Abstract
Background
Robotic surgery has been introduced to overcome the limitations of conventional laparoscopy. A systematic review and meta-analysis were performed to assess the safety and feasibility for three subgroups of robot-assisted laparoscopic liver resection: (i) minor resections of easily accessible segments: 2/3, 4B, 5, 6, (ii) minor resections of difficult located segments: 1, 4A, 7, 8 and (iii) major resections: ≥ 4 segments.
Methods
A systematic search was performed in PubMed, EMBASE and Cochrane Library.
Results
Twelve observational, mostly retrospective studies reporting on 363 patients were included. Data were pooled and analyzed. For subgroup (i) (n = 81) the weighted mean operative time was 215 ± 65 min. One conversion (1%) to laparotomy was needed. Weighted mean operative time for subgroup (ii) (n = 17) was 220 ± 60 min. No conversions were needed. For subgroup (iii) (n = 99) the weighted mean operative time was 405 ± 100 min. In this subgroup 8 robotic procedures (8%) were converted to open surgery.
Conclusion
Data show that robot-assisted laparoscopic liver resection is feasible in minor resections of all segments and major resections. Larger, prospective studies are warranted to compare the possible advantages of robot-assisted surgery with conventional laparoscopy and open surgery.
Introduction
Liver resection was once considered a complex procedure, with high morbidity and mortality. Nowadays, liver resection is regarded a routine procedure1. Traditionally, liver resections are performed using laparotomy, but in the early 1990s minimally invasive techniques emerged. The first laparoscopic non-anatomic liver resection was performed in 1992 and the first anatomic liver resection in 19962, 3. Since then, several non-randomized studies have shown that laparoscopic liver resection is safe and feasible in selected patients4, 5. Compared to open surgery, laparoscopic liver resection has been associated with less blood loss, shorter hospital stay and similar oncologic outcomes6, 7, 8, 9, 10, 11. Laparoscopic liver resection was initially performed in patients with benign or peripherally located lesions. But, as time progressed, laparoscopic major hepatectomies and resections of the postero-superior segments were also reported12, 13, 14, 15.
However, laparoscopy has its disadvantages, most notably the limited mobility of the straight laparoscopic instruments. The robotic system provides a 3-dimensional, magnified view of the operative field. This, in combination with the computer-to-human interface and wristed instruments, results in improved precision in surgical dissection. In theory, the improved dexterity makes robotic systems particularly suited for those resections that require non-linear manipulation, such as the curved parenchymal transection, hilar dissection and resection of the posterosuperior segments in liver surgery. Furthermore, the use of a robotic surgical system leads to decreased fatigue and tremor with the surgeon1, 16, 17.
Recently, a number of case-series reporting on robotic liver resection have been published. It remains unclear from each of these series whether, in larger groups of patients, use of the robot is feasible and if the use of a robotic system is especially advantageous in a specific subgroup of liver resection. Hence, the aim of this review is twofold: First, to assess the feasibility and safety in terms of morbidity and mortality for all types of resections together; second, to perform a pooled analysis for three subgroups (minor resections of easily accessible segments, minor resections of difficult located segments, and major resections).
Materials and methods
Study selection
A systematic search, restricted to papers published in English, up to 25-04-2015, was performed in PubMed, EMBASE and Cochrane Library. The study was conducted according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines18.
Search terms were: ‘(robot OR robotic OR da Vinci) AND (liver OR hepatic OR hepatectomy OR liver resection OR hepatic resection)’. Titles and abstracts of the identified papers were screened. Two authors (CN and JH) examined full-text versions of papers considered for inclusion. The bibliographies of the selected articles were reviewed for other potentially relevant studies.
Eligibility criteria
Included were all clinical studies reporting on robotic liver resection, with full-text available in English. Studies focusing on biliary surgery, studies from which data were unavailable or insufficient, review articles and conference abstracts published in abstract form only, were excluded. Studies with sample size of fewer than five patients were also excluded. Disagreement on eligibility was addressed by discussion and consensus. Data were carefully examined to avoid double counting of patients and if multiple studies were published by one center, the study reporting the largest number of patients was selected for inclusion, unless it was clear data did not overlap.
Methodological quality
Two authors (CN and JH) assessed methodological quality of the included studies independently. Since all of the included studies were cohort studies, grading was performed using the Newcastle–Ottawa quality assessment scale (NOS)19.
Data extraction
Data extracted from the selected studies included country, study design, study interval, relevant patients, total number of patients in the study, type of resection and whether comparisons were made between robotic, laparoscopic and open surgery. Patient demographics extracted from the selected studies included: sex, age, ASA-score, previous abdominal surgery, number of lesions, tumor size and histopathology of the resected specimen. BMI is not presented in the tables, since only four of the included studies provided data on this and presentation was very heterogeneous. Documented data on (outcomes of) surgery included: operating time, blood loss, conversion rate, transection method, number of positive surgical margins, complication rate, length of hospital stay and mortality. Pooled data were analyzed for three different subgroups of resections: (i) minor resections of easily accessible segments: 2/3, 4B, 5, 6. (ii) Minor resections of difficult to reach segments: 1, 4A, 7, 8. (iii) Major resections: ≥ 4 segments20, 21. If studies did not report outcomes separately for the different segments or resection types, authors were contacted to provide the additional data.
Statistical analyses
If studies documented the outcomes as medians and ranges, means and SD's were estimated according to the methods described by Hozo et al22. Weighted means and weighted SD's were calculated for all types of resection together and for the three separate subgroups of robot-assisted laparoscopic liver resection. Data regarding age, blood loss, operation time and tumor size are rounded in all tables. Data regarding length of stay are rounded to whole days.
Results
The search yielded a total of 799 studies. A total of 12 studies, one prospective23 and eleven retrospective24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, including 363 relevant patients, met the inclusion criteria to be included in this systematic review. (Fig. 1)23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45 Study characteristics are summarized in Table 1. Four studies solely reported robotic patients. Six studies compared outcomes for robot-assisted laparoscopic liver resection with conventional laparoscopic surgery. Two studies compared robot-assisted laparoscopic liver resection with conventional laparoscopic and open surgery.
Figure 1.
Flow diagram of the included studies
Table 1.
Study characteristics
| Authors | Country | Study interval | Relevant patients/patients in study | Robotic procedure sorted per subgroup 1,2,3 (n=) |
|---|---|---|---|---|
| Giulianotti et al. | USA & Italy | March 2002–March 2009 | 70/70 | 1/2 (43) |
| 3 (27) | ||||
| Tsung et al. | USA | November 2007–December 2011 | 57/171 | 1 (31) |
| 2 (5) | ||||
| 3 (21) | ||||
| Wu et al. | Taiwan | 2012 | 38/121 | 1/2 (39) |
| 3 (13) | ||||
| Lai et al. | China | May 2009–March 2012 | 41/41 | 1/2 (33) |
| 3 (10) | ||||
| Troisi et al. | Italy & Belgium | March 2008–March 2012 | 40/263 | 1/2 (40) |
| 3 (0) | ||||
| Choi et al. | Korea | November 2008–April 2011 | 30/30 | 1 (8) |
| 2 (2) | ||||
| 3 (20) | ||||
| Spampinato et al. | Italy | January 2009–December 2012 | 25/50 | 1 (0) |
| 2 (0) | ||||
| 3 (25) | ||||
| Felli et al. | Italy | April 2013–May 2014 | 20/20 | 1 (12) |
| 2 (6) | ||||
| 3 (2) | ||||
| Ji et al. | China | April 2009–July 2009 | 13/65 | 1 (4) |
| 2 (0) | ||||
| 3 (9) | ||||
| Yu et al. | Korea | July 2007–October 2011 | 13/30 | 1 (10) |
| 2 (0) | ||||
| 3 (3) | ||||
| Berber et al. | USA | October 2008–September 2009 | 9/32 | 1/2 (9) |
| 3 (0) | ||||
| Kandil et al. | USA | February 2011–August 2011 | 7/7 | 1 (5) |
| 2 (1) | ||||
| 3 (1) |
Methodological quality
For all the included studies, details of the methodological quality are summarized in Table 2. Overall, the methodological quality of the included studies was adequate. However, almost all of the cohort studies included selected populations (e.g. excluding patients with vascular involvement, liver cirrhosis or tumor size >5 cm), which were not entirely representative for the general patient population undergoing liver resection. Most of the included studies were retrospective24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34. However, data from five studies were extracted from prospectively maintained databases24, 27, 28, 29, 30.
Table 2.
Assessment methodological quality for cohort studies
| Selection |
Comparability |
Outcome |
||||||
|---|---|---|---|---|---|---|---|---|
| Authors | Representativeness | Selection of controls | Ascertainment | Outcome of interest not present at start study | Comparability of cohorts | Assessment of outcome | Length follow-up | Adequacy of follow up |
| Giulianotti et al. (70) |  |
– | ■ | – | – | ■ | |
■ |
| Tsung et al. (57) | ■ | ■ | ■ | – | ■ | ■ | ■ | ■ |
| Wu et al. (38) | |
■ | ■ | – | |
■ | ■ | ■ |
| Lai et al. (41) | |
■ | ■ | – | |
■ | ■ | ■ |
| Troisi et al. (40) | |
☐ | ■ | – | |
■ | ■ | ■ |
| Choi et al. (30) | |
– | ■ | – | – | ■ | ■ | ■ |
| Spampinato et al. (25) | |
☐ | ■ | – | |
■ | ■ | ■ |
| Felli et al. (20) | |
– | ■ | – | – | ■ | ■ | ■ |
| Ji et al. (13) | |
■ | ■ | – | ■ | ■ | |
■ |
| Yu et al. (13) | ☐ | ■ | ■ | – | |
■ | |
■ |
| Berber et al. (9) | |
■ | ■ | – | |
■ | ■ | ■ |
| Kandil et al. (7) | |
– | ■ | – | – | ■ | |
■ |
■Consistent with criteria, low risk of bias.
Partially consistent with criteria, unknown risk of bias.
☐ Not consistent with criteria, high risk of bias.
–, Not applicable.
Outcomes for all types of resection and pooled analysis
Patient characteristics and surgical outcomes of all resections are provided in Table 3 and Table 4. Pooled data per type of resection subgroup are summarized in Table 5. Outcomes by individual subgroup type are provided as supplementary material. (Tables S1–S3).
Table 3.
Patient characteristics
| Authors | Male gender n = (%) | Age (years) | ASA-score I, II, III, IV (n = ) | Previous abdominal surgery n = (%) | Number of patients with cirrhosis n = (%) | No. of lesions n= | Tumor size in mm | Pathology n = (%) |
|---|---|---|---|---|---|---|---|---|
| Giulianotti et al. (70) | 30 (43) | 60 (20–85)c | I (13) | 34 (49) | 8 (11) | 1 (0–6)b | 50 (10–110)e | Malignant 42 (60) |
| II (29) | Benign 28 (40) | |||||||
| III (28) | ||||||||
| Tsung et al. (57) | 24 (42) | 60 ± 15a | I (0) | NR | 3 (5) | 1 (1–2)b | 30 (20–50)f | Malignant 28 (49) |
| II (8) | Benign 19 (33) | |||||||
| III (42) | Other 10 (18) | |||||||
| IV (7) | ||||||||
| Wu et al. (38) | 32 | 60 ± 15a | NR | NR | NR | NR | 35 ± 15a | Malignant 38 |
| Lai et al. (41) | 31 | 60 ± 10a | NR | NR | 34 | NR | 35 ± 20a | Malignant 42 |
| Troisi et al. (40) | 27 | 65 ± 10a | NR | 13 | NR | NR | NR | Malignant 28 |
| Benign 10 | ||||||||
| Other 2 | ||||||||
| Choi et al. (30) | 14 | 50 (30–70)c | NR | NR | 5 | Single (n = 20) Multiple (n = 3) | (HCC only) 30 (10–50)c | Malignant 21 |
| Benign 9 | ||||||||
| Spampinato et al. (25) | 13 | 65 (30–80)b | I (2) | 16 | NR | NR | NR | Malignant 17 |
| II (20) | Benign 8 | |||||||
| III (3) | Other 4 | |||||||
| Felli et al. (20) | 8 | 65 (50–80)c | I (5) | 11 | 6 | 1 (n = 20) | 35 (10–120)c | Malignant 17 |
| II (9) | Benign 3 | |||||||
| III (6) | ||||||||
| Ji et al. (13) | 9 | 55 (40–80)c | NR | 2 | 4 | NR | 65 (20–120)c | Malignant 8 |
| Benign 5 | ||||||||
| Yu et al. (13) | 7 | 50 ± 10a | NR | NR | 4 | NR | 30 ± 15a | Malignant 10 |
| Benign 3 | ||||||||
| Berber et al. (9) | 7 | 65 ± 5d | NR | NR | NR | NR | 30 ± 15d | Malignant 7 |
| Other 2 | ||||||||
| Kandil et al. (7) | 5 | 45 (20–70)c | NR | NR | NR | NR | 40 ± 35a | Malignant 4 |
| Benign 3 |
Reported as mean ± SD.
