Sage Journals: Discover world-class research

Abstract

Background:

Theoretical advantages of robotic surgery compared to conventional laparoscopic surgery include improved instrument dexterity, 3D visualization, and better ergonomics. This systematic review and meta-analysis aimed to determine advantages of robotic surgery over laparoscopic surgery in patients undergoing liver resections.

Method:

A systematic literature search was conducted for studies comparing robotic assisted or totally laparoscopic liver resection. Meta-analysis of intraoperative (operative time, blood loss, transfusion rate, conversion rate), oncological (R0 resection rates), and postoperative (bile leak, surgical site infection, pulmonary complications, 30-day and 90-day mortality, length of stay, 90-day readmission and reoperation rates) outcomes was performed using a random effects model.

Result:

Twenty-six non-randomized studies including 2630 patients (950 robotic and 1680 laparoscopic) were included, of which 20% had major robotic liver resection and 14% had major laparoscopic liver resection. Intraoperatively, robotic liver resection was associated with significantly less blood loss (mean: 286 vs 301 mL, p < 0.001) but longer operating time (mean: 281 vs 221 min, p < 0.001). There were no significant differences in conversion rates or transfusion rates between robotic liver resection and laparoscopic liver resection. Postoperatively, there were no significant differences in overall complications, bile leaks, and length of hospital stay between robotic liver resection and laparoscopic liver resection. However, robotic liver resection was associated with significantly lower readmission rates than laparoscopic liver resection (odds ratio: 0.43, p = 0.005).

Conclusions:

Robotic liver resection appears to offer some advantages compared to conventional laparoscopic surgery, although both techniques appear equivalent. Importantly, the quality of evidence is generally limited to cohort studies and a high-quality randomized trial comparing both techniques is needed.

Keywords

Robotic hepatectomy outcomes complications laparoscopic costs

Introduction

Over the last decade, robotic surgery has emerged as a potentially valid alternative to conventional laparoscopic surgery. Advantages of current robotic surgical platforms include 3D visualization of the surgical field and improved instrument dexterity which may facilitate complex dissection and surgical reconstructions. In addition, the use of an ergonomic surgical console may reduce surgeon fatigue for long and complex procedures as well as easier control of bleeding which are two of the reasons why the laparoscopic approach remains unpopular for major resections (1). In addition, robotic liver resections (RLR) may therefore encourage more surgeons to take up complex minimally invasive techniques which they previously would not have considered doing. Robotic surgery has been shown to be superior to conventional laparoscopic surgery in a variety of different complex surgical procedures. For instance, robotic surgery for distal pancreatectomy is associated with significantly lower conversion rates and shorter hospital stay compared to laparoscopic surgery (2).

Minimally invasive liver resections (MILR) has been gaining popularity in recent years, with systematic reviews suggesting minimally invasive pancreaticoduodenectomy (MIPD) (combining both laparoscopic (LLR) and RLR) were associated with significantly less blood loss, and lower rates of margin-positive resections compared to conventional (open) liver resections (3 –5). A recent meta-analysis comparing LLR and open liver resection for the management of hepatocellular carcinoma has concluded that the use of the laparoscopic approach is associated with less intraoperative blood loss, the need for a blood transfusion, increased R0 resection rates and shorter length of hospital stay. However, LLR and open liver resections have similar overall survival, disease free survival and rates of recurrence (3). The laparoscopic approach was, however, associated with a shorter duration of hospital stay and lower overall complications (6). The ongoing ORANGE SEGMENTS and ORANGE-II PLUS randomized controlled trials will provide high-quality evidence on the benefit of LLR over open liver resection (7). Whether the use of a robotic approach may prove to be superior to both the conventional laparoscopic and open techniques for liver resections still remains to be determined (8).

To date, evidence comparing the benefits of RLR and LLR is limited (9), and more data are still needed to offer clearer guidance on the future development of minimally invasive liver surgery. The aim of this systematic review and meta-analysis was to evaluate the current evidence regarding RLR and to compare its advantages with the conventional laparoscopic approaches.

Methods

Search Strategy

A systematic search of PubMed, EMBASE, and the Cochrane Library databases was conducted on the 21 March 2019 by two independent investigators (S.K.K., J.B.). The search terms used were “robotic surgery,” or “laparoscopic surgery,” or “open surgery,” and “hepatectomy,” or “liver resection” either individually or in combination. The “related articles” function was used to broaden the search, and all citations were considered for relevance. A manual search of reference lists in recent reviews and eligible studies was also undertaken. A summary of search terms are presented in Supplementary Table 1. This paper is reported according to the PRISMA guidelines and flow diagram presented in Fig. 1 (10). This study was prospectively registered with the PROSPERO database (Registration CRD42019131493).

Fig. 1.

Flowchart of PRISMA diagram.

Inclusion and Exclusion Criteria

Inclusion criteria were as follows: (1) studies comparing the use of robotic and laparoscopic for liver resections for benign and malignant indications and (2) published in the English language. Exclusion criteria were as follows: (1) conference abstracts, review articles, and case reports (<5 patients), (2) non-comparative analysis between minimally invasive surgery, and (3) studies where outcomes were not reported separately for robotic and laparoscopic surgery. After excluding duplicates, two researchers (S.K.K., J.B.) independently reviewed the titles and abstracts of studies identified by the literature search. Where a study was considered to be potentially relevant to the research question a full copy of the publication was obtained for further review. The reference lists of all included studies were hand-searched in order to identify other potentially relevant studies. Any areas of disagreement between the two primary researchers were resolved through discussion.

Study Outcomes

The primary outcome measure was post-operative complications such as overall and major complications (⩾Grade III reported according to Clavien-Dindo Classification) (11). Secondary outcome measures were intraoperative (operative time, blood loss, transfusion rate, conversion rate), oncological (R0 resection rates), and surgery-specific complications such as bile leak, surgical site infection, pulmonary complications, 30-day and 90-day mortality, length of stay, 90-day readmission and reoperation rates. Intraoperative techniques such as Pringle maneuver and vascular clamping were also evaluated.

Definitions

TR was defined as complete use of the robotic technique for liver resection without laparoscopic or hand-assisted techniques during the procedure, this also included the use of laparoscopic ports by a surgical assistant as part of the robotic procedure. TL was defined as complete use of a laparoscopic technique for liver resection without robotic or hand-assisted techniques. Overall and major complications were defined according to the Clavien-Dindo classification, whereby major complications were defined as ⩾Grade III Clavien-Dindo complications (11 –14).

Data Extraction

The following data were extracted from the papers: name of first author, year of publication, country of study conducted, study design, number of patients in robotic and laparoscopic group, patients’ characteristics (age, gender, ASA score, body mass index (BMI), pathology type, size of lesion), surgical techniques (use of Pringle’s manouvre, parenchymal transection), intra-operative variables (operative time, total blood loss, transfusion rate, conversion rate, R0 margin status), and post-operative variables (length of stay, 90 days readmission rate, 90 days reoperation rate, complication rate, major complication rate, bile leaks, pulmonary complications, and surgical site infections).

Quality Assessment

Methodological quality and standard of outcome reporting within included studies were assessed by two independent researchers (S.K.K., J.B.). Methodological quality was formally assessed using the Newcastle-Ottawa score (NOS) for cohort studies (S.K.K., J.B.) and the Cochrane Risk of Bias Tool for randomized controlled trial, where applicable (15,16).

Statistical Analysis

This systematic review and meta-analysis were conducted in accordance with the recommendations of the Cochrane Library and PRISMA guidelines (17,18). For categorical variables, analysis was performed by calculating the odds ratio (OR). The random effects called the DerSimonian-Laird method was used for the meta-analysis of outcomes. Funnel plots were used to visually assess publication bias of included studies. Heterogeneity between studies was assessed using the I₂ value in order to determine the degree of variation not attributable to chance alone. I₂ values were considered to represent low, moderate, and high degrees of heterogeneity where values were <25%, 25–75%, and >75%, respectively. Funnel plot asymmetry was assessed using the Egger test. Statistical significance was considered when p < 0.05. Statistical analyses were performed using the R Foundation Statistical software (R 3.2.1) and Stata 15 (Version 15.1, StataCorp, College Station, Texas) as previously described (2,18).

Results

Patients’ Characteristics and Pre-Operative Variables

This review included 26 studies involving 2630 patients (950 robotic and 1680 laparoscopic) undergoing liver resections. Study selection as a PRISMA flowchart is summarized in Fig. 1. Study-level and patient-level characteristics of RLR and LLR groups are listed in Table 1. Median NOS study quality assessment score was 7, ranging from 6 to 9 across the studies (Table 2), reflecting high study qualities. None of the studies had a blinded assessment of the outcomes or performed a prospective calculation of sample size.

Table 1

Details of included studies reporting minimally invasive surgery for hepatectomy.

Study demographics				Patients, n			Age, years		ASA Grade > 1, %		BMI, kg/m²		Male, %
Study name	Country	Study interval	Study design	Overall	TR	TL	TR	TL	TR	TL	TR	TL	TR	TL
Berber et al. (19)	USA	October 2008—September 2009	RCS	32	9	23	67 (6)	67 (10)	NR	NR	NR	NR	78	52
Packiam et al. (2012) (20)	USA	January 2009–July 2011	RCS	29	11	18	57 (16)	52 (17)	NR	NR	31 (7)	29 (7)	27	22
Lai et al. (2013) (21)	China	October 1998–March 2012	RCS	66	33	33	NR	NR	NR	NR	NR	NR	0	0
Troisi et al. (2013) (25)	Belgium	January 2004–March 2012	RCS	263	40	223	65 (12)	55 (16)	NR	NR	NR	NR	68	44
Spampinato et al. (2014) (26)	Italy	January 2009–December 2012	RCS	50	25	25	63 (32–80)	62 (33–80)	92	76	24 (16–22)	25 (20–29)	52	40
Wu et al. (2014) (27)	Taiwan	2007–2011	RCS	79	38	41	61 (15)	54 (14)	NR	NR	NR	NR	84	68
Yu et al. (2014) (28)	Korea	July 2007–October 2011	RCS	30	13	17	50 (12)	53 (10)	NR	NR	NR	NR	54	53
Kim et al. (43)	Korea	May 2007–July 2013	RCS	43	12	31	54 (12)	56 (12)	NR	NR	NR	NR	50	58
Lai (2016) (22)	China	October 1998–February 2015	RCS	135	100	35	62 (11)	58 (10)	NR	NR	NR	NR	66	74
Lee et al. (2016) (29)	China	November 2003–January 2015	RCS	67	38	29	60 (34–80)	59 (20–81)	89	79	NR	NR	68	52
Lee et al. (2016) (29)	China	November 2003–January 2015	RCS	136	70	66	58 (20–82)	58 (25–85)	86	80	NR	NR	66	59
Montalti et al. (2016) (31)	Belgium	June 2008–February 2014	RCS	108	36	72	62 (32–84)	57 (17–79)	89	86	NR	NR	58	54
Efanov et al. (2017) (32)	Russia	May 2010–June 2016	RCS	131	40	91	45 (18–76)	51 (21-77)	NR	NR	NR	NR	23	40
Magistri et al. (2017) (33)	Italy	June 2012–May 2016.	RCS	46	22	24	61 (10)	67 (12)	100	100	27 (4)	27 (4)	82	63
Salloum et al. (2017) (34)	France	March 1997–February 2011	RCS	96	16	80	56 (15)	58 (16)	38	30	27 (5)	26 (5)	50	48
Marino et al. 2019 (35)	Poland	April 2016–March 2017	RCS	34	14	20	58 (10)	62 (10)	100	100	28 (5)	28 (7)	57	55
Fruscione et al. 2019 (36)	USA	2011–2016	RCS	173	57	116	58 (16)	53 (15)	100	100	28 (6)	30 (7)	35	45
Lim et al. 2019 (37)	Italy	2011–2017	RCS	172	61	111	66 (10)	63 (12)	NR	NR	25 (4)	26 (6)	67	75
Lai et al. 2011 (23)	China	January 1998–August 2010	PCS	7	6	1	NR	NR	NR	NR	NR	NR	0	0
Lai et al. 2011 (23)	China	January 1998–August 2010	PCS	19	9	10	NR	NR	NR	NR	NR	NR	0	0
Lai et al. 2012 (24)	China	October 1998–January 2011	PCS	49	32	17	NR	NR	0	0	NR	NR	0	0
Ji et al. 2011 (38)	China	April–July 2009	RCS	33	13	20	53 (39–79)	NR	NR	NR	NR	NR	69	NR
Tranchart et al. 2010 (39)	France	January 2008–April 2013	RCS	56	28	28	67 (42–84)	66 (41–78)	82	82	26 (17–36)	23 (16–33)	46	46
Croner 2016 et al. (40)	Germany	2011–2015	RCS	29	10	19	64 (45–76)	59 (32–85)	90	89	28	27	80	68
Cortolillo et al. 2019 (41)	USA	2013–2014	RCS	724	204	520	NR	NR	NR	NR	NR	NR	0	0
Lee et al. 2019 (42)	Korea	June 2016–April 2018	RCS	23	13	10	62.2 (9.8)	58.8 (11.2)	0	0	NR	NR	54	50

ASA: American Society of Anaesthesiology; BMI: body mass index; TR: totally robotic; TL: totally laparoscopic; RCS: retrospective cohort study; NR: not reported; PCS: prospective cohort study.

Table 2

Study quality according to Newcastle Ottawa Scale.

Study name	Study design	Selection	Comparability	Reliability	Total
Berber et al. (19)	RCS	4	2	3	9
Packiam et al. 2012 (20)	RCS	3	1	3	7
Lai et al. 2013 (21)	RCS	3	0	3	6
Troisi et al. 2013 (25)	RCS	4	2	3	9
Spampinato et al. 2014 (26)	RCS	4	2	3	9
Wu et al. 2014 (27)	RCS	3	1	3	7
Yu et al. 2014 (28)	RCS	3	1	3	7
Kim et al. (43)	RCS	3	2	3	8
Lai 2016 (22)	RCS	3	2	2	7
Lee et al. 2016 (29)	RCS	3	2	3	8
Lee et al. 2016 (29)	RCS	4	2	2	8
Montalti et al. 2016 (31)	RCS	3	1	3	7
Efanov et al. 2017 (32)	RCS	4	0	3	7
Magistri et al. 2017 (33)	RCS	3	2	3	8
Salloum et al. 2017 (34)	RCS	3	2	3	8
Marino et al. 2019 (35)	RCS	4	1	3	8
Fruscione et al. 2019 (36)	RCS	3	0	3	6
Lim et al. 2019 (37)	RCS	4	2	3	9
Lai et al. 2011 (23)	PCS	3	0	3	6
Lai et al. 2011 (23)	PCS	3	0	3	6
Lai et al. 2012 (24)	PCS	4	0	3	7
Ji et al. 2011 (38)	RCS	3	2	2	7
Tranchart et al. 2010 (39)	RCS	4	2	2	8
Croner et al. 2016 (40)	RCS	3	2	3	8
Cortolillo et al. 2019 (41)	RCS	4	2	2	8
Lee et al. 2019 (42)	RCS	3	0	3	6

PCS: prospective cohort study; RCS: retrospective cohort study.

Patient-level characteristics were analyzed through meta-analysis. There were no significant differences in age, gender, American Society of Anaesthesiologist (ASA) grade, BMI, previous abdominal surgery, and malignant tumor pathology between both groups (Table 1, Supplementary Fig. 1A to F). There were also no significant differences in tumor number, tumor size, and tumor type (both hepatocellular carcinoma (HCC) and colorectal liver metastases (CRLM)). Patients undergoing RLR had significantly lower rates of cirrhosis than LLR (OR: 0.67, p = 0.017, I² = 0%, Supplementary Fig. 1G). Types of liver resections for each study are presented in Supplementary Table 2.

Extent of Surgical Resection

Of the 26 studies included in the review, 14 studies included a mix of major and minor resections, 10 studies included minor resections only, and 2 studies included major resections. Of the 10 studies reporting minor resections, only 3 studies reported outcomes for left lateral section resections. A summary of the extent of resection are presented in Supplementary Table 2.

Parenchymal Transection

Of the 26 studies, 21 studies reported the type of parenchymal transection for both RLR and LLR. Harmonic scalpel (20 vs 15 studies) and Cavitron Ultrasonic Surgical Aspirator (5 vs 12 studies) were the most commonly used transection techniques for RLR and LLR, respectively. Parenchymal transection techniques are presented in Supplementary Table 3.

Intra-Operative Outcomes

Twenty-five studies reported operative times, all of which included docking times. RLR had significantly longer operating time than LLR (mean: 281 vs 221 min, p < 0.001; I² = 90%) (Fig. 2A). Twenty-four studies reported blood loss showing significantly less after RLR compared to LLR (mean: 286 vs 301 mL, p < 0.001; I² = 99%) (Fig. 2B). Pringle’s maneuver and vascular clamping were reported in eight and four studies, respectively. There were no significant differences between use of Pringle maneuver and vascular clamping between RLR and LLR (Table 3). Transfusion rates, conversion rates, and R0 resection rates were reported in 11, 17, and 13 studies, respectively. There were no significant differences in transfusion rate (10% vs 8%, OR: 1.13, CI_95%: 0.49–2.58, p = 0.8; I² = 50%; Fig. 2C), conversion rate (6% vs 8%, OR: 0.86, CI_95%: 0.49–1.51, p = 0.6; I² = 32%; Fig. 2D) and R0 resection rate (89% vs 86%, OR: 1.24, CI_95%: 0.85–1.79, p = 0.3; I² = 0%; Fig. 2E) between RLR and LLR.

Fig. 2.

Meta-analysis of intraoperative and oncological outcomes (A) operating time (B) blood loss (C) pringle maneuver (D) use of vascular clamping (E) duration of vascular clamping (F) blood transfusion (G) conversion (H) R0 resection.

Table 3

Summary of the meta-analysis regarding baseline demographics, intraoperative and postoperative outcomes.

Outcomes	Number of studies	OR/MD (CI_95%)	p-value	I2, %
Baseline Demographics
Age, years	20	1.43 (−0.53–3.40)	0.2	54
Gender, male	20	0.99 (0.74–1.34)	1.0	0
ASA grade, > 1	7	1.52 (0.94–2.47)	0.090	0
BMI, kg/m²	9	0.14 (−1.52–1.80)	0.9	88
Previous abdominal surgery	7	0.69 (0.39–1.21)	0.2	54
Tumor number, solitary	9	0.70 (0.47–1.04)	0.079	11
Tumor size, mm	18	2.25 (−1.24–5.74)	0.2	66
Tumor pathology, malignant	16	0.98 (0.59–1.66)	1.0	67
Tumor type, HCC	13	0.94 (0.66–1.34)	0.7	0
Tumor type, CRLM	14	1.11 (0.79–1.56)	0.6	0
Presence of cirrhosis, yes	11	0.67 (0.48–0.93)	0.017	0
Intraoperative
Operating time, min	25	57 (36–77)	<0.001	90
Blood loss, mL	24	−51 (−68–−36)	<0.001	99
Pringle maneuver	8	3.33 (0.96–11.63)	0.058	74
Vascular clamping, yes	4	0.81 (0.20–3.25)	0.8	76
Duration vascular clamping, min	3	7.32 (−6.48–21.13)	0.3	94
Transfusion rate	11	1.13 (0.49–2.58)	0.8	50
Conversion rate	17	0.86 (0.49–1.51)	0.6	32
R0 resection rate	13	1.24 (0.85–1.79)	0.3	0
Post-operative
Overall complications	24	0.93 (0.70–1.24)	0.6	0
Major complications	10	1.06 (0.60–1.85)	0.8	0
Bile Leak	12	1.59 (0.78–3.24)	0.2	0
SSI	5	0.66 (0.26–1.69)	0.4	0
Pulmonary complications	6	0.88 (0.32–2.45)	0.8	41
Liver failure	4	1.34 (0.27–6.71)	0.7	10
30 day mortality	8	0.56 (0.19–1.60)	0.3	0
90 day mortality	2	0.72 (0.07–7.13)	0.8	0
Length of stay, days	22	−0.27 (−0.83–0.28)	0.3	80
90 days readmission rate	4	0.43 (0.24–0.78)	0.005	9
90 days reoperation rate	6	0.88 (0.26–2.98)	0.8	0

OR: odds ratio; CI: confidence interval; ASA: American Society of Anaesthesiologist; BMI: body mass index; HCC: hepatocellular carcinoma; CRLM: colorectal liver metastatses; SSI: surgical site infection.

Bold values indicate significant p-values.

Post-Operative Outcomes

Overall and major complications were reported in 24 and 10 studies, respectively. There were no significant differences in complication rates between RLR and LLR for overall (OR: 0.93, CI_95%: 0.70–1.24, p = 0.6; I² = 0%; Fig. 3A) and major complications (OR: 1.06, CI_95%: 0.60–1.85, p = 0.8; I² = 0%; Fig. 3B). Bile leaks, surgical site infections, pulmonary complications and liver failure were reported in 12, 5, 6, and 4 studies, respectively. There were no significant differences in bile leak (3% vs 2%, OR: 1.59, CI_95%: 0.78–3.24, p = 0.2; I² = 0%; Fig. 3C), surgical site infections (SSI) (OR: 0.66, CI_95%: 0.26–1.69, p = 0.4; I² = 0%; Fig. 3D), pulmonary complications (OR: 0.88, CI_95%: 0.32–2.45, p = 0.8; I² = 0%; Fig. 3E) and liver failure (OR: 1.34, CI_95%: 0.27–6.71, p = 0.7; I² = 10%; Fig. 3F) between RLR and LLR.

Fig. 3.

Meta-analysis of postoperative outcomes (A) overall complications (B) major complications (C) bile leak (D) surgical site infection (E) pulmonary complications (F) liver failure (G) 30-day mortality (H) 90-day mortality (I) length of stay (J) 90-day readmission (K) 90-day reoperation.

Peri-operative 30-day and 90-day mortality were reported in eight and two studies, respectively. There was no significant difference in 30 day (0% vs 1%, OR: 0.56, CI_95%: 0.19–1.60, p = 0.3; I² = 0%) and 90 day (0% vs 1%, OR: 0.72, CI_95%: 0.07–7.13, p = 0.8; I² = 0%) mortality rates between RLR and LLR.

Length of hospital stay was reported in all 22 studies. There were no significant differences in length of hospital stay between RLR and LLR (mean: 7 vs 8 days, p = 0.3; I² = 80%). Readmission rates at 90 days were reported in all four studies. Patients undergoing RLR had significantly lower readmission rates than LLR (4% vs 11%, OR: 0.43, CI_95%: 0.24–0.78, p = 0.005; I² = 9%) (Fig. 3G).

Publication Biases

Funnel plot analysis for the intra-operative and post-operative variables was done to assess the possibility of publication bias. All of the studies were within 95% CI, and there was no evidence of publication bias in this study for all outcomes studied.

Discussion

Over the last decade, both laparoscopic and robotic approaches have been applied to a variety of HPB resections. However, minimally invasive liver resection remains limited to specialist centers with no general consensus regarding the translatability of minimally invasive liver surgery for improving clinical outcomes, although recent guidelines have been developed to guide surgeons as to its appropriate application (44). Several meta-analyses have published outcomes comparing robotic and open liver resections, which have demonstrated that RLR were associated with significantly lower overall complications, blood loss and blood transfusion along with a shorter hospital stay by 3–5 days (3,5). Oncologically, RLR achieves slightly better but still significant R0 resection rates (93% vs 94%).

Theoretical advantages of robotic technology include improved dexterity, visual magnification and precision by eliminating surgical tremor (45). For experienced liver surgeons who are only familiar with an open approach, the learning curve for robotic-assisted surgery may be less steep compared with conventional laparoscopic surgery (46 –48). This is evident from lower rates of conversion in a recent meta-analysis in distal pancreatic resections and also to be a robotic surgeon the skills are not necessarily transferable from laparoscopic (2). Since the first reported robotic-assisted liver resection performed in 2003 in Italy (49), case reports and single institution series of RLR have been published, highlighting the feasibility of the robotic approach for major and minor hepatectomies (50). Despite the encouraging early outcomes demonstrated by these studies, no single study has provided conclusive results in favor of either approach Furthermore, robotic liver resection may offer expansion to more complex cases such as major hepatectomies, extended hepatectomies with biliary reconstruction and difficult segmentectomies of the posterior-superior segments. For instance, LLR of posterosuperior (PS) segments (Segments 1, 4a, 7, and 8) are considered to be challenging due to liver mobilization and access along with control of any bleeding (51 –53). Many authors do not consider lesions in PS segments to be amenable to a pure laparoscopic approach, while others advocate ‘‘hand assistance” (54).

Compared with previous published meta-analysis (55 –57), more high-quality studies and patients undergoing minimally invasive laparoscopic surgery (MILS) have been included, providing more reliable evidence. This systematic review and meta-analysis highlights (1) the current evidence supporting both RLR and LLR to be similar but limited to retrospective cohort studies (2) although the robotic approach was associated with a longer operating time, RLR was associated with less blood loss and readmission rates (3) comparable outcomes in terms of complications, blood transfusion and conversion rates reaffirm some of the difficulties faced in performing minimally invasive liver resections. Although we accept that RLR took longer there was still no statistical difference in terms of hospital stay or R1 resection rate, which confirms the two approaches are similar in terms of safety and effectiveness. This highlights the importance of continuing to develop RLR so as to develop further marginal gains.

Similar trends were seen between robotic and laparoscopic approaches in other surgical procedures such as nephrectomy (58), hysterectomy (59), anterior resections for rectal cancers (60) and distal pancreatectomy (2), where similar morbidity and mortality of the two minimally invasive approaches have been reported, but the majority all show lower conversion rates during robotic surgery for hysterectomy (59) (OR: 0.29, CI_95%: 0.18–0.46) and anterior resections (60) (OR: 0.58, CI_95%: 0.35–0.97, p = 0.04), although non-significant in radical nephrectomy (58) (OR: 0.44, CI_95%: 0.18–1.09, p = 0.08) were noted.

This review also found significantly less blood loss during RLR compared to LLR. To our knowledge, bleeding can be controlled more easily and freely in robotic surgery due to the seven degrees of freedom afforded by the EndoWrist and the three-dimensional optics. However, these advantages do not embody in the present study. On the one hand, more major hepatectomies have prolonged operative time and are associated with more blood loss. On the other hand, the robotic system does not provide an ultrasonic dissector, which is the most popular device for parenchymal transection in the United Kingdom (61). During robotic surgery, parenchymal transection is usually conducted using either the harmonic scalpel, Endowrist sealer, scissors or bipolar forceps (43). This is because the Cavitron Ultrasonic Surgical Aspirator (CUSA) is not available in a robotic format. However, it can be used through an assistant port but in general has been obsolete during our robotic liver resections. This area needs further development and engagement with companies who manufacture parenchymal transection devices.

Previously, it was thought that intermittent inflow occlusion (Pringles maneuver) was more commonly used after RLR and seldomly performed in LLR. This maneuver creates an ischemia/reperfusion injury particularly in patients with cirrhotic livers. However, this review found no significant differences in rates of Pringle’s maneuver or vascular clamping between RLR and LLR. Also, robotic enthusiasts would also argue that the superior vision quality allows a more bloodless field as smaller vessels can be seen more readily and dealt with before they start bleeding.

Since limited studies in this review report total costs of RLR, we did not evaluate the cost associated with RLR, although it has been well described elsewhere that this procedure does typically incur an increased cost for the institution (19,62). Notwithstanding this disadvantage having a robotic program may actually have the opposite effect by increasing the number of referrals (patient choice) thus actually increasing income for the institution but again this is yet to be proven. It is perceived that over coming years the development of new robotic systems will increase competition in the marketplace and lower the overall cost of robotic surgery making it more accessible for institutions and thus making RLR more likely to achieve at least cost neutrality when compared to LLR. Also, lower conversion rates as shown previous review may translate to lower overall hospital costs (2). Nevertheless, it could also be argued that robotic systems will become technologically more advanced thus actually increasing cost.

Our review has strengths important to note such as high-quality rating of all included studies and detailed data extraction encompassing several intra-operative and postoperative outcomes. This review has limitations which are important to address. First, all studies included in this review were mainly retrospective, lacking any randomized controlled trials. This may reflect that RLR is still in the early phase of the learning curve. Second, none of the studies have evaluated the long-term outcomes such as survival, which limits our ability to draw useful prognostic conclusions and improvements in quality of life. Finally, all studies in this review do not stratify outcomes between indication (benign and malignant) and neither extent of surgery (minor or major) hepatectomy which are also important to know. However, only two studies included major resections and similar results were observed for patients undergoing minor resections only.

Conclusion

In summary, this systematic review and meta-analysis comparing RLR and LLR suggest that both techniques can be used safely. RLR appears to offer some advantages compared to LLR, although both techniques appear equivalent. Further studies and in particular a randomized controlled trial (RCT) is warranted to enable us to draw meaningful conclusions regarding patients’ survival, quality of life, cost and long-term oncological outcome.

Supplemental Material

sj-pdf-1-sjs-10.1177_1457496920925637 – Supplemental material for Robotic versus conventional laparoscopic liver resections: A systematic review and meta-analysis

Supplemental material, sj-pdf-1-sjs-10.1177_1457496920925637 for Robotic versus conventional laparoscopic liver resections: A systematic review and meta-analysis by Sivesh Kathir Kamarajah, James Bundred, Derek Manas, Long Jiao, Mohammad Abu Hilal and S. A. White in Scandinavian Journal of Surgery

Footnotes

Author contributions

All authors listed in this manuscript meet the authorship requirements set out by the International Committee of Medical Journal Editors (ICMJE). Conception and design was done by S.K. and S.A.W. Analysis and interpretation was done S.K., J.B., and S.A.W. Data collection was by SK and JB. The article was written by S.K., D.M.M., L.R.J., M.A.B., and S.A.W. Critical revision of the article was done by S.K., D.M.M., L.R.J., M.A.B., and S.A.W.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Sivesh K Kamarajah

Supplemental material

Supplemental material for this article is available online.

References

Palep

: Robotic assisted minimally invasive surgery. J Minim Access Surg 2009;5(1):1–7.

Kamarajah

Sutandi

Robinson

, et al: Robotic versus conventional laparoscopic distal pancreatic resection: A systematic review and meta-analysis. HPB (Oxford) 2019:21:1107–1118.

Jiang

Yan

Zhang

: Meta-analysis of laparoscopic versus open liver resection for hepatocellular carcinoma. Hepatol Res 2018;48(8):635–663.

Guo

Gao

Chen

, et al: Minimally invasive versus open simultaneous resections of colorectal cancer and synchronous liver metastases: A meta-analysis. Am Surg 2018;84(2):192–200.

Machairas

Papaconstantinou

Tsilimigras

, et al: Comparison between robotic and open liver resection: A systematic review and meta-analysis of short-term outcomes. Updates Surg 2019;71:39–48.

Chen

Liu

Pan

, et al: Expanding laparoscopic pancreaticoduodenectomy to pancreatic-head and periampullary malignancy: Major findings based on systematic review and meta-analysis. BMC Gastroenterol 2018;18(1):102.

van Dam

Wong-Lun-Hing

van Breukelen

, et al: Open versus laparoscopic left lateral hepatic sectionectomy within an enhanced recovery ERAS(R) programme (ORANGE II-trial): Study protocol for a randomised controlled trial. Trials 2012;13:54.

van Hilst

de Rooij

Bosscha

, et al: Laparoscopic versus open pancreatoduodenectomy for pancreatic or periampullary tumours (LEOPARD-2): A multicentre, patient-blinded, randomised controlled phase 2/3 trial. Lancet Gastroenterol Hepatol 2019;4(3):199–207.

Hirst

Philippou

Blazeby

, et al: No surgical innovation without evaluation: Evolution and further development of the IDEAL framework and recommendations. Ann Surg 2019;269(2):211–220.

10.

Liberati

Altman

Tetzlaff

, et al: The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ 2009;339:b2700.

11.

Clavien

Barkun

de Oliveira

, et al: The Clavien-Dindo classification of surgical complications: Five-year experience. Ann Surg 2009;250(2):187–196.

12.

Dindo

Muller

Weber

, et al: Obesity in general elective surgery. Lancet 2003;361(9374):2032–2035.

13.

EuroSurg Collaborative: Body mass index and complications following major gastrointestinal surgery: A prospective, international cohort study and meta-analysis. Colorectal Dis 2018;20(8):O215–O225.

14.

Kamarajah

Sowida

Adlan

, et al: Preoperative assessment of patients undergoing elective gastrointestinal surgery: Does body mass index matter? J Obes 2017;2017:4285204.

15.

Mertz

Loeb

: Newcastle-Ottawa Scale: Comparing reviewers’ to authors’ assessments. BMC Med Res Methodol 2014;14:45.

16.

Stang

: Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25(9):603–605.

17.

Stroup

Berlin

Morton

, et al: Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 2000;283(15):2008–2012.

18.

Kamarajah

Bundred

Tan

BHL

: Body composition assessment and sarcopenia in patients with gastric cancer: A systematic review and meta-analysis. Gastric Cancer 2019;22:10–22.

19.

Berber

Akyildiz

Aucejo

, et al: Robotic versus laparoscopic resection of liver tumours. HPB (Oxford) 2010;12(8):583–586.

20.

Packiam

Bartlett

Tohme

et al: Minimally invasive liver resection: Robotic versus laparoscopic left lateral sectionectomy. J Gastrointest Surg 2012;16(12):2233–2238.

21.

Lai

Yang

Tang

: Robot-assisted laparoscopic liver resection for hepatocellular carcinoma: Short-term outcome. Am J Surg 2013;205(6):697–702.

22.

Lai

Tang

: Long-term survival analysis of robotic versus conventional laparoscopic hepatectomy for hepatocellular carcinoma: A comparative study. Surg Laparosc Endosc Percutan Tech 2016;26(2):162–166.

23.

Lai

Tang

Yang

et al: Multimodality laparoscopic liver resection for hepatic malignancy—from conventional total laparoscopic approach to robot-assisted laparoscopic approach. Int J Surg 2011;9(4):324–328.

24.

Lai

Tang

: Conventional laparoscopic and robot-assisted laparoscopic liver resection for benign and malignant pathologies: A cohort study. J Robot Surg 2012;6(4):295–300.

25.

Troisi

Patriti

Montalti

et al: Robot assistance in liver surgery: A real advantage over a fully laparoscopic approach? Results of a comparative bi-institutional analysis. Int J Med Robot 2013;9(2):160–166.

26.

Spampinato

Coratti

Bianco

et al: Perioperative outcomes of laparoscopic and robot-assisted major hepatectomies: An Italian multi-institutional comparative study. Surg Endosc 2014;28(10):2973–2979.

27.

Lai

et al: Robotic-assisted minimally invasive liver resection. Asian J Surg 2014;37(2):53–57.

28.

Kim

Jung

et al: Robotic versus laparoscopic liver resection: A comparative study from a single center. Langenbecks Arch Surg 2014;399(8):1039–1045.

29.

Lee

Cheung

Chong

et al: Laparoscopic and robotic hepatectomy: Experience from a single centre. ANZ J Surg 2016;86(3):122–126.

30.

Lee

Fong

Chong

et al: Robotic liver resection for primary hepatolithiasis: Is it beneficial? World J Surg 2016;40(10):2490–2496.

31.

Montalti

Scuderi

Patriti

et al: Robotic versus laparoscopic resections of posterosuperior segments of the liver: A propensity score-matched comparison. Surg Endosc 2016;30(3):1004–1013.

32.

Efanov

Alikhanov

Tsvirkun

et al: Comparative analysis of learning curve in complex robot-assisted and laparoscopic liver resection. HPB 2017;19(9):818–824.

33.

Magistri

Tarantino

Guidetti

et al: Laparoscopic versus robotic surgery for hepatocellular carcinoma: The first 46 consecutive cases. J Surg Res 2017;217:92–99.

34.

Salloum

Lim

Lahat

et al: Robotic-assisted versus laparoscopic left lateral sectionectomy: Analysis of surgical outcomes and costs by a propensity score matched cohort study. World J Surg 2017;41(2):516–524.

35.

Marino

Shabat

Guarrasi

et al: Comparative study of the initial experience in performing robotic and laparoscopic right hepatectomy with technical description of the robotic technique. Dig Surg 2019;36(3):241–250.

36.

Fruscione

Pickens

Baker

et al: Robotic-assisted versus laparoscopic major liver resection: Analysis of outcomes from a single center. HPB 2019;21(7):906–911.

37.

Lim

Salloum

Tudisco

et al: Short- and long-term outcomes after robotic and laparoscopic liver resection for malignancies: A propensity score-matched study. World J Surg 2019;43(6):1594–1603.

38.

Wang

Zhao

et al: Robotic-assisted laparoscopic anatomic hepatectomy in China: Initial experience. Ann Surg 2011;253(2):342–348.

39.

Tranchart

Di Giuro

Lainas

et al: Laparoscopic resection for hepatocellular carcinoma: A matched-pair comparative study. Surg Endosc 2010;24(5):1170–1176.

40.

Croner

Perrakis

Hohenberger

et al: Robotic liver surgery for minor hepatic resections: A comparison with laparoscopic and open standard procedures. Langenbecks Arch Surg 2016;401(5):707–714.

41.

Cortolillo

Patel

Parreco

et al: Nationwide outcomes and costs of laparoscopic and robotic vs. open hepatectomy. J Robot Surg 2019;13(4):557–565.

42.

Lee

et al: The feasibility of robotic left-side hepatectomy with comparison of laparoscopic and open approach: Consecutive series of single surgeon. Int J Med Robot 2019;15(2):e1982.

43.

Kim

Park

Han

, et al: Robotic versus laparoscopic left lateral sectionectomy of liver. Surg Endosc 2016;30(11):4756–4764.

44.

Abu Hilal

Aldrighetti

Dagher

, et al: The Southampton consensus guidelines for laparoscopic liver surgery: From indication to implementation. Ann Surg 2018;268(1):11–18.

45.

Idrees

Bartlett

: Robotic liver surgery. Surg Clin North Am 2010;90(4):761–774.

46.

Dokmak

Aussilhou

Fteriche

, et al: Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg 2016;263(3):e48.

47.

Patriti

Marano

Casciola

: MILS in a general surgery unit: Learning curve, indications, and limitations. Updates Surg 2015;67(2):207–213.

48.

Sudan

Bennett

Jacobs

, et al: Multifactorial analysis of the learning curve for robot-assisted laparoscopic biliopancreatic diversion with duodenal switch. Ann Surg 2012;255(5):940–945.

49.

Giulianotti

Coratti

Angelini

, et al: Robotics in general surgery: Personal experience in a large community hospital. Arch Surg 2003;138(7):777–784.

50.

Kowalewski

Schmidt

Proctor

, et al: Skills in minimally invasive and open surgery show limited transferability to robotic surgery: Results from a prospective study. Surg Endosc 2018;32(4):1656–1667.

51.

Buell

Cherqui

Geller

, et al: The international position on laparoscopic liver surgery: The Louisville statement, 2008. Ann Surg 2009;250(5):825–830.

52.

Cho

Han

Yoon

, et al: Feasibility of laparoscopic liver resection for tumors located in the posterosuperior segments of the liver, with a special reference to overcoming current limitations on tumor location. Surgery 2008;144(1):32–38.

53.

Kazaryan

Rosok

Marangos

, et al: Comparative evaluation of laparoscopic liver resection for posterosuperior and anterolateral segments. Surg Endosc 2011;25(12):3881–3889.

54.

Nitta

Sasaki

Fujita

, et al: Laparoscopy-assisted major liver resections employing a hanging technique: The original procedure. Ann Surg 2010;251(3):450–453.

55.

Guan

Chen

Yang

, et al: Clinical efficacy of robot-assisted versus laparoscopic liver resection: A meta analysis. Asian J Surg 2019;42(1):19–31.

56.

Montalti

Berardi

Patriti

, et al: Outcomes of robotic vs laparoscopic hepatectomy: A systematic review and meta-analysis. World J Gastroenterol 2015;21(27):8441–8451.

57.

Qiu

Chen

Chengyou

: A systematic review of robotic-assisted liver resection and meta-analysis of robotic versus laparoscopic hepatectomy for hepatic neoplasms. Surg Endosc 2016;30(3):862–875.

58.

Leow

Heah

Chang

, et al: Outcomes of robotic versus laparoscopic partial nephrectomy: An updated meta-analysis of 4,919 patients. J Urol 2016;196(5):1371–1377.

59.

Xie

Cao

Yang

, et al: Robot-assisted surgery versus conventional laparoscopic surgery for endometrial cancer: A systematic review and meta-analysis. J Cancer Res Clin Oncol 2016;142(10):2173–2183.

60.

Prete

Pezzolla

Prete

, et al: Robotic versus laparoscopic minimally invasive surgery for rectal cancer: A systematic review and meta-analysis of randomized controlled trials. Ann Surg 2018;267(6):1034–1046.

61.

Lochan

Ansari

Coates

, et al: Methods of haemostasis during liver resection: A UK national survey. Dig Surg 2013;30(4–6):375–382.

62.

Magge

Zenati

Hamad

, et al: Comprehensive comparative analysis of cost-effectiveness and perioperative outcomes between open, laparoscopic, and robotic distal pancreatectomy. HPB (Oxford) 2018;20(12):1172–1180.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.67 MB