Minimally invasive repeat liver resection for recurrent hepatocellular carcinoma: a systematic review of the current literature

Introduction

After its first application in the early ‘90s (1), laparoscopic liver surgery has had a progressively increasing diffusion worldwide and is now routinely applied in all hepato-biliary centers (2,3). The minimally invasive approach is considered a standard for left lateral sectionectomy and limited resection of anterolateral segments (4,5). Hepatocellular carcinoma (HCC) is the commonest indication, despite the potential risks related to the underlying liver cirrhosis (6,7). Most procedures are peripheral limited resections, but laparoscopic complex anatomical resections and major hepatectomies have been recently reported (8-12).

Available evidence demonstrated the feasibility, safety, and oncological adequacy of minimally invasive surgery for HCC (13-16). A laparoscopic approach leads to some generic advantages compared to a standard open one, i.e., less intraoperative blood loss, faster postoperative recovery, and reduced pain. In addition, specific benefits have been reported in cirrhotic patients: laparoscopic surgery is associated with a decreased risk of postoperative liver decompensation and ascites, most likely due to restriction of fluid administration, avoidance of long abdominal incisions with muscles divisions, collateral vessels preservation, and less respiratory impairment (17-19). A further advantage of a minimally invasive approach that should not be overlooked is that it prevents adhesions, thus facilitating salvage transplantation if needed (20,21).

Liver resection for HCC is affected by a high risk of recurrence, up to 80–90% (22-24). Patients with a recurrent tumor should be systematically re-evaluated by a multidisciplinary team to schedule, whenever possible, a new potentially curative treatment. A new hepatectomy can be considered in selected cases (24,25). The possibility to perform a repeat liver resection with a minimally invasive approach has been reported (26,27) but the dense adhesions and the altered anatomy could lead to high operative risks.

The present review aims to analyze the available series of patients undergoing a minimally invasive (laparoscopic or robotic) repeat liver resection for recurrent HCC, focusing on indications, technical and intraoperative peculiarities, short-term results, oncological adequacy, benefits in comparison with a standard open approach, and peculiarities in comparison with a first laparoscopic liver resection. We present the following article in accordance with the PRISMA reporting checklist (available at https://ls.amegroups.com/article/view/10.21037/ls-22-8/rc) (28).

Methods

Systematic literature search and selection criteria

The authors performed a systematic search of articles pertinent to minimally invasive (laparoscopic or robotic) repeat resection for recurrent HCC in PubMed and Embase databases. The following keywords were used: “hepatocellular carcinoma” or “HCC” or “hepatocarcinoma” combined with “laparoscopic” or “robotic” or “minimally invasive” combined with “liver resection” or “hepatectomy” combined with “repeat” or “recurrence” or “recurrent”. All articles published before December 1^st, 2021 (including online first papers) were considered. The list of articles was screened for duplicates; if present, these were removed. Titles and abstracts of the identified articles were reviewed. All eligible studies in English were retrieved, and their references were reviewed for potentially relevant publications. The following types of articles were retained for the analyses: randomized controlled trials, cohort studies, case-control studies, and case series. We used the following exclusion criteria: topic out of the scope of the review; articles concerning repeat liver resection for diseases other than HCC or mixed series including HCC patients without the possibility to extract specific data for HCC; studies on animals; simulation studies; case reports (one or two patients) and reviews; conference proceedings. The full text of the selected articles was retrieved. If the same group published multiple papers including the same population, only the most recent study was retained. Four authors (LC, CAPF, CP, CR) evaluated all manuscripts; in cases of discordