Abstract
Introduction:
The role of minimally invasive right anterior and right posterior sectionectomy (MI-RAS/MI-RPS) for right-sided liver lesions remains debatable. Although technically more demanding, these procedures might result in faster recovery and lower postoperative morbidity compared to minimally invasive right hemihepatectomy (MI-RH).
Methods:
This is an international multicenter retrospective analysis of 1114 patients undergoing MI-RH, MI-RAS and MI-RPS at 21 centers between 2006–2019. MIS included pure laparoscopic, robotic, hand-assisted or hybrid approach. A propensity matched and coarsened-exact matched analysis was performed.
Results:
1100 cases met study criteria of whom 759 underwent laparoscopic, 283 robotic, 11 hand-assisted and 47 laparoscopic-assisted (hybrid) surgery. There were 632 RH, 373 RPS and 95 RAS. There were no differences in baseline characteristics after matching. In the MI-RAS/MI-RPS group, median blood loss was higher (400 VS 300ml, p=0.001) as well as intraoperative blood transfusion rate (19.6% VS 10.7%, p=0.004). However, the overall morbidity rate was lower including major morbidity (7.1% VS 14.3%, p=0.007) and reoperation rate (1.4% VS 4.6%, p=0.029). The rate of close/involved margins was higher in the MI-RAS/MI-RPS group (23.4% VS 8.9%, p<0.001). These findings were consistent after both propensity and coarsened-exact matching.
Conclusion:
Although technically more demanding, MI-RAS/MI-RPS is a valuable alternative for MI-RH in right sided liver lesions with lower postoperative morbidity, possibly due to the preservation of parenchyma. However, the rate of close/involved margins is higher in these procedures. These findings might guide surgeons in preoperative counselling and in selecting the appropriate procedure for their patients.
Keywords: Laparoscopic liver resection, right hemihepatectomy, laparoscopic major liver resection, right posterior sectionectomy, right anterior sectionectomy
Precis
Minimally invasive right anterior and right posterior sectionectomy was associated with the advantages of lower postoperative morbidity at the expense of a higher blood loss and close/involved resection margins compared with minimally invasive right hemihepatectomy.
Introduction
Over the course of three decades, laparoscopic liver surgery (LLS) has been expanding worldwide. The initial uptake was slow, yet nowadays laparoscopy is the standard of care in many expert centers (1–2). Several papers showed the advantages of minimally invasive surgery (MIS) compared to the open approach in terms of less pain, reduced blood loss, shorter hospital stay and lower complication rates (3–8). Furthermore, the oncological results of LLS are at least equal or possibly even superior compared to open surgery (9,10). Data about robotic liver surgery (RLS) are more scarce. However, several analyses also suggested benefits compared to the open approach (11–14).
Nonetheless, debate remains about the management of large or deeply located right sided liver lesions requiring major hepatectomies. Today, minimally invasive right hemihepatectomy (MI-RH) is a standard procedure in many expert centers (1,2,8,15–17). However, the role of “technically major” anatomical resections such as right posterior and right anterior sectionectomies especially when performed via the minimally-invasive approach remains poorly well-defined (14,18). It is commonly accepted that MI-RH is technically less demanding than minimally invasive right anterior and right posterior sectionectomy (MI-RAS/MI-RPS) (19).
Although several authors have described the feasibility of these procedures (20–23), they remain highly technically challenging due to difficult access to the portal pedicle necessitating intra-operative ultrasound (IOUS), limited access hidden from the surgeon’s view and a large parenchyma transection area, theoretically leading to longer operating times, higher rates of bleeding and bile leak (19). Despite these limitations, the theoretical advantages resulting from the preservation of functional liver parenchyma potentially resulting in a decrease in overall and liver-specific morbidity and mortality has made these parenchyma preserving resections attractive (18,24,25). In this era of aggressive, multimodal treatment of primary and metastatic liver diseases, parenchyma preservation allows for multiple repeat hepatectomies if necessary, leading to better long-term outcomes (26–28).
To date, limited small single center studies have investigated the role of MI-RPS compared to MI-RH in the treatment of large or deeply located liver tumours in segments 6 and 7 (29,30). Hence, the role of MI-RAS and MI-RPS as parenchyma-preserving alternatives of MI-RH still remains unclear. The primary objective of the present study is to compare the short-term outcomes of MI-RAS and MI-RPS versus MI-RH in the treatment of right-sided liver tumours in a large international multi-center cohort.
Methods
This is an international multicenter post-hoc analysis of 1114 patients undergoing MI-RH, MI-RAS and MI-RPS at 21 centers between 2006–2019. All institutions obtained their respective approvals according to their local center’s requirements. This study was approved by the Singapore General Hospital Institution Review Board and the need for patient consent was waived. The anonymized data were collected in the individual centers. These were collected and analyzed centrally at the Singapore General Hospital.
In this study, MIS included patients who underwent pure laparoscopic, robotic-assisted laparoscopic surgery, hand-assisted and laparoscopic assisted cases. Patients undergoing donor hepatectomy for transplant, associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) and hepatectomy with bilio-enteric anastomoses were excluded.
Definitions
RH, RPS and RAS was defined according to the 2000 Brisbane classification as resection as resections of segments 5/6/7/8, 6/7 and 5/8 respectively (31). The diameter of the largest lesion was used in the cases of multiple tumours. Post-operative morbidity was recorded for up to 30 days or during the same hospitalization. This were considered major morbidity if graded 3/4/5 according to the Clavien-Dindo classification (32). Difficulty of resections was graded according to the Iwate score (33,34).
Statistical analysis
To minimize confounding and selection biases, and to ensure the robustness of our conclusions, analyses were carried out using two methodologies in the causal inference toolbox—coarsened exact matching and propensity-score matching.
One-to-one coarsened exact matching was used to identify approximately-exact matches between patients who were assigned to RAS/RPS or RH, and took into account all variables shown in Table 1 except for gender (35–38). Variables included in the matching process were age, ASA status, approach (laparoscopic, robotic, lap-assisted, hand-assisted), previous abdominal surgery, previous liver surgery, malignant pathology and type of malignancy (HCC, CRM or others), cirrhosis and Child-Pugh status, presence of portal hypertension, multifocality, multiple resections, concomitant surgeries excluding cholecystectomy, tumour size, and Iwate difficulty grade. Continuous variables were coarsened using an automatic binning algorithm based on Sturge’s rule.
Table 1.
Comparison Between Baseline Clinicopathological Characteristics of Minimally Invasive Right Anterior and Right Posterior Sectionectomy vs Minimally Invasive Right Hemihepatectomy
| Characteristic | Total n = 1100 | Unmatched cohort | 1:1 Propensity-matched cohort | 1:1 Coarsened-exact matched cohort | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| MI-RA/RPS n = 468 | MI-RH n = 632 | p Value | MI-RA/RPS n = 280 | MI-RH n = 280 | p Value | MI-RA/RPS n = 188 | MI-RH n = 188 | p Value | ||
| Age, y, median (IQR) | 61 (53–70) | 61 (53–70) | 62 (53–70) | 0.432 | 61 (52–70) | 61 (53–68) | 0.904 | 60.5 (52–69) | 61 (52.5–68) | 0.696 |
| Male sex, n (%) | 728/1099 (66.2) | 308/467 (66.0) | 420/632 (66.5) | 0.862 | 186/280 (66.4) | 191/280 (68.2) | 0.616 | 134/188 (71.3) | 122/188 (64.9) | 0.453 |
| ASA score, n/N (%) | 0.760 | 0.462 | 1.000 | |||||||
| I | 154/1097 (14.0) | 64/466 (13.7) | 90/631 (14.3) | 41/279 (14.7) | 39/280 (13.9) | 18/188 (9.6) | 18/188 (9.6) | |||
| II | 650/1097 (59.3) | 281/466 (60.3) | 369/631 (58.5) | 174/279 (62.4) | 164/280 (58.6) | 128/188 (68.1) | 128/188 (68.1) | |||
| III | 290/1097 (26.4) | 119/466 (25.5) | 171/631 (27.1) | 64/279 (22.9) | 77/280 (27.5) | 42/188 (22.3) | 42/188 (22.3) | |||
| IV | 3/1097 (0.3) | 2/466 (0.4) | 1/631 (0.2) | 0/279 (0.0) | 0/280 (0.0) | - | - | |||
| Approach, n/N (%) | 0.693 | 1.000 | 1.000 | |||||||
| Lap | 759/1100 (69.0) | 325/468 (69.4) | 434/632 (68.7) | 201/280 (71.8) | 201/280 (71.8) | 138/188 (73.4) | 138/188 (73.4) | |||
| Robotic | 283/1100 (25.7) | 120/468 (25.6) | 163/632 (25.8) | 76/280 (27.1) | 76/280 (27.1) | 48/188 (25.5) | 48/188 (25.5) | |||
| Hand-assisted | 11/1100 (1.0) | 6/468 (1.3) | 5/632 (0.8) | 0/280 (0.0) | 0/280 (0.0) | 0/188 (0.0) | 0/188 (0.0) | |||
| Lap-assisted | 47/1100 (4.3) | 17/468 (3.6) | 30/632 (4.7) | 3/280 (1.1) | 3/280 (1.1) | 2/188 (1.1) | 2/188 (1.1) | |||
| Previous abdominal operation, n/N (%) | 422/1100 (38.4) | 157/468 (33.5) | 265/632 (41.9) | 0.005* | 78/280 (27.9) | 78/280 (27.9) | 1.000 | 51/188 (27.1) | 51/188 (27.1) | 1.000 |
| Previous liver operation, n/N (%) | 78/1100 (7.1) | 19/468 (4.1) | 59/632 (9.3) | 0.001* | 7/280 (2.5) | 7/280 (2.5) | 1.000 | 6/188 (3.2) | 6/188 (3.2) | 1.000 |
| RAS, n/N (%) | 373/468 (79.7) | 373/468 (79.7) | NA | NA | 226/280 (80.7) | NA | NA | 152/188 (80.9) | NA | NA |
| RPS, n/N (%) | 95/468 (20.3) | 95/468 (20.3) | NA | NA | 54/280 (19.3) | NA | NA | 36/188 (19.1) | NA | NA |
| Malignant pathology, n/N (%) | 980/1100 (89.1) | 421/468 (90.0) | 559/632 (88.4) | 0.428 | 244/280 (87.1) | 247/280 (88.2) | 0.706 | 170/188 (90.4) | 170/188 (90.4) | 1.000 |
| Pathology type, n/N (%) | <0.001 * | 1.000 | 1.000 | |||||||
| HCC | 507/1100 (46.1) | 260/468 (55.6) | 247/632 (39.1) | 152/280 (54.3) | 152/280 (54.3) | 104/188 (55.3) | 104/188 (55.3) | |||
| CRM | 335/1100 (30.5) | 115/468 (24.6) | 220/632 (34.8) | 66/280 (23.6) | 66/280 (23.6) | 51/188 (27.1) | 51/188 (27.1) | |||
| Other | 258/1100 (23.5) | 93/468 (19.9) | 165/632 (26.1) | 62/280 (22.1) | 62/280 (22.1) | 33/188 (17.6) | 33/188 (17.6) | |||
| Cirrhosis, n/N (%) | 284/1100 (25.8) | 158/468 (33.8) | 126/632 (19.9) | <0.001 * | 80/280 (28.6) | 80/280 (28.6) | 1.000 | 48/188 (25.5) | 48/188 (25.5) | 1.000 |
| Childs Pugh score, n/N (%) | <0.001 * | 0.835 | 1.000 | |||||||
| No cirrhosis | 816/1100 (74.2) | 310/468 (66.2) | 506/632 (80.1) | 200/280 (71.4) | 200/280 (71.4) | 140/188 (74.5) | 140/188 (74.5) | |||
| A | 266/1100 (24.2) | 149/468 (31.8) | 117/632 (18.5) | 73/280 (26.1) | 75/280 (26.8) | 47/188 (25.0) | 47/188 (25.0) | |||
| B | 18/1100 (1.6) | 9/468 (1.9) | 9/632 (1.4) | 7/280 (2.5) | 5/280 (1.8) | 1/188 (0.5) | 1/188 (0.5) | |||
| Portal hypertension, n/N (%) | 51/1099 (4.6) | 28/468 (6.0) | 23/631 (3.6) | 0.068 | 13/280 (4.6) | 12/280 (4.3) | 0.832 | 4/188 (2.1) | 4/188 (2.1) | 1.000 |
| Tumor size, mm, median (IQR) | 40 (25–62) | 35 (26–50) | 45 (25–70) | <0.001 * | 40 (30–55) | 45 (30–65) | 0.213 | 40 (30–58) | 43 (30–60) | 0.619 |
| Multiple tumors, n/N (%) | 319/1100 (29.0) | 103/468 (22.0) | 216/632 (34.2) | <0.001 * | 69/280 (24.6) | 69/280 (24.6) | 1.000 | 48/188 (25.5) | 48/188 (25.5) | 1.000 |
| Multiple resections, n/N (%) | 67/1100 (6.1) | 29/468 (6.2) | 38/632 (6.0) | 0.900 | 13/280 (4.6) | 14/280 (5.0) | 0.828 | 5/188 (2.7) | 5/188 (2.7) | 1.000 |
| Concomitant operation non cholecystectomy, n/N (%) | 116/1100 (10.5) | 40/468 (8.5) | 76/632 (12.0) | 0.063 | 28/280 (10.0) | 21/280 (7.5) | 0.265 | 12/188 (6.4) | 12/188 (6.4) | 1.000 |
| Iwate score, n/N (%) | <0.001 * | 1.000 | 1.000 | |||||||
| Intermediate | 28/1100 (2.5) | 23/468 (4.9) | 5/632 (0.8) | 3/280 (1.1) | 3/280 (1.1) | 2/188 (1.1) | 2/188 (1.1) | |||
| High | 294/1100 (26.7) | 125/468 (26.7) | 169/632 (26.7) | 55/280 (19.6) | 55/280 (19.6) | 27/188 (14.4) | 27/188 (14.4) | |||
| Expert | 778/1100 (70.7) | 320/468 (68.4) | 458/632 (72.5) | 222/280 (79.3) | 222/280 (79.3) | 159/188 (84.6) | 159/188 (84.6) | |||
For categorical variables, denominators may differ from total numbers due to missing data.
Statistically significant.
CRM, colorectal metastasis; HCC, hepatocellular carcinoma; IQR, interquartile range; MI, minimally invasive; NA, not applicable; RAS, right anterior sectionectomy; RH, right hemihepatectomy; RPS, right posterior sectionectomy
Propensity-scores were developed using mixed-effects logistic regression modelling of all variables shown in Table 1 (39–46). Prior to propensity-score estimation, missing baseline covariates were addressed using multiple imputation (M=50) with chained equations with the following specifications: ordinal logistic regression for ordinal factor variables (e.g., ASA status), 5 k-nearest neighbors for continuous variables (e.g., tumour size), and augmented logistic regression for binary variables (e.g., portal hypertension). This model exhibited good discrimination (AUC=0.806, bias-corrected 95% CI: 0.777–0.835) and calibration (P=0.983 from Hosmer-Lemeshow test with 10 deciles) (Supplemental Digital Content 1–2). A random-effects term was used to to account for any between-center variation that may exist. Propensity-score matching was performed using 1:1 nearest-neighbour matching algorithm without replacement and a caliper of 0.25*standard deviations of the linear predictor (i.e. log odds of the propensity score), with exact matching for surgical approach, previous surgeries, cirrhosis, pathology type, multifocality, and Iwate difficulty grade. After matching, both groups were well-balanced for all variables, as shown in Table 1 and Supplemental Digital Content 3–5).
In the unmatched cohort, comparisons of patient characteristics and peri-operative outcomes between patients undergoing MI-RAS/MI-RPS or MI-RH were performed using Mann-Whitney U test and Pearson’s χ2 test for continuous and categorical variables respectively. Comparisons in the 1:1 propensity-score matched and coarsened-exact matched cohorts took into account the paired nature of the data; hence, Wilcoxon signed-rank test and McNemar’s χ2 test were used for continuous and binary variables. Statistical analyses were done in Stata version 16.0 (StataCorp), and nominal P<0.05 were considered to indicate statistical significance.
Results
One thousand one hundred cases met study criteria of whom 759 underwent laparoscopic, 283 robotic, 11 hand-assisted and 47 underwent laparoscopic-assisted (hybrid) surgery. There were 632 RH, 373 RPS and 95 RAS.
Major morbidity (> grade 2) occurred in 93/632 (14.7%) RH and 36/468 (7.7%) RPS/RAS. Thirteen cases had missing information on the type of major morbidity. The most common type of major surgical complications included bile leak/infected collection [MI-RH, 44/622 (7.1%) vs MI-RAS/MI-RPS, 17/465 (3.7%), p=0.015], liver failure/ascites [MI-RH, 14/622 (2.3%) vs MI-RAS/RPS, 3/465 (0.6%), p=0.046] and bleeding/hematoma [MI-RH, 5/622 (0.8%) vs MI-RAS/MI-RPS, 3/465 (0.6%), p=1.000].
Open conversion occurred in 99 cases (9.0%) and this was due to bleeding [20 (3.2%) and 15 (3.2%)], oncological reasons [6 (0.9%) and 4 (0.9%)], dense adhesions [9 (1.4%) and 2 (0.4%)] and other reasons [29 (4.6%) and 14 (3.0%)] for MI-RH and MI-RAS/MI-RPS, respectively.
Comparison between MI-RAS/MI-RPS and MI-RH in the entire unmatched cohort
Baseline characteristics are summarized in Table 1. The proportion of patients with previous abdominal surgery and previous liver surgery was higher in the MI-RH group (p = 0.005 and p < 0.001 respectively). The proportion of patients treated for HCC was significantly higher in the MI-RAS/MI-RPS group (p < 0.001), as well as the prevalence of cirrhosis (p < 0.001). Tumour size was larger in the MI-RH group (p < 0.001). Perioperative outcomes are summarized in Table 2. Median blood loss was higher in the MI-RAS/MI-RPS group (p < 0.001), as well as the rate of major hemorrhage (blood loss > 500ml) (p < 0.001). The need for intraoperative blood transfusion was higher in the MI-RAS/MI-RPS group (p = 0.017). The Pringle maneuver was used more frequently and Pringle duration was longer in the MI-RAS/MI-RPS group (p < 0.001). Postoperative morbidity was higher in the MI-RH group (p < 0.001), with a higher proportion of major morbidity (Clavien-Dindo grade 2 or higher). The need for reoperation was higher in the MI-RH group (p = 0.004). In patients treated for malignancy, the proportion of close/involved margins was higher in the MI-RAS/MI-RPS group (p < 0.001).
Table 2.
Comparison Between Perioperative Outcomes of Minimally Invasive Right Anterior and Right Posterior Sectionectomy vs Minimally Invasive Right Hemihepatectomy
| Outcomes | Total n = 1100 | Entire unmatched cohort | 1:1 Propensity matched cohort | 1:1 Coarsened-exact matched cohort | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| MI-RA/RPS n = 468 | MI-RH n = 632 | p Value | MI-RA/RPS n = 280 | MI-RH n = 280 | p Value* | MI-RA/RPS n = 188 | MI-RH n = 188 | p Value* | ||
| Operating time, min, median (IQR) | 310 (240–410) | 305 (230–390) | 310 (244–417) | 0.708 | 307 (237–395) | 300 (240–413) | 0.866 | 300 (227–407) | 310 (240–432) | 0.536 |
| Blood loss, mL, median (IQR) | 300 (200–600) | 400 (200–750) | 300 (200–500) | 0.001* | 400 (200–750) | 300 (150–500) | 0.022* | 400 (200–850) | 300 (120–500) | 0.001* |
| Blood loss (categories), n/N (%) | <0.001* | 0.015* | <0.001 * | |||||||
| <500 mL | 666/1045 (63.7) | 249/438 (56.8) | 417/607 (68.7) | 156/269 (58.0) | 183/270 (67.8) | 97/179 (54.2) | 131/181 (72.4) | |||
| ≥500 mL | 379/1045 (36.3) | 189/438 (43.2) | 190/607 (31.3) | 113/269 (42.0) | 87/270 (32.2) | 82/179 (45.8) | 50/181 (27.6) | |||
| Intraoperative blood transfusion, n/N (%) | 169/1100 (15.4) | 86/468 (18.4) | 83/632 (13.1) | 0.017* | 55/280 (19.6) | 30/280 (10.7) | 0.004* | 39/188 (20.7) | 23/188 (12.2) | 0.023* |
| Pringle maneuver applied, n/N (%) | 521/1084 (48.1) | 276/466 (59.2) | 245/618 (39.6) | <0.001* | 179/278 (64.4) | 102/277 (36.8) | <0.001 * | 114/187 (61.0) | 67/187 (35.8) | <0.001 * |
| Pringle duration when applied, min, median (IQR) | 40 (21–60) | 44 (29–68) | 35 (16–55) | <0.001* | 45 (30–70) | 40 (20–55) | 0.279 | 45 (30–75) | 40 (20–55) | 0.276 |
| Open conversion, n/N (%) | 99/1100 (9.0) | 35/468 (7.5) | 64/632 (10.1) | 0.129 | 22/280 (7.9) | 31/280 (11.1) | 0.191 | 11/188 (5.9) | 21/188 (11.2) | 0.110 |
| Postoperative stay, d, | ||||||||||
| Median (IQR) | 7 (5–10) | 7 (5–9) | 7 (6–11) | <0.001* | 7 (5–9) | 7 (6–10) | 0.025* | 6 (5–8) | 7 (6–10) | 0.002* |
| Mean ± SD | - | 8.1 ± 6.7 | 9.8 ± 7.9 | <0.001*† | 8.1 ± 6.1 | 9.3 ± 7.0 | 0.027*† | 8.0 ± 6.7 | 9.4 ± 7.5 | 0.009*† |
| 30-d readmission, n/N (%) | 54/1100 (4.9) | 16/468 (3.4) | 38/632 (6.0) | 0.049* | 8/280 (2.9) | 12/280 (4.3) | 0.371 | 5/188 (2.7) | 6/188 (3.2) | 0.763 |
| Postoperative morbidity, n/N (%) | 336/1100 (30.5) | 108/468 (23.1) | 228/632 (36.1) | <0.001* | 63/280 (22.5) | 86/280 (30.7) | 0.027* | 37/188 (19.7) | 56/188 (29.8) | 0.021* |
| Major morbidity (Clavien-Dindo grade> 2), n/N (%) | 129/1100 (11.7) | 36/468 (7.7) | 93/632 (14.7) | <0.001* | 20/280 (7.1) | 40/280 (14.3) | 0.007* | 14/188 (7.4) | 22/188 (11.7) | 0.139 |
| Reoperation, n/N (%) | 30/1100 (2.7) | 5/468 (1.1) | 25/632 (4.0) | 0.004* | 4/280 (1.4) | 13/280 (4.6) | 0.029* | 3/188 (1.6) | 10/188 (5.3) | 0.028* |
| 30-d mortality, n/N (%) | 12/1100 (1.1) | 2/468 (0.4) | 10/632 (1.6) | 0.068 | 2/280 (0.7) | 2/280 (0.7) | 1.000 | 2/188 (1.1) | 1/188 (0.5) | 0.571 |
| In-hospital mortality, n/N (%) | 14/1100 (1.3) | 5/468 (1.1) | 9/632 (1.4) | 0.603 | 3/280 (1.1) | 2/280 (0.7) | 0.657 | 3/188 (1.6) | 1/188 (0.5) | 0.341 |
| 90-d mortality, n/N (%) | 24/1100 (2.2) | 8/468 (1.7) | 16/632 (2.5) | 0.356 | 4/280 (1.4) | 4/280 (1.4) | 1.000 | 4/188 (2.1) | 3/188 (1.6) | 0.706 |
| Close/involved margins (≤1 mm) for malignancy, n/N (%) | 127/978 (13.0) | 75/421 (17.8) | 52/557 (9.3) | <0.001* | 57/244 (23.4) | 22/247 (8.9) | <0.001 * | 40/170 (23.5) | 14/170 (8.2) | <0.001 * |
For categorical variables, denominators may differ from total numbers due to missing data
Statistically significant
p Values additionally obtained (as a sensitivity analysis) from mixed-effects negative binomial regression with robust variance, which treats length of stay as a count response, whereby a random-effects term was used to account for the paired data structure. The marginal model was used in the full (unmatched) cohort. The incidence rate ratios in the full cohort, propensity score-matched cohort, and coarsened-exact matched cohorts were 0.83 (95% CI 0.75 to 0.91), 0.87 (95% CI 0.77 to 0.98), and 0.85 (95% CI 0.75 to 0.96) respectively, indicating a shorter postoperative stay in the RAS/RPS arm compared with the RH arm.
IQR, interquartile range; MI, minimally invasive; NA, not applicable; RAS, right anterior sectionectomy; RH, right hemihepatectomy; RPS, right posterior sectionectomy
Comparison between MI-RAS/MI-RPS and MI-RH in the matched cohort
After PSM, there were no differences in baseline characteristics (Table 1). Median blood loss and major hemorrhage rate remained higher in the MI-RAS/MI-RPS group, as well as the need for blood transfusion. The Pringle maneuver was applied more frequently in the MI-RAS/MI-RPS group (p < 0.001), yet there was no longer a significant difference in duration of the Pringle maneuver. Postoperative morbidity remained higher in the MI-RH group, with a higher proportion of major morbidity. Reoperations occurred more frequently in the MI-RH group. The rate of close/involved margins remained significantly higher in the MI-RAS/MI-RPS group (p < 0.001). The other perioperative outcomes after both propensity score and coarsened-exact matched testing remained similar (Table 2).
Comparison between MI-RAS and MI-RPS
Comparison was performed between MI-RAS and MI-RPS using 1:3 PSM (66 MI-RAS vs 198 MI-RPS) (Supplemental Digital Content 6 and 7). There was no significant difference between the perioperative outcomes of MI-RAS and MI-RPS after PSM.
Comparison between MI-RAS/MI-RPS and MI-RH in the subset of CRLM and HCC
These results are summarized in Supplemental Digital Content 8 and 9.
In the subset of patients with HCC (165 vs 165), MI-RAS/RPS was associated with significantly increased blood loss, blood transfusion rate, application of Pringles maneuver and close/ involved margin rates. In the subset of patients with CRLM (97 vs 97), MI-RAS/RPS was associated with significantly increased blood loss, application of Pringles maneuver, close/involved margin rates, shorter hospital stay, decreased morbidity rate and decreasd readmission rate.
Discussion
In this multicenter analysis, the perioperative outcomes of MI-RAS/MI-RPS are compared to those of MI-RH and the advantages and disadvantages of both procedures are identified. Several pioneers have overcome the learning curve for laparoscopic major hepatectomies and have introduced these procedures as standard of care, despite the technical difficulties related to these procedures (1,2,8,15–17, 47). MI-RAS/MI-RPS are uniformly considered technically more demanding than MI-RH (14,48,49) due to difficult access to the portal pedicle necessitating intra-operative ultrasound (IOUS), limited visibility and a larger parenchyma transection area, theoretically leading to higher rates of bleeding and bile leak (23). However, these procedures have also been reported to be safe and feasible when performed in expert centers (19–22).
As MI-RH has become a standard procedure, expected morbidity and mortality is low and these procedures might be preferred. On the other hand, the preservation of functional liver parenchyma is important as well, as this has been shown to be an independent predictor of decreased overall and liver-specific morbidity and mortality (18,24,25). Furthermore, the preservation of liver parenchyma allows for multiple repeat hepatectomies, which is occurring more frequently in this era of aggressive multimodal treatment, which in turn leads to better long-term outcomes (26–28).
Considering these factors, controversy remains about the optimal procedure for deeply located or large right sided liver lesions requiring major liver resections. Only a few studies have reported the comparison of MI-RH and MI-RPS. A retrospective study by Portigliotti et al. in patients with colorectal liver metastases (CRLM) in the posterosuperior segments found significantly lower postoperative morbidity in the laparoscopic RPS group, without comprising the rate of clear surgical margins or long-term survival (29). Rhu et al investigated the outcomes of laparoscopic RPS and RH for hepatocellular carcinoma (HCC) in the posterosuperior segments (30). This analysis found similar postoperative and oncological outcomes in both groups. However, both these single center studies were severely limited by the small sample size.
In this large, multicentre study, we performed both propensity score and coarsened-exact matching to minimize bias. We observed a significantly higher median blood loss and the rate of major bleeding in the MI-RAS/MI-RPS group, as well as the use of the Pringle maneuver over MI-RH. These inferior intraoperative outcomes clearly indicate that these 2 procedures are technically more challenging to perform compared to MI-RH. Nonetheless, the postoperative morbidity rate was significantly lower in the MI-RAS/MI-RPS group, with a lower incidence of major morbidity and lower reoperation rates. These results confirm the importance of a parenchyma-sparing approach when possible, thus decreasing postoperative morbidity and mortality. Nonetheless, an important disadvantage of RPS and RAS was the higher rate of close or involved resections margins. This observation is not surprising as the large wide parenchymal transaction areas associated with both RPS and RAS can be difficult to navigate resulting in higher rates of close margins (14,48). However, it is also plausible that the close or R1 margins observed in many of these patients may be intentional in order for the need to preserve liver parenchyma. Unfortunately. due to the nature of this study, no data was available on the long-term oncological follow-up of these patients. It is important to note that, margin involvement remains an important predictor of long-term survival after liver resection for malignancies (50,51, 39).
Notable in this study, all pathology types were included in the analysis. Hepatocellular carcinoma (HCC) was most common pathology, followed by colorectal liver metastases (CRLM). Subgroup analyses was performed for HCC and CRLM and summarized in Supplemental Digital Content 6–9. In general, our analyses demonstrated the same general trend in the results in these 2 subgroup analyses compared to the overall cohort. Some outcomes were not statistically significant possibly due to Type 2 errors due to the smaller sample size in each subgroup. These findings were concordant with findings from previous studies that these results can most probably be extrapolated to both subgroups (29,30).
