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Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?
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Contents lists available at ScienceDirect
Laparoscopic, Endoscopic and Robotic Surgery journal homepage: www.keaipublishing.com/en/journals/ laparoscopic-endoscopic-and-robotic-surgery
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Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed? Sanjay Goja a, b, *, Sanjay Kumar Yadav a, Rohan Jagat Chaudhary a, Manoj Kumar Singh a, Arvinder Singh Soin a a b
Institute of Liver Transplantation and Regenerative Medicine, Medanta-The Medicity, Gurugram, 122001, India Program Director and Clinical Lead-Liver Transplant Narayan Health City, Bengaluru, India
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 June 2019 Received in revised form 1 August 2019 Accepted 11 August 2019 Available online xxx
Objective: The authors present outcomes of robotic liver resections in comparison with open technique questioning the need to have experience of laparoscopy for such procedures before transition to robotic assisted. Materials and methods: Retrospective review of liver resections done robotically from February 2015 to June 2017 compared to matched control cohort of open cases from January 2012 to December 2016. Results: Twenty-one patients in the study group were compared with matched control of 42 open cases (1:2 ratio). The types of procedure were similar in both the groups. There were 4 left lateral hepatectomy, 3 left hepatectomy, and 1 left hepatectomy with hepatico-jejunostomy, 3 right hepatectomy, 3 right posterior sectorectomy, 4 bisegmentectomy and 4 mono-segmentectomy. There were 9 patients with primary liver cancer, 2 each with liver metastasis and carcinoma gall bladder and 8 patients had benign liver disease. Mean blood loss was 370 ± 311 ml in the robotic group compared to 451 ± 330 ml in control group (p ¼ 0.06). Minor complications developed in 19% of robotic cases compared to 40% in open surgery, while major complications occurred in 4.7% of robotic cases compared to 7.1% of open cases. Mean hospital stay was 5.3 ± 0.8 days for the robotic group and 7.7 ± 4.2 days for open group (p ¼ 0.02). Local tumor recurrence occurred in 1 out of 13 resections done for malignancy in the robotic group and 7 out of 26 in the open group. Conclusion: This study highlights the utility of surgical robots for segmental and complex liver resections with equivalent outcomes and decreased length of stay compared to open surgery without having experience of same with the laparoscopy. © 2019 Sir Run Run Shaw Hospital affiliated to Zhejiang University School of Medicine. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
Keywords: Robotic Liver resection Open surgery
1. Introduction Minimal invasive surgery is a well-accepted alternative approach for resection of anterior liver segments and left lateral secterectomies.1e3 The well established advantages of minimal invasive liver surgery are less estimated blood loss and postoperative pain, lower morbidity, shorter hospital stay, improved cosmesis and equivalent oncological outcomes compared to traditional open surgery.2,4e6 There is mounting evidence on the utility
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* Corresponding author: Program Director and Clinical Lead-Liver Transplant Narayan Health City, Bengaluru, India. E-mail address: [email protected] (S. Goja).
of minimally invasive approaches for liver resection vis a vis laparoscopy and robotic platform with a recent tilt towards robotic surgery for complex and major hepatic resections.7,8 However, the inherent disadvantages of conventional laparoscopy have led to the evolution of robotic assisted liver surgery with an aim of overcoming the disadvantages of conventional laparoscopy. A spate of papers in the recent literature comparing robotic liver resections with laparoscopy have shown similar outcomes,4,5,9e11 preceded by papers comparing laparoscopic with open liver resections.2,12e16 The increasing popularity of robotic liver surgery is evident by the constantly growing number of reports in the literature. The authors present a comparative study of robotic cases compared with matched open liver resections in 1:2 ratio.
https://doi.org/10.1016/j.lers.2019.08.002 2468-9009/© 2019 Sir Run Run Shaw Hospital affiliated to Zhejiang University School of Medicine. Published by Elsevier B.V. This is an open access article under the CC BYNC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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rates of patients operated for hepatocellular carcinoma (HCC) were calculated using KaplaneMeier methods, and differences between the curves were calculated using log-rank test. For all statistical analysis, p 0.05 was considered as statistically significant. This study was approved by the institutional review board of the hospital, and data acquisition and database maintenance were complaint with institutional guidelines.
2. Materials and methods A retrospective review of liver resections done robotically using the da Vinci platform Si (Intuitive Surgical Inc., Milford, CT, USA) from February 2015 to June 2017 compared with matched control open cases in 1:2 ratio from January 2012 to December 2016. This is a retrospective comparative study from a tertiary care hospital (Medanta, the Medicity, Delhi-NCR, India), a high volume liver transplantation and hepatobiliary surgery centre, comparing operative variables, post-operative outcomes (morbidity and mortality) and the length of hospital stay and recurrence. Consecutive robotic liver resection cases were compared to matched open liver resection cases by review of the hospital-based database. Hospital records were retrospectively reviewed for patient history and demographics, liver pathology, intraoperative as well as postoperative outcomes. Matching criteria included: number of resected liver segments, histology, age group and body mass index (BMI). Postoperative complications up to 30 days were obtained from discharge summaries and followed up the database and graded according to Clavien-Dindo classification scale.17 The study cohort was consecutive robotic liver resection cases done during the study period. There is no laparoscopic arm for comparison in the group. The authors have performed only non-anatomical left lateral, exophytic and easily accessible segment 6 liver resections by laparoscopy. So the matched control group in the laparoscopic arm couldn't be formed thus.
3. Results There were 21 patients in the robotic group, 10 females and 11 males with mean age of 43.5 ± 19.4 years old; their characteristics in comparison to 42 matched open cases are listed in Table 1. The groups were matched with no difference in age, gender, BMI, American Society of Anesthesiologists classification and distribution of malignant and benign disease. The percentage of cirrhotic patients (Child's A) were similar in both groups with 2 in the robotic group and 4 in the open group. The robotic group patient had 1 patient with Hepatitis C Virus (HCV) and 1 with Hepatitis B Virus (HBV) cirrhosis and the open group had 2 with HCV and 2 with HBV cirrhosis. The types of procedures were similar in both the groups (Table 2). There were 4 left lateral hepatectomy, 3 left hepatectomy, and 1 left hepatectomy with hepatico-jejunostomy, 3 right hepatectomy, 3 right posterior sectorectomy, 4 bisegmentectomy and 4 mono-segmentectomy. The intraoperative image of various steps of robotic liver resection are shown in Fig. 1(AeF). There were 9 patients with primary liver cancer, 2 each with liver metastasis and carcinoma gall bladder and 8 patients had benign liver disease. The mean operative duration was 442 ± 135 minutes in the robotic group compared to 357 ± 127 minutes in the open group (p ¼ 0.03); the mean operative blood loss was 370 ± 311 ml in the robotic group and 451 ± 330 ml in the open group (p ¼ 0.06). Four patients required intra-operative blood transfusion and there were no reexplorations in either group. There was no conversion to open in the present robotic study group.
2.1. Statistical analysis Study data were analyzed using SPSS (version 20.0; SPSS Inc, Chicago, IL). Groups were compared using Fisher's exact test for categorical variables, student t test for continuous parametric variables. Categorical variables are presented as whole numbers and percentages. Continuous parametric variables are presented as means ± SD. Continuous nonparametric variables are presented as medians with interquartile range. The cumulative overall survival
Table 1 Comparison of clinical profile of study population in robotic and open liver resection groups. Parameters
Robotic liver resections (n ¼ 21)
Open liver resections (n ¼ 42)
p
Age, years (Mean ± SD) Gender, n (%) Male Female BMI, kg/m2 (Mean ± SD) ASAa classification, n (%) 1 2 3 4 Pathology, n (%) Primary liver cancer Hepatocellular carcinoma Intrahepatic cholangiocarcinoma Liver metastasis Carcinoma stomach metastasis Colorectal liver metastasis Incidental carcinoma gall bladder post laparoscopic cholecystectomy Benign tumor Hemangioma Polycystic liver disease Recurrent primary Cholangitis Adenoma Cirrhosis, n (%) Child A None
43.5 ± 19.4
47.6 ± 16.3
0.43
11 (52.3) 10 (47.6) 24.12 ± 3.7
23 (54.8) 19 (45.2) 24.6 ± 2.8
1.00
4 (19.0) 14 (66.7) 3 (14.3) 0
8 (19.0) 21 (50.0) 12 (28.6) 1 (2.4)
9 7 2 2 1 1 2 8 4 2
18 (42.9) 14 4 4 (9.5) 0 4 4 (9.5) 16 (38.1) 8 4
a
(42.9)
(9.5)
(9.5) (38.1)
1 1
2 2
2 (9.5) 19 (90.5)
4 (9.5) 38 (90.5)
0.63 0.26
1.00
1.00
1.00 1.00
0.53
ASA: American Association of Anesthesiologist.
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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Table 2 Details of liver resection done by robotic and open approaches. Parameters Type of surgical procedures, n (%) Left lateral hepatectomy Left hemihepatectomy Right hemihepatectomy Bi- segmentectomy Segment 4b þ 5 Segment 5 þ 6 Right posterior secterectomy (segment 6 þ 7) Monosegmentectomy Additional procedure, n Hepatico-jejunostomy Blood loss, ml (Mean ± SD) Operative time, minutes (Mean ± SD) Blood transfusion (number of units) (Mean ± SD)
Robotic liver resections (n ¼ 21)
Open liver resections (n ¼ 42)
4 (19.0) 3 (14.3) 3 (14.3)
8 (19.0) 6 (14.3) 6 (14.3)
2 2 3 4
4 4 6 8
p 0.99
(9.5) (9.5) (14.3) (19.0)
1 370 ± 311 442 ± 135 0.67 ± 1.23
(9.5) (9.5) (14.3) (19.0)
0 451 ± 330 357 ± 127 0.79 ± 1.06
0.06 0.03 0.71
Fig. 1 The intraoperative image of various steps of robotic liver resection.
The histopathological characteristics of all patients operated for malignancy were shown in Table 3. The median tumor size in the robotic group was 6.4 ± 3.6 cm compared to 6.8 ± 4.1 cm in the open group (p ¼ 0.7), with negative resection margins in all 13 of the patients with tumor in the robotic arm and all 26 tumor patients in the open arm. Local tumor recurrence occurred in one out of 13 resections done for malignancy in the robotic group and 7 out of 26 in the open group; nonlocal recurrence occurred in 2 of 13 in the robotic group and 2 of 26 in the open group (Table 3). No significant difference in overall survival was observed among HCC patients (7 in robotic arm and 14 in open arm) operated using either robotic or open approach (log rank p ¼ 0.65). See Fig. 2. The morbidity in both the groups was compared based on Clavien-Dindo scale and described in Table 4. There were 19% minor complications (Clavien grade 1e2) in the robotic group and 40% in the open group. Major complications (Clavien grade 3 and higher) were 4.7% in the robotic group compared to 7.1% in the open group. The mean hospital length of stay was 5.3 ± 0.8 days in the robotic group, compared to 7.7 ± 4.2 days in the open group (p ¼ 0.02). The mean operative cost in the robotic group was $1000 USD more than the open cases irrespective of the complexity of the case.
The median follow-up duration was 24 months in the robotic group and 28 months in the open group. 4. Discussion We reported the first robotic left hepatectomy in 2015 and the first robotic right hepatectomy a year later.18e20 Since then, we had performed 21 robotic assisted liver resections. In this study, we have given an account of our experience of robotic-assisted liver resections and have compared it with a case-matched group of open cases without previous experience of laparoscopy for such procedures. The advantages of the robotic surgery are improved view via three-dimensional vision, visual magnification, tremor suppression, scaled surgeon movements as well as the flexibility and dexterity of the instruments which increases the precision in operative techniques. This allows the surgeons to perform the delicate and precise dissection especially in narrow and deeper areas and inaccessible areas with better depth perception, transection of liver in curve planes and precise intra-corporeal suturing. The indications of robotic liver resections are same as laparoscopic resections with the added advantage of better access to the lesion
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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Table 3 Comparison of histopathological parameters of all patients operated for malignancy between robotic and open resection groups. Parameters
Histology, n Hepatocellular carcinoma Well differentiated Moderately differentiated Poorly differentiated Intrahepatic cholangiocarcinoma Completion radical cholecystectomy post laparoscopic cholecystectomy Metastatic adenocarcinoma Mean tumor size, cm (Mean ± SD) Positive resection margins, n Recurrence, n Local Nonlocal
Robotic liver resections (n ¼ 13)
Open liver resections (n ¼ 26)
3 4 0 2 2
5 8 1 4 4
2 6.4 ± 3.6 0
4 6.8 ± 4.1 0
1 2
7 2
Fig. 2 Kaplan Meier Survival Curve of HCC patients operated by robotic and open approaches.
in a posterosuperior segment of the liver which is difficult to access in conventional laparoscopy.4,21 The available evidence in the literature suggests that robotic hepatectomy appears to be similar to conventional laparoscopic hepatectomy in terms of blood loss, morbidity, mortality rate and hospital stay but prolonged operative times and increased costs.4e6,10,22e24 Therefore, robotic surgery is usually considered as an alternative minimally invasive approach for liver resection. Robotic-assisted laparoscopic surgery overcomes the limitation of conventional laparoscopic instruments in performing liver surgery including depth perception, rigid instruments and difficulty of suturing and access to postero-superior segments of the liver. The major advantage of robotic hepatectomy may lie in sectoral, segmental, or subsegmental resections in difficult-to-reach positions like postero-superior segments and caudate lobe, where these patients may be spared of the large incisions and extensive mobilization required in an open approach for such incision dominant areas. Hepatic resections for hilar cholangiocarcinoma, caudate lobectomy and bile duct anastomosis,25,26 especially for small ducts is difficult via pure laparoscopic approach and generally not performed. Use of robotic surgical system may allow these to be approached in a minimally invasive manner with decreased tremor and fatigue for the surgeon. Therefore, lesions in the posterosuperior segments of the liver, as well as those with major vascular involvement could be more easily approached in robotic surgery as compared to conventional laparoscopy. Similarly, robotic approach may of greater value in facilitating a parenchymal-sparing liver resection as limited ability of laparoscopy approach in transection in transverse and curved planes leads to major liver resection, sacrificing a substantial volume of normal liver. In fact, some papers showed that parenchymal-sparing resection of the poster superior segments was performed more often by a robotic approach as compared to laparoscopic procedures.27,28 The less surgeon fatigue, especially in longer procedures, is an additional advantage of robotic liver surgery. Operative duration in our series was longer in the robotic group, with less blood loss and decreased the post-operative length of stay compared to the open group. Morbidity rates were similar in both groups but there was one mortality in open group. Meta-analyses by Croome KP et al. and Jackson NR et al. have shown that minimally invasive approaches afford shorter hospital stay, decreased blood loss and postoperative morbidity
Table 4 Comparison of postoperative outcomes of liver resection done by robotic and open approaches. Parameters
Robotic liver resections (n ¼ 21)
Open liver resections (n ¼ 42)
p
Minor post-operative complications, n (%) Clavien grade 1 Pleural effusion Persistent nausea and vomiting Clavien grade 2 Ileus Pleural effusion requiring oxygen supplement Major post-operative complications, n (%) Clavien grade 3a Bile leak requiring percutaneous drainage Non bilious collection requiring percutaneous drainage Clavien grade 3b Clavien grade 4 Clavien grade 5 Death due to PHLFa, n PHLFa, n Mean length of hospital stay, days (Mean ± SD) Median follow up, months Re-admission, n (%) Re-operation, n (%)
4 (19.0)
17 (40.4)
0.16
2 0
4 7
2 0 1 (4.8)
4 2 3 (7.1)
1 0 0 0 0 0 0 5.3 ± 0.8 24 0 0
1 1 0 0 1 1 2 7.7 ± 4.2 28 0 0
a
1.00
0.02
PHLP: Post hepatectomy liver failure.
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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with similar total operative times.6,16 Croome KP et al. had also demonstrated the value of laparoscopic liver resections for malignant tumors as well; no differences in the long-term survival and tumor recurrence for patients between open and laparoscopic procedures were observed.16 A recent paper by Chen et al. showed similar oncological outcomes after resection for HCC between the robotic and open group with decreased length of stay and pain requirement in the robotic group.29 In our experience, the robotic system can be safely used to perform major hepatectomies, with greater ease of hemostasis and biliary pedicle suturing which is difficult in laparoscopy needing a long learning curve. Access to superior segments, 7 and 8 which is a challenge in laparoscopy, is far easier using the robotic platform as shown in two of our cases in the present series. Studies have shown that the minimal number of laparoscopic minor and major hepatectomies to overcome learning curve are 22e64 cases, and 45e75 cases, respectively.30,31 However, the learning curve numbers for robotic liver resections are lacking at present. One of the major proposed advantages of robotic surgery is the possibility of shortened learning curve for complex liver resection based on the study of pancreatic resection studies,32 which is considered equally complex as compared to liver resection. The laparoscopy complex liver resections need both expertise in open complex hepatobiliary surgery as well as advanced laparoscopy. The same does not hold true for robotic liver surgery, one can easily translate expertise in open liver surgery to robot. In our study, there was no laparoscopic arm for comparison because the matched controlled arm couldn't be formed due to only non-anatomical and monosegmental resection performed laparoscopically by the authors. However, at the same time, the present study highlights the non-necessity of experience in laparoscopic complex liver resections before moving to robotic one. Robotic liver resections have shown promising results at our centre. It has proven useful for hepatectomies, both major and minor, because of better vision, less surgeon's fatigue, 360-degree wrist like movements of instruments, easy intra-corporeal suturing, achieving good hemostasis with the available devices and less blood loss (due to pneumoperitoneum). Thus, our experience highlights the utility of robotics for liver resections with better outcomes and decreased the length of hospital stay albeit with higher operative time. The study's limitations include its retrospective nature along with small sample size, but data accrual for more cases takes longer in complex liver resections, hence this is a pilot study. 5. Conclusion The authors present this comparative case series of roboticassisted hepatic resections for benign and malignant tumors, showcasing the feasibility, safety, and equivalence compared to open surgery with all advantages of minimally invasive surgery and shorter hospital stay. Also non necessity of previous laparoscopic experience is highlighted. Authors contributions Study concept and design: Sanjay Goja, Sanjay Kumar Yadav, Arvinder Singh Soin. Acquisition of data: Sanjay Kumar Yadav, Rohan Jagat Chaudhary, Manoj Kumar Singh. Analysis and interpretation: Sanjay Goja, Sanjay Kumar Yadav. Study supervision: Sanjay Goja, Sanjay Kumar Yadav, Arvinder Singh Soin.
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66 67 68 No funding received for this work. 69 70 Ethical approval 71 72 This study was approved by Institutional review board and 73 conducted in accordance with Declaration of Helsinki. 74 75 Conflict of interest 76 77 None. 78 79 80 References 81 1. Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic 82 liver surgery: the Louisville Statement, 2008. Ann Surg. 2009;250(5):825e830. 83 2. Nguyen KT, Marsh JW, Tsung A, Steel JJL, Gamblin TC, Geller DA. Comparative 84 benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg. 2011;146(3):348e356. 85 3. Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic 86 liver resection: a report from the second international consensus conference 87 held in Morioka. Ann Surg. 2015;261(4):619e629. 4. Giulianotti PC, Coratti A, Sbrana F, et al. Robotic liver surgery: results for 70 88 resections. Surgery. 2011;149(1):29e39. 89 5. Tsung A, Geller DA, Sukato DC, et al. Robotic versus laparoscopic hepatectomy: 90 a matched comparison. Ann Surg. 2014;259(3):549e555. 91 6. Jackson NR, Hauch A, Hu T, Buell JF, Slakey DP, Kandil E. The safety and efficacy of approaches to liver resection: a meta-analysis. JSLS. 2015;19(1):e2014, 92 00186. Q2 93 7. Idrees K, Bartlett DL. Robotic liver surgery. Surg Clin N Am. 2010;90(4): 94 761e774. 8. Leung U, Fong Y. Robotic liver surgery. Hepatobiliary Surg Nutr. 2014;3(5): 95 288e294. 96 9. Choi SB, Park JS, Kim JK, et al. Early experiences of robotic-assisted laparoscopic 97 liver resection. Yonsei Med J. 2008 30;49(4):632e638. 10. Berber E, Akyildiz HY, Aucejo F, Gunasekaran G, Chalikonda S, Fung J. Robotic 98 versus laparoscopic resection of liver tumours. HPB (Oxford). 2010;12(8): 99 583e586. 100 11. Choi GH, Choi SH, Kim SH, et al. Robotic liver resection: technique and results of 30 consecutive procedures. Surg Endosc. 2012;26(8):2247e2258. 101 12. Simillis C, Constantinides VA, Tekkis PP, et al. Laparoscopic versus open hepatic 102 resections for benign and malignant neoplasmsea meta-analysis. Surgery. 103 2007;141(2):203e211. 13. Buell JF, Thomas MT, Rudich S, et al. Experience with more than 500 minimally 104 invasive hepatic procedures. Ann Surg. 2008;248(3):475e486. 105 14. Bryant R, Laurent A, Tayar C, Cherqui D. Laparoscopic liver resection106 understanding its role in current practice: the Henri Mondor Hospital experience. Ann Surg. 2009;250(1):103e111. 107 15. Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver 108 resection-2,804 patients. Ann Surg. 2009;250(5):831e841. 109 16. Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign 110 and malignant tumors: an updated meta-analysis. Arch Surg. 2010;145(11): 1109e1118. 111 17. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a 112 new proposal with evaluation in a cohort of 6336 patients and results of a 113 survey. Ann Surg. 2004;240(2):205e213. 18. Goja S, Singh MK, Vohra V, Soin AS. Robotic left hepatectomy: a case report 114 (first reported case of robotic hepatectomy in India). Indian J Surg. 2015;77(4): 115 338e340. 116 19. Goja S, Singh MK, Soin AS. Robotics in hepatobiliary surgery-initial experience, first reported case series from India. Int J Surg Case Rep. 2017;33:16e20. 117 20. Goja S, Singh MK, Chaudhary RJ, Soin AS. Robotic-assisted right hepatectomy 118 via anterior approach for intrahepatic cholangiocarcinoma. Ann Hepato-Biliary119 Pancreatic Surg. 2017;21(2):80e83. 21. Giulianotti PC, Tzvetanov I, Jeon H, et al. Robot-assisted right lobe donor 120 hepatectomy. Transpl Int. 2012;25(1):e5ee9. 121 22. Lai ECH, Tang CN. Training robotic hepatectomy: the Hong Kong experience 122 and perspective. Hepatobiliary Surg Nutr. 2017;6(4):222e229. 123 23. Choi GH, Chong JU, Han DH, Choi JS, Lee WJ. Robotic hepatectomy: the Korean experience and perspective. Hepatobiliary Surg Nutr. 2017;6(4):230e238. 124 24. Nota CL, Rinkes IHB, Molenaar IQ, van Santvoort HC, Fong Y, Hagendoorn J. 125 Robot-assisted laparoscopic liver resection: a systematic review and pooled 126 analysis of minor and major hepatectomies. HPB (Oxford). 2016;18(2): 113e120. 127 25. Giulianotti PC, Sbrana F, Bianco FM, Addeo P. Robot-assisted laparoscopic 128 extended right hepatectomy with biliary reconstruction. J Laparoendosc Adv 129 Surg Tech. 2010;20(2):159e163. 130 Funding
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Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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Contents lists available at ScienceDirect
Laparoscopic, Endoscopic and Robotic Surgery journal homepage: www.keaipublishing.com/en/journals/ laparoscopic-endoscopic-and-robotic-surgery
Q5 Q4
Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed? Sanjay Goja a, b, *, Sanjay Kumar Yadav a, Rohan Jagat Chaudhary a, Manoj Kumar Singh a, Arvinder Singh Soin a a b
Institute of Liver Transplantation and Regenerative Medicine, Medanta-The Medicity, Gurugram, 122001, India Program Director and Clinical Lead-Liver Transplant Narayan Health City, Bengaluru, India
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 June 2019 Received in revised form 1 August 2019 Accepted 11 August 2019 Available online xxx
Objective: The authors present outcomes of robotic liver resections in comparison with open technique questioning the need to have experience of laparoscopy for such procedures before transition to robotic assisted. Materials and methods: Retrospective review of liver resections done robotically from February 2015 to June 2017 compared to matched control cohort of open cases from January 2012 to December 2016. Results: Twenty-one patients in the study group were compared with matched control of 42 open cases (1:2 ratio). The types of procedure were similar in both the groups. There were 4 left lateral hepatectomy, 3 left hepatectomy, and 1 left hepatectomy with hepatico-jejunostomy, 3 right hepatectomy, 3 right posterior sectorectomy, 4 bisegmentectomy and 4 mono-segmentectomy. There were 9 patients with primary liver cancer, 2 each with liver metastasis and carcinoma gall bladder and 8 patients had benign liver disease. Mean blood loss was 370 ± 311 ml in the robotic group compared to 451 ± 330 ml in control group (p ¼ 0.06). Minor complications developed in 19% of robotic cases compared to 40% in open surgery, while major complications occurred in 4.7% of robotic cases compared to 7.1% of open cases. Mean hospital stay was 5.3 ± 0.8 days for the robotic group and 7.7 ± 4.2 days for open group (p ¼ 0.02). Local tumor recurrence occurred in 1 out of 13 resections done for malignancy in the robotic group and 7 out of 26 in the open group. Conclusion: This study highlights the utility of surgical robots for segmental and complex liver resections with equivalent outcomes and decreased length of stay compared to open surgery without having experience of same with the laparoscopy. © 2019 Sir Run Run Shaw Hospital affiliated to Zhejiang University School of Medicine. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
Keywords: Robotic Liver resection Open surgery
1. Introduction Minimal invasive surgery is a well-accepted alternative approach for resection of anterior liver segments and left lateral secterectomies.1e3 The well established advantages of minimal invasive liver surgery are less estimated blood loss and postoperative pain, lower morbidity, shorter hospital stay, improved cosmesis and equivalent oncological outcomes compared to traditional open surgery.2,4e6 There is mounting evidence on the utility
Q1
* Corresponding author: Program Director and Clinical Lead-Liver Transplant Narayan Health City, Bengaluru, India. E-mail address: [email protected] (S. Goja).
of minimally invasive approaches for liver resection vis a vis laparoscopy and robotic platform with a recent tilt towards robotic surgery for complex and major hepatic resections.7,8 However, the inherent disadvantages of conventional laparoscopy have led to the evolution of robotic assisted liver surgery with an aim of overcoming the disadvantages of conventional laparoscopy. A spate of papers in the recent literature comparing robotic liver resections with laparoscopy have shown similar outcomes,4,5,9e11 preceded by papers comparing laparoscopic with open liver resections.2,12e16 The increasing popularity of robotic liver surgery is evident by the constantly growing number of reports in the literature. The authors present a comparative study of robotic cases compared with matched open liver resections in 1:2 ratio.
https://doi.org/10.1016/j.lers.2019.08.002 2468-9009/© 2019 Sir Run Run Shaw Hospital affiliated to Zhejiang University School of Medicine. Published by Elsevier B.V. This is an open access article under the CC BYNC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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rates of patients operated for hepatocellular carcinoma (HCC) were calculated using KaplaneMeier methods, and differences between the curves were calculated using log-rank test. For all statistical analysis, p 0.05 was considered as statistically significant. This study was approved by the institutional review board of the hospital, and data acquisition and database maintenance were complaint with institutional guidelines.
2. Materials and methods A retrospective review of liver resections done robotically using the da Vinci platform Si (Intuitive Surgical Inc., Milford, CT, USA) from February 2015 to June 2017 compared with matched control open cases in 1:2 ratio from January 2012 to December 2016. This is a retrospective comparative study from a tertiary care hospital (Medanta, the Medicity, Delhi-NCR, India), a high volume liver transplantation and hepatobiliary surgery centre, comparing operative variables, post-operative outcomes (morbidity and mortality) and the length of hospital stay and recurrence. Consecutive robotic liver resection cases were compared to matched open liver resection cases by review of the hospital-based database. Hospital records were retrospectively reviewed for patient history and demographics, liver pathology, intraoperative as well as postoperative outcomes. Matching criteria included: number of resected liver segments, histology, age group and body mass index (BMI). Postoperative complications up to 30 days were obtained from discharge summaries and followed up the database and graded according to Clavien-Dindo classification scale.17 The study cohort was consecutive robotic liver resection cases done during the study period. There is no laparoscopic arm for comparison in the group. The authors have performed only non-anatomical left lateral, exophytic and easily accessible segment 6 liver resections by laparoscopy. So the matched control group in the laparoscopic arm couldn't be formed thus.
3. Results There were 21 patients in the robotic group, 10 females and 11 males with mean age of 43.5 ± 19.4 years old; their characteristics in comparison to 42 matched open cases are listed in Table 1. The groups were matched with no difference in age, gender, BMI, American Society of Anesthesiologists classification and distribution of malignant and benign disease. The percentage of cirrhotic patients (Child's A) were similar in both groups with 2 in the robotic group and 4 in the open group. The robotic group patient had 1 patient with Hepatitis C Virus (HCV) and 1 with Hepatitis B Virus (HBV) cirrhosis and the open group had 2 with HCV and 2 with HBV cirrhosis. The types of procedures were similar in both the groups (Table 2). There were 4 left lateral hepatectomy, 3 left hepatectomy, and 1 left hepatectomy with hepatico-jejunostomy, 3 right hepatectomy, 3 right posterior sectorectomy, 4 bisegmentectomy and 4 mono-segmentectomy. The intraoperative image of various steps of robotic liver resection are shown in Fig. 1(AeF). There were 9 patients with primary liver cancer, 2 each with liver metastasis and carcinoma gall bladder and 8 patients had benign liver disease. The mean operative duration was 442 ± 135 minutes in the robotic group compared to 357 ± 127 minutes in the open group (p ¼ 0.03); the mean operative blood loss was 370 ± 311 ml in the robotic group and 451 ± 330 ml in the open group (p ¼ 0.06). Four patients required intra-operative blood transfusion and there were no reexplorations in either group. There was no conversion to open in the present robotic study group.
2.1. Statistical analysis Study data were analyzed using SPSS (version 20.0; SPSS Inc, Chicago, IL). Groups were compared using Fisher's exact test for categorical variables, student t test for continuous parametric variables. Categorical variables are presented as whole numbers and percentages. Continuous parametric variables are presented as means ± SD. Continuous nonparametric variables are presented as medians with interquartile range. The cumulative overall survival
Table 1 Comparison of clinical profile of study population in robotic and open liver resection groups. Parameters
Robotic liver resections (n ¼ 21)
Open liver resections (n ¼ 42)
p
Age, years (Mean ± SD) Gender, n (%) Male Female BMI, kg/m2 (Mean ± SD) ASAa classification, n (%) 1 2 3 4 Pathology, n (%) Primary liver cancer Hepatocellular carcinoma Intrahepatic cholangiocarcinoma Liver metastasis Carcinoma stomach metastasis Colorectal liver metastasis Incidental carcinoma gall bladder post laparoscopic cholecystectomy Benign tumor Hemangioma Polycystic liver disease Recurrent primary Cholangitis Adenoma Cirrhosis, n (%) Child A None
43.5 ± 19.4
47.6 ± 16.3
0.43
11 (52.3) 10 (47.6) 24.12 ± 3.7
23 (54.8) 19 (45.2) 24.6 ± 2.8
1.00
4 (19.0) 14 (66.7) 3 (14.3) 0
8 (19.0) 21 (50.0) 12 (28.6) 1 (2.4)
9 7 2 2 1 1 2 8 4 2
18 (42.9) 14 4 4 (9.5) 0 4 4 (9.5) 16 (38.1) 8 4
a
(42.9)
(9.5)
(9.5) (38.1)
1 1
2 2
2 (9.5) 19 (90.5)
4 (9.5) 38 (90.5)
0.63 0.26
1.00
1.00
1.00 1.00
0.53
ASA: American Association of Anesthesiologist.
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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Table 2 Details of liver resection done by robotic and open approaches. Parameters Type of surgical procedures, n (%) Left lateral hepatectomy Left hemihepatectomy Right hemihepatectomy Bi- segmentectomy Segment 4b þ 5 Segment 5 þ 6 Right posterior secterectomy (segment 6 þ 7) Monosegmentectomy Additional procedure, n Hepatico-jejunostomy Blood loss, ml (Mean ± SD) Operative time, minutes (Mean ± SD) Blood transfusion (number of units) (Mean ± SD)
Robotic liver resections (n ¼ 21)
Open liver resections (n ¼ 42)
4 (19.0) 3 (14.3) 3 (14.3)
8 (19.0) 6 (14.3) 6 (14.3)
2 2 3 4
4 4 6 8
p 0.99
(9.5) (9.5) (14.3) (19.0)
1 370 ± 311 442 ± 135 0.67 ± 1.23
(9.5) (9.5) (14.3) (19.0)
0 451 ± 330 357 ± 127 0.79 ± 1.06
0.06 0.03 0.71
Fig. 1 The intraoperative image of various steps of robotic liver resection.
The histopathological characteristics of all patients operated for malignancy were shown in Table 3. The median tumor size in the robotic group was 6.4 ± 3.6 cm compared to 6.8 ± 4.1 cm in the open group (p ¼ 0.7), with negative resection margins in all 13 of the patients with tumor in the robotic arm and all 26 tumor patients in the open arm. Local tumor recurrence occurred in one out of 13 resections done for malignancy in the robotic group and 7 out of 26 in the open group; nonlocal recurrence occurred in 2 of 13 in the robotic group and 2 of 26 in the open group (Table 3). No significant difference in overall survival was observed among HCC patients (7 in robotic arm and 14 in open arm) operated using either robotic or open approach (log rank p ¼ 0.65). See Fig. 2. The morbidity in both the groups was compared based on Clavien-Dindo scale and described in Table 4. There were 19% minor complications (Clavien grade 1e2) in the robotic group and 40% in the open group. Major complications (Clavien grade 3 and higher) were 4.7% in the robotic group compared to 7.1% in the open group. The mean hospital length of stay was 5.3 ± 0.8 days in the robotic group, compared to 7.7 ± 4.2 days in the open group (p ¼ 0.02). The mean operative cost in the robotic group was $1000 USD more than the open cases irrespective of the complexity of the case.
The median follow-up duration was 24 months in the robotic group and 28 months in the open group. 4. Discussion We reported the first robotic left hepatectomy in 2015 and the first robotic right hepatectomy a year later.18e20 Since then, we had performed 21 robotic assisted liver resections. In this study, we have given an account of our experience of robotic-assisted liver resections and have compared it with a case-matched group of open cases without previous experience of laparoscopy for such procedures. The advantages of the robotic surgery are improved view via three-dimensional vision, visual magnification, tremor suppression, scaled surgeon movements as well as the flexibility and dexterity of the instruments which increases the precision in operative techniques. This allows the surgeons to perform the delicate and precise dissection especially in narrow and deeper areas and inaccessible areas with better depth perception, transection of liver in curve planes and precise intra-corporeal suturing. The indications of robotic liver resections are same as laparoscopic resections with the added advantage of better access to the lesion
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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Table 3 Comparison of histopathological parameters of all patients operated for malignancy between robotic and open resection groups. Parameters
Histology, n Hepatocellular carcinoma Well differentiated Moderately differentiated Poorly differentiated Intrahepatic cholangiocarcinoma Completion radical cholecystectomy post laparoscopic cholecystectomy Metastatic adenocarcinoma Mean tumor size, cm (Mean ± SD) Positive resection margins, n Recurrence, n Local Nonlocal
Robotic liver resections (n ¼ 13)
Open liver resections (n ¼ 26)
3 4 0 2 2
5 8 1 4 4
2 6.4 ± 3.6 0
4 6.8 ± 4.1 0
1 2
7 2
Fig. 2 Kaplan Meier Survival Curve of HCC patients operated by robotic and open approaches.
in a posterosuperior segment of the liver which is difficult to access in conventional laparoscopy.4,21 The available evidence in the literature suggests that robotic hepatectomy appears to be similar to conventional laparoscopic hepatectomy in terms of blood loss, morbidity, mortality rate and hospital stay but prolonged operative times and increased costs.4e6,10,22e24 Therefore, robotic surgery is usually considered as an alternative minimally invasive approach for liver resection. Robotic-assisted laparoscopic surgery overcomes the limitation of conventional laparoscopic instruments in performing liver surgery including depth perception, rigid instruments and difficulty of suturing and access to postero-superior segments of the liver. The major advantage of robotic hepatectomy may lie in sectoral, segmental, or subsegmental resections in difficult-to-reach positions like postero-superior segments and caudate lobe, where these patients may be spared of the large incisions and extensive mobilization required in an open approach for such incision dominant areas. Hepatic resections for hilar cholangiocarcinoma, caudate lobectomy and bile duct anastomosis,25,26 especially for small ducts is difficult via pure laparoscopic approach and generally not performed. Use of robotic surgical system may allow these to be approached in a minimally invasive manner with decreased tremor and fatigue for the surgeon. Therefore, lesions in the posterosuperior segments of the liver, as well as those with major vascular involvement could be more easily approached in robotic surgery as compared to conventional laparoscopy. Similarly, robotic approach may of greater value in facilitating a parenchymal-sparing liver resection as limited ability of laparoscopy approach in transection in transverse and curved planes leads to major liver resection, sacrificing a substantial volume of normal liver. In fact, some papers showed that parenchymal-sparing resection of the poster superior segments was performed more often by a robotic approach as compared to laparoscopic procedures.27,28 The less surgeon fatigue, especially in longer procedures, is an additional advantage of robotic liver surgery. Operative duration in our series was longer in the robotic group, with less blood loss and decreased the post-operative length of stay compared to the open group. Morbidity rates were similar in both groups but there was one mortality in open group. Meta-analyses by Croome KP et al. and Jackson NR et al. have shown that minimally invasive approaches afford shorter hospital stay, decreased blood loss and postoperative morbidity
Table 4 Comparison of postoperative outcomes of liver resection done by robotic and open approaches. Parameters
Robotic liver resections (n ¼ 21)
Open liver resections (n ¼ 42)
p
Minor post-operative complications, n (%) Clavien grade 1 Pleural effusion Persistent nausea and vomiting Clavien grade 2 Ileus Pleural effusion requiring oxygen supplement Major post-operative complications, n (%) Clavien grade 3a Bile leak requiring percutaneous drainage Non bilious collection requiring percutaneous drainage Clavien grade 3b Clavien grade 4 Clavien grade 5 Death due to PHLFa, n PHLFa, n Mean length of hospital stay, days (Mean ± SD) Median follow up, months Re-admission, n (%) Re-operation, n (%)
4 (19.0)
17 (40.4)
0.16
2 0
4 7
2 0 1 (4.8)
4 2 3 (7.1)
1 0 0 0 0 0 0 5.3 ± 0.8 24 0 0
1 1 0 0 1 1 2 7.7 ± 4.2 28 0 0
a
1.00
0.02
PHLP: Post hepatectomy liver failure.
Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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with similar total operative times.6,16 Croome KP et al. had also demonstrated the value of laparoscopic liver resections for malignant tumors as well; no differences in the long-term survival and tumor recurrence for patients between open and laparoscopic procedures were observed.16 A recent paper by Chen et al. showed similar oncological outcomes after resection for HCC between the robotic and open group with decreased length of stay and pain requirement in the robotic group.29 In our experience, the robotic system can be safely used to perform major hepatectomies, with greater ease of hemostasis and biliary pedicle suturing which is difficult in laparoscopy needing a long learning curve. Access to superior segments, 7 and 8 which is a challenge in laparoscopy, is far easier using the robotic platform as shown in two of our cases in the present series. Studies have shown that the minimal number of laparoscopic minor and major hepatectomies to overcome learning curve are 22e64 cases, and 45e75 cases, respectively.30,31 However, the learning curve numbers for robotic liver resections are lacking at present. One of the major proposed advantages of robotic surgery is the possibility of shortened learning curve for complex liver resection based on the study of pancreatic resection studies,32 which is considered equally complex as compared to liver resection. The laparoscopy complex liver resections need both expertise in open complex hepatobiliary surgery as well as advanced laparoscopy. The same does not hold true for robotic liver surgery, one can easily translate expertise in open liver surgery to robot. In our study, there was no laparoscopic arm for comparison because the matched controlled arm couldn't be formed due to only non-anatomical and monosegmental resection performed laparoscopically by the authors. However, at the same time, the present study highlights the non-necessity of experience in laparoscopic complex liver resections before moving to robotic one. Robotic liver resections have shown promising results at our centre. It has proven useful for hepatectomies, both major and minor, because of better vision, less surgeon's fatigue, 360-degree wrist like movements of instruments, easy intra-corporeal suturing, achieving good hemostasis with the available devices and less blood loss (due to pneumoperitoneum). Thus, our experience highlights the utility of robotics for liver resections with better outcomes and decreased the length of hospital stay albeit with higher operative time. The study's limitations include its retrospective nature along with small sample size, but data accrual for more cases takes longer in complex liver resections, hence this is a pilot study. 5. Conclusion The authors present this comparative case series of roboticassisted hepatic resections for benign and malignant tumors, showcasing the feasibility, safety, and equivalence compared to open surgery with all advantages of minimally invasive surgery and shorter hospital stay. Also non necessity of previous laparoscopic experience is highlighted. Authors contributions Study concept and design: Sanjay Goja, Sanjay Kumar Yadav, Arvinder Singh Soin. Acquisition of data: Sanjay Kumar Yadav, Rohan Jagat Chaudhary, Manoj Kumar Singh. Analysis and interpretation: Sanjay Goja, Sanjay Kumar Yadav. Study supervision: Sanjay Goja, Sanjay Kumar Yadav, Arvinder Singh Soin.