Reported as median (range).
Reported as mean (range).
Reported as mean ± SEM.
Reported as weighted mean (range).
Reported as median (IQR).
Table 4.
Surgical outcomes all studies
| Authors | Operating time (min) | Blood loss (mL) | Conversion rate n (%) | LoS (days) | Positive surgical margins | Transection method | Patients with ≥1 complication n (%) | Mortality |
|---|---|---|---|---|---|---|---|---|
| Giulianotti et al. (70) | 270 (90–660)b | 260 (20–2000)b | 4 (6) | 7 (2–26)b | 0/42 | Harmonic device and bipolar forceps | 15 (21) | 0 |
| Tsung et al. (57) | 255 (62–597)b | 200 (30–3600)b | 4 (7) | 4 (1–31)b | 2/42 | NR | 11(19) | 0 |
| Wu et al. (38) | 380 ± 165a | 325 ± 480a | 2 | 8 ± 5a | NR | NR | 3 | 0 |
| Lai et al. (41) | 230 ± 85a | 415 (10–3500)b | 2 | 6 ± 4a | 3/42 | NR | 3 | 0 |
| Troisi et al. (40) | 270 ± 100a | 330 ± 300a | 8 | 6 ± 3a | 3/28 | Straight-line: Harmonic scalpel Curved and angulated section lines: Kelly Clamp crushing technique using endowristed bipolar Precise Forceps | 5 | 0 |
| Choi et al. (30) | 510 (120–815)c | 345 (95–1500)c | 2 | 12 (5–46)b | 0/13 | Harmonic curved shears and Maryland bipolar forceps | 13 | 0 |
| Spampinato et al. (25) | 430 (240–725)b | 250 (100–1900)b | 1 | 8 (4–22)b | 0/17 | NR | 4 | 0 |
| Felli et al. (20) | 140 (100–200)c | 50 (0–200)c | 0 | 6 (4–14)b | 2/17 | Combination of Kelly crushing technique, bipolar forceps, monopolar crochet andharmonic scalpel | 2 | 0 |
| Ji et al. (13) | 340 (150–720)c | 280e | 0 | 7e | 0/8 | Harmonic curved shears and bipolar electrocautery | 1 | NR |
| Yu et al. (13) | 290 ± 85a | 390 ± 65a | 0 | 8±2a | 0/12 | Harmonic scalpel | 0 | 0 |
| Berber et al. (9) | 260 ± 30d | 135 ± 60d | 1 | NR | 0/9 | Harmonic scalpel, clips, scissors or stapler | 1 | NR |
| Kandil et al. (7) | 60 ± 30a | 100 (10–200)c | 0 | 2 (1–5)b | NR | Harmonic scalpel | 2 | 0 |
Reported as mean ± SD.
Reported as median (range).
Reported as mean (range).
Reported as mean ± SEM.
Reported as mean.
Table 5.
Pooled surgical outcomes
| Group | Patients | Operating time (min) | Blood loss (mL) | Conversion rate n (%) | LoS (days) | Positive surgical margin n (%) | Patients with ≥1 complication n (%) | Mortality |
|---|---|---|---|---|---|---|---|---|
| All types of resection | 363 | 300 ± 130 | 300 ± 575 | 24 (7) | 7 ± 6 | 10 (4) | 60 (17) | 0 |
| Minor resections 2/3, 4B, 5, 6 | 81 | 215 ± 65 | 230 ± 310 | 1 (1) | 5 ± 2 | 2 | 15 (19) | 0 |
| Minor resections 1, 4A, 7, 8 | 17 | 220 ± 60 | 170 ± 120 | 0 | 5 ± 1 | 2 | 4 | 0 |
| Resections of 4 or more segments | 99 | 405 ± 100 | 380 ± 505 | 8 (8) | 11 ± 6 | 0 | 26 (26) | 0 |
Discussion
Here, the largest review on robot-assisted laparoscopic liver resections to date as well as the first pooled analysis for subgroups of liver resection are provided. Collectively, the data show that the robotic platform is safe and suitable in all subgroups of liver resection in terms of operative time, blood loss, and number of conversions. Evidently, the fact that all published series so far selected patients must be taken into account. Larger, prospective series are therefore needed to confirm the suitability of robot-assisted laparoscopic surgery.
It remains to be determined if the robotic platform provides definitive advantages over standard laparoscopy in liver surgery. The data show significantly longer operating times for robot-assisted liver resection over conventional laparoscopic liver resection. However, this finding is biased by the fact that the learning curve of robot-assisted laparoscopic liver resection had not been completed, as most series included here represent initial experience. As was shown by Tsung et al., operating time, as well as blood loss and length of stay, significantly decrease as experience grows31. Moreover, it will be interesting to learn if robot-assisted laparoscopic liver resection has steeper learning curves than conventional laparoscopy, as was shown previously in complex minimally invasive abdominal surgery such as pancreatic resection46. The data show that conversion rates are low in any subgroup (1%, 0%, and 8% respectively in groups 1, 2, and 3). Although group 2 included 17 patients only, the data suggest that the robotic platform may be of particular advantage in resections of the posterosuperior segments1, 47. In comparison, studies reporting on minor laparoscopic resections of the posterosuperior segments describe the technique as technically challenging. Moreover, when comparing converted procedures versus non-converted procedures, there are significantly more posterosuperior segments resections in the converted group (12.7% vs. 2.5%)47, 48. This is in line with the 2008 Louisville statement, which recommends laparoscopic liver resection for lesions located in segments 2 to 6, but recommended that laparoscopic resections of segments 1, 7 and 8 should not be considered as standard of care due to their difficult to reach location20. In major liver resection, use of the robotic platform leads to a larger number of procedures performed totally laparoscopically31.
Taken together, the data show that robot-assisted laparoscopic liver resection is suitable for both minor and major resections. The authors speculate that minimally invasive approaches to liver surgery, nowadays still widely performed in an open manner, will more likely come through robotic surgery. Since in minor liver resection, rather than in major resection, size of the incision dominates postoperative recovery, it is suggested that the greatest potential clinical benefit of the robotic platform lies in minor resection of difficult located lesions.
How to proceed with further clinical implementation? First, surgical technique needs to be refined and clarified in larger studies. For instance, it remains unclear which technique is best for parenchymal transection during robotic liver resection. Wristed (bipolar forceps, PK dissector, Vessel Sealer) as well as non-wristed (Harmonic curved shears) coagulation devices, as well as clip appliers, staplers, and plain sutures may all be suitable for precise parenchymal dissection, however, their comparison needs to be worked out. As of yet, the CUSA system, widely used in open and laparoscopic liver surgery, is not available for the robotic platform. Also, optimal patient position, port placement, and possible elimination of transthoracic trocars in segment 7–8 resections needs to be clarified along with novel applications such as indocyanine-green biliary contrast (FireFly imaging) and integrated augmented-reality navigation. Second, cost of the robot-assisted laparoscopic liver resection compared to conventional laparoscopy needs to be assessed.
In conclusion, based on the currently available literature, robot-assisted liver resection seems to be safe and feasible in selected patients for all categories of liver resection. The real benefit of the use of a robotic system over conventional laparoscopy presumably lies in minor resections of the posterior segments. However, given the limited number of available studies, large randomized studies are needed to compare robot-assisted surgery with conventional laparoscopy and open surgery.
Acknowledgments
The authors like to thank Dr. G.H. Choi, Department of Surgery, Yonsei University Health System, Seoul, South Korea, Dr. E. Felli, Digestive and Transplant Liver Surgery Unit, S.Camillo Hospital, Rome, Italy, Dr. P.C. Giulianotti and D. Daskalaki, MD, Division of General, Minimally Invasive and Robotic Surgery, University of Illinois, Chicago, IL, USA, Dr. M.G. Spampinato, Department of General and Advanced Minimally Invasive Surgery, Abano Terme, Italy, Dr. A. Tsung and D. Sukato, BA, Department of Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USA, Dr. K.H. Kim, Department of Surgery, Asan Medical Center, Seoul, South Korea and Dr. Y.-D. Yu, Department of Surgery, Korea University College of Medicine, Seoul, South Korea, for providing additional data from their studies.
The authors also like to thank R. van Hillegersberg, J.P. Ruurda, A. Gerritsen, F.J. Smits, and D.S.J. Tseng for support during preparation of the manuscript. This work was supported in part by KWF UU 2014-6904 (to JH).
Footnotes
Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.hpb.2015.09.003.
Conflicts of interest and source of funding
C.L. Nota, I.H. Borel Rinkes, I.Q. Molenaar, H.C. van Santvoort, Y. Fong and J. Hagendoorn have no conflicts of interest or financial ties to disclose.
Appendix A. Supplementary data
The following are the supplementary data related to this article:
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