Several factors play a major role in selecting the appropriate surgical procedure for a patient. One of the most important factors remains the anatomical location of the tumour, including the proximity of major vasculature, as well as tumour size. The decision should be based firstly on the possibility to achieve a complete resection with free margins. Other factors that should be taken into account include the presence of liver disease such as steatosis or cirrhosis and the primary pathology type such as colorectal liver metastases versus hepatocellular carcinoma. Based on current literature, it has been suggested that the long-term oncological outcomes of colorectal liver metastases are less likely to be affected by close resection margins and a parenchymal preservation is preserved. On the other hand, anatomical resections with wide margins have a major impact on the oncological outcomes of hepatocellular carcinoma and a wider resection margin is preferred in this subset of patients when the remnant liver function is adequate. Parenchyma preservation is also especially important in patients that received systemic therapy before undergoing liver resection or those with a compromised liver function. In this study, a higher proportion of HCC rather than metastases was observed in the parenchyma-preserving RPS/RAS cohort compared to the RH group. This may be due to the need for parenchyma-preservation due to the compromised liver function in patients with primary liver malignancies who were more likely to have cirrhosis. Moreover, RPS/RAS are still considered anatomical resections.
Another important consideration is the potential need in future for patients to undergo a repeat hepatectomy. Currently, there is a myriad of evidence supporting the role of repeat hepatectomy especially for colorectal liver metastases which has resulted in a paradigm shift towards parenchyma sparing resections in the treatment of these malignancies (18,25–28).
Besides patients and tumour characteristics, the surgical team and other institution factors also play an important role. The experience of the team also influences the decisions made in selecting the correct procedure. With increasing uptake of laparoscopy, increasing number of surgeons have become familiar with laparoscopic major hepatectomies and are becoming proficient in technically more demanding procedures such as laparoscopic RPS and RAS (19–22).
The limitations of this study are mostly due to the study design. As it is a retrospective study, it has the accompanying limitations, including an inevitable potential for information bias and selection bias. As a multicentric analysis, it is impossible to determine the factors leading to the decision for a particular resection type. Importantly, in many of the RH cases, it may not have been possible to perform a more limited resection such as RAS/RPS. However, we performed PSM and CEM in an attempt to minimize selection bias and to create comparable cohorts. Furthermore, this study included multiple centres involving multiple surgeons with a differing range of experience in minimally invasive liver surgery and who adopted different surgical techniques and equipment for inflow control and parenchymal transection. Finally, as this study focussed only on short term perioperative outcomes, the long-term oncological outcome was not available. Nonetheless, this study represents the largest series comparing MI-RH and MI-RAS/MI-RPS to date. While a prospective randomized controlled trial would be ideal, this would be difficult to achieve given the propensity for most experienced surgeons to favor one modality over the other.
Conclusion
This analysis showed the advantages and limitations MI-RAS/RPS compared to MI-RH. Although MI-RAS/MI-RPS were technically more demanding as evidenced by the inferior intraoperative outcomes, they offer a valuable alternative to MI-RH in patients with right-sided liver lesions. Despite a higher median blood loss and more major hemorrhage, postoperative morbidity and mortality were lower, likely due the preservation of functional liver parenchyma. However, the higher rate of involved or close resection margins observed in the MI-RAS/MI-RPS group deserves further investigation as this has potential impact on the long-term prognosis of selected patients with malignant tumours. The present findings should guide surgeons in selecting the appropriate procedure for the individual patient, based on patient, tumour type and surgeon characteristics.
Supplementary Material
Supplemental Digital Content 1. Discrimination of propensity score (PS) model.
Supplemental Digital Content 3. Propensity score (PS) distribution before matching. MI-RH, RH, right hemihepatectomy; MI-RAS/RPS, minimally invasive right anterior sectionectomy/right posterior sectionectomy.
Supplemental Digital Content 2. Calibration of propensity score (PS) model. RAS/RPS, right anterior sectionectomy/RPS, right posterior sectionectomy.
Supplemental Digital Content 4. Propensity score (PS) distribution after 1:1 matching. MI-RH, RH, right hemihepatectomy; MI-RAS/RPS, minimally invasive right anterior sectionectomy/right posterior sectionectomy.
Supplemental Digital Content 5. Love plot balance diagnostics. CEM, coarsened exact matching; CRLM, colorectal liver metastasis; HCC, hepatocellular carcinoma; HTN, hypertension; PSM, propensity score-matching.
Supplemental Digital Content 6. Comparison between baseline clinicopathological characteristics of minimally invasive right anterior sectionectomy vs right posterior sectionectomy
Supplemental Digital Content 7. Comparison between baseline perioperative outcomes of minimally invasive right anterior sectionectomy vs right posterior sectionectomy
Supplemental Digital Content 8. Comparison between baseline clinicopathological characteristics of minimally invasive right anterior/right posterior sectionectomy vs minimally invasive right hemihepatectomy within hepatocellular carcinoma and colorectal liver metastasis subgroups
Supplemental Digital Content 9. Comparison between perioperative outcomes of minimally invasive right anterior/right posterior sectionectomy vs minimally invasive right hemihepatectomy within hepatocellular carcinoma and colorectal liver metastasis subgroups
Disclosure Information:
Dr Goh received travel grants and honoraria from Transmedic, the local distributor for the Da Vinci Robot.
Disclosures outside the scope of this work:
Dr Goh received travel grants and honoraria from Johnson and Johnson and Olympus. Dr Marino is a paid consultant to CAVA Robotics, LLC. Dr Pratschke receives research grant funding from Intuitive Surgical Deutschland GmbH and consulting fees or non-financial support from Johnson & Johnson, Medtronic, AFS Medical, Astellas, CHG Meridian, Chiesi, Falk Foundation, La Fource Group, Merck, Neovii, NOGGO, pharma-consult Peterson, and Promedicis. Dr Schmelzle receives consulting fees Merck, Bayer, ERBE, Amgen, Johnson & Johnson, Takeda, Olympus, Medtronic, Intuitive. Dr Kingham is a paid consultant to Olympus Surgical.
Support:
This study was partially supported by the US National Cancer Institute Memorial Sloan Kettering Cancer Center Core Grant number P30 CA00878
Appendix
The International Robotic and Laparoscopic Liver Resection Study Group Investigators: Chung-Yip Chan (Department of Hepatopancreatobiliary and Transplant Surgery, Singapore General Hospital and National Cancer Centre Singapore); Mizelle D’Silva (Department of Surgery, Seoul National University Hospital Bundang, Seoul National University College of Medicine, Seoul, Korea); Henri Schotte (Department of Digestive and Hepatobiliary/Pancreatic Surgery, AZ Groeninge Hospital, Kortrijk, Belgium); Celine De Meyere (Department of Digestive and Hepatobiliary/Pancreatic Surgery, AZ Groeninge Hospital, Kortrijk, Belgium); Eric C. Lai (Department of Surgery, Pamela Youde Nethersole Eastern Hospital, Hong Kong SAR, China); Felix Krenzien (Department of Surgery, Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany); Moritz Schmelzle (Department of Surgery, Campus Charité Mitte and Campus Virchow-Klinikum, Charité-Universitätsmedizin, Corporate Member of Freie Universität Berlin, and Berlin Institute of Health, Berlin, Germany); Prashant Kadam (Department of Hepatopancreatobiliary and Liver Transplant Surgery, University Hospitals Birmingham NHS Foundation Trust, Birmingham, United Kingdom); Roberto Montalti (Department of Clinical Medicine and Surgery, Division of HPB, Minimally Invasive and Robotic Surgery, Federico II University Hospital Naples, Naples, Italy); Qu Liu (Faculty of Hepatopancreatobiliary Surgery, The First Medical Center of Chinese People’s Liberation Army (PLA) General Hospital, Beijing, China); Kit Fai Lee (Department of Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong SAR, China); Diana Salimgereeva (Department of Hepato-Pancreato-Biliary Surgery, Moscow Clinical Scientific Center, Moscow, Russia); Ruslan Alikhanov (Department of Hepato-Pancreato-Biliary Surgery, Moscow Clinical Scientific Center, Moscow, Russia); Lip Seng Lee (Hepatopancreatobiliary Unit, Department of Surgery, Changi General Hospital, Singapore); Mikel Gastaca (Hepatobiliary Surgery and Liver Transplantation Unit, Biocruces Bizkaia Health Research Institute, Cruces University Hospital, University of the Basque Country, Bilbao, Spain Hepatobiliary Surgery and Liver Transplantation Unit, Cruces); Jae Young Jang (Department of General Surgery, CHA Bundang Medical Center, CHA University School of Medicine, Seongnam, Korea).
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Associated Data
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Supplementary Materials
Supplemental Digital Content 1. Discrimination of propensity score (PS) model.
Supplemental Digital Content 3. Propensity score (PS) distribution before matching. MI-RH, RH, right hemihepatectomy; MI-RAS/RPS, minimally invasive right anterior sectionectomy/right posterior sectionectomy.
Supplemental Digital Content 2. Calibration of propensity score (PS) model. RAS/RPS, right anterior sectionectomy/RPS, right posterior sectionectomy.
Supplemental Digital Content 4. Propensity score (PS) distribution after 1:1 matching. MI-RH, RH, right hemihepatectomy; MI-RAS/RPS, minimally invasive right anterior sectionectomy/right posterior sectionectomy.
Supplemental Digital Content 5. Love plot balance diagnostics. CEM, coarsened exact matching; CRLM, colorectal liver metastasis; HCC, hepatocellular carcinoma; HTN, hypertension; PSM, propensity score-matching.
Supplemental Digital Content 6. Comparison between baseline clinicopathological characteristics of minimally invasive right anterior sectionectomy vs right posterior sectionectomy
Supplemental Digital Content 7. Comparison between baseline perioperative outcomes of minimally invasive right anterior sectionectomy vs right posterior sectionectomy
Supplemental Digital Content 8. Comparison between baseline clinicopathological characteristics of minimally invasive right anterior/right posterior sectionectomy vs minimally invasive right hemihepatectomy within hepatocellular carcinoma and colorectal liver metastasis subgroups
Supplemental Digital Content 9. Comparison between perioperative outcomes of minimally invasive right anterior/right posterior sectionectomy vs minimally invasive right hemihepatectomy within hepatocellular carcinoma and colorectal liver metastasis subgroups