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66 67 68 No funding received for this work. 69 70 Ethical approval 71 72 This study was approved by Institutional review board and 73 conducted in accordance with Declaration of Helsinki. 74 75 Conflict of interest 76 77 None. 78 79 80 References 81 1. Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic 82 liver surgery: the Louisville Statement, 2008. Ann Surg. 2009;250(5):825e830. 83 2. Nguyen KT, Marsh JW, Tsung A, Steel JJL, Gamblin TC, Geller DA. Comparative 84 benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg. 2011;146(3):348e356. 85 3. Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic 86 liver resection: a report from the second international consensus conference 87 held in Morioka. Ann Surg. 2015;261(4):619e629. 4. Giulianotti PC, Coratti A, Sbrana F, et al. Robotic liver surgery: results for 70 88 resections. Surgery. 2011;149(1):29e39. 89 5. Tsung A, Geller DA, Sukato DC, et al. Robotic versus laparoscopic hepatectomy: 90 a matched comparison. Ann Surg. 2014;259(3):549e555. 91 6. Jackson NR, Hauch A, Hu T, Buell JF, Slakey DP, Kandil E. The safety and efficacy of approaches to liver resection: a meta-analysis. JSLS. 2015;19(1):e2014, 92 00186. Q2 93 7. Idrees K, Bartlett DL. Robotic liver surgery. Surg Clin N Am. 2010;90(4): 94 761e774. 8. Leung U, Fong Y. Robotic liver surgery. Hepatobiliary Surg Nutr. 2014;3(5): 95 288e294. 96 9. Choi SB, Park JS, Kim JK, et al. Early experiences of robotic-assisted laparoscopic 97 liver resection. Yonsei Med J. 2008 30;49(4):632e638. 10. Berber E, Akyildiz HY, Aucejo F, Gunasekaran G, Chalikonda S, Fung J. Robotic 98 versus laparoscopic resection of liver tumours. HPB (Oxford). 2010;12(8): 99 583e586. 100 11. Choi GH, Choi SH, Kim SH, et al. Robotic liver resection: technique and results of 30 consecutive procedures. Surg Endosc. 2012;26(8):2247e2258. 101 12. Simillis C, Constantinides VA, Tekkis PP, et al. Laparoscopic versus open hepatic 102 resections for benign and malignant neoplasmsea meta-analysis. Surgery. 103 2007;141(2):203e211. 13. Buell JF, Thomas MT, Rudich S, et al. Experience with more than 500 minimally 104 invasive hepatic procedures. Ann Surg. 2008;248(3):475e486. 105 14. Bryant R, Laurent A, Tayar C, Cherqui D. Laparoscopic liver resection106 understanding its role in current practice: the Henri Mondor Hospital experience. Ann Surg. 2009;250(1):103e111. 107 15. Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver 108 resection-2,804 patients. Ann Surg. 2009;250(5):831e841. 109 16. Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign 110 and malignant tumors: an updated meta-analysis. Arch Surg. 2010;145(11): 1109e1118. 111 17. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a 112 new proposal with evaluation in a cohort of 6336 patients and results of a 113 survey. Ann Surg. 2004;240(2):205e213. 18. Goja S, Singh MK, Vohra V, Soin AS. Robotic left hepatectomy: a case report 114 (first reported case of robotic hepatectomy in India). Indian J Surg. 2015;77(4): 115 338e340. 116 19. Goja S, Singh MK, Soin AS. Robotics in hepatobiliary surgery-initial experience, first reported case series from India. Int J Surg Case Rep. 2017;33:16e20. 117 20. Goja S, Singh MK, Chaudhary RJ, Soin AS. Robotic-assisted right hepatectomy 118 via anterior approach for intrahepatic cholangiocarcinoma. Ann Hepato-Biliary119 Pancreatic Surg. 2017;21(2):80e83. 21. Giulianotti PC, Tzvetanov I, Jeon H, et al. Robot-assisted right lobe donor 120 hepatectomy. Transpl Int. 2012;25(1):e5ee9. 121 22. Lai ECH, Tang CN. Training robotic hepatectomy: the Hong Kong experience 122 and perspective. Hepatobiliary Surg Nutr. 2017;6(4):222e229. 123 23. Choi GH, Chong JU, Han DH, Choi JS, Lee WJ. Robotic hepatectomy: the Korean experience and perspective. Hepatobiliary Surg Nutr. 2017;6(4):230e238. 124 24. Nota CL, Rinkes IHB, Molenaar IQ, van Santvoort HC, Fong Y, Hagendoorn J. 125 Robot-assisted laparoscopic liver resection: a systematic review and pooled 126 analysis of minor and major hepatectomies. HPB (Oxford). 2016;18(2): 113e120. 127 25. Giulianotti PC, Sbrana F, Bianco FM, Addeo P. Robot-assisted laparoscopic 128 extended right hepatectomy with biliary reconstruction. J Laparoendosc Adv 129 Surg Tech. 2010;20(2):159e163. 130 Funding
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Please cite this article as: Goja S et al., Transition from open to robotic assisted liver resection: A retrospective comparative study. Is experience of laparoscopic liver resections needed?, Laparoscopic, Endoscopic and Robotic Surgery, https://doi.org/10.1016/j.lers.2019.08.002
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