falk Foundation, La Fource Group, Merck, Neovii, NOGGO, pharma-consult Peterson, and Promedicis. M.S. (collaborator) reports personal fees or other support outside of the submitted work from Merck, Bayer, ERBE, Amgen, Johnson & Johnson, Takeda, Olympus, Medtronic, and Intuitive. F.R. reports speaker fees and support outside the submitted work from Integra, Medtronic, Olympus, Corza, Sirtex and Johnson & Johnson.
Contributor Information
Hye Yeon Yang, Division of Hepatopancreatobiliary Surgery, Department of Surgery, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea.
Gi Hong Choi, Division of Hepatopancreatobiliary Surgery, Department of Surgery, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea.
Ken-Min Chin, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital, Singapore.
Sung Hoon Choi, Department of General Surgery, CHA Bundang Medical Centre, CHA University School of Medicine, Seongnam, Korea.
Nicholas L. Syn, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Tan-To Cheung, Department of Surgery, Queen Mary Hospital, University of Hong Kong, Hong Kong, China.
Adrian K. H. Chiow, Hepatopancreatobiliary Unit, Department of Surgery, Changi General Hospital, Singapore
Iswanto Sucandy, AdventHealth Tampa, Digestive Health Institute, Tampa, Florida, USA.
Marco V. Marino, General Surgery Department, Azienda Ospedaliera Ospedali Riuniti Villa Sofia-Cervello, Palermo, Italy Oncologic Surgery Department, P. Giaccone University Hospital, Palermo, Italy.
Mikel Prieto, Hepatobiliary Surgery and Liver Transplantation Unit, Biocruces Bizkaia Health Research Institute, Cruces University Hospital, University of the Basque Country, Bilbao, Spain.
Charing C. Chong, Division of Hepatobiliary and Pancreatic Surgery, Department of Surgery, Prince of Wales Hospital, Chinese University of Hong Kong, New Territories, Hong Kong, China
Jae Hoon Lee, Department of Surgery, Division of Hepato-Biliary and Pancreatic Surgery, Asan Medical Centre, University of Ulsan College of Medicine, Seoul, Korea.
Mikhail Efanov, Department of Hepato-Pancreato-Biliary Surgery, Moscow Clinical Scientific Centre, Moscow, Russia.
T. Peter Kingham, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Robert P. Sutcliffe, Department of Hepatopancreatobiliary and Liver Transplant Surgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK
Roberto I. Troisi, Department of Clinical Medicine and Surgery, Division of Hepato-Pancreato-Biliary, Minimally Invasive and Robotic Surgery, Federico II University Hospital Naples, Naples, Italy
Johann Pratschke, 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.
Xiaoying Wang, Department of Liver Surgery and Transplantation, Liver Cancer Institute, Zhongshan Hospital, Fudan University, Shanghai, China.
Mathieu D’Hondt, Department of Digestive and Hepatobiliary/Pancreatic Surgery, Groeninge Hospital, Kortrijk, Belgium.
Chung Ngai Tang, Department of Surgery, Pamela Youde Nethersole Eastern Hospital, Hong Kong, China.
Rong Liu, Faculty of Hepatopancreatobiliary Surgery, First Medical Centre of Chinese People’s Liberation Army General Hospital, Beijing, China.
James O. Park, Hepatobiliary Surgical Oncology, Department of Surgery, University of Washington Medical Center, Seattle, Washington, USA
Fernando Rotellar, Hepatopancreatobiliary and Liver Transplant Unit, Department of General Surgery, Clinica Universidad de Navarra, Universidad de Navarra, Pamplona, Spain; Institute of Health Research of Navarra (IdisNA), Pamplona, Spain.
Olivier Scatton, Department of Digestive, Hepato-biliary-pancreatic and Liver Transplantation, Hôpital Pitie-Salpetriere, AP-HP, Sorbonne Université, Paris, France.
Atsushi Sugioka, Department of Surgery, Fujita Health University School of Medicine, Aichi, Japan.
Tran Cong Duy Long, Department of Hepatopancreatobiliary Surgery, University Medical Center, University of Medicine and Pharmacy, Ho Chi Minh City, Vietnam.
Chung-Yip Chan, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and Duke National University of Singapore Medical School, Singapore.
David Fuks, Department of Digestive, Oncologic and Metabolic Surgery, Institute Mutualiste Montsouris, Université Paris Descartes, Paris, France.
Ho-Seong Han, Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Korea.
Brian K. P. Goh, Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and Duke National University of Singapore Medical School, Singapore
Collaborators
M. D’Silva (Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Korea); H. Schotte (Groeninge Hospital, Kortrijk, Belgium); C. De Meyere (Groeninge Hospital, Kortrijk, Belgium); E.C. Lai (Pamela Youde Nethersole Eastern Hospital, Hong Kong, China); F. Krenzien (Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany); M. Schmelzle (Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany); P. Kadam (University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK); R. Montalti (Federico II University Hospital Naples, Naples, Italy); M. Giglio (Federico II University Hospital Naples, Naples, Italy); Q. Liu (the First Medical Centre of Chinese People’s Liberation Army General Hospital, Beijing, China); K.F. Lee (Prince of Wales Hospital, Chinese University of Hong Kong, New Territories, Hong Kong, China); D. Salimgereeva (Moscow Clinical Scientific Centre, Moscow, Russia); R. Alikhanov (Moscow Clinical Scientific Centre, Moscow, Russia); L.S. Lee (Changi General Hospital, Singapore); M. Gastaca (Biocruces Bizkaia Health Research Institute, Cruces University Hospital, University of the Basque Country, Bilbao, Spain); J.Y. Jang (CHA Bundang Medical Centre, CHA University School of Medicine, Seongnam, Korea); C. Lim (Hopital Pitte-Salpetriere, Sourbonne Université, Paris, France); K.P. Labadie (University of Washington Medical Center, Seattle, Washington, USA); P.P. Nghia (University Medical Centre, Ho Chi Minh City, Vietnam); M. Kojima (Fujita Health University School of Medicine, Aichi, Japan); Y. Kato (Fujita Health University School of Medicine, Aichi, Japan).
Supplementary material
Supplementary material is available at BJS online.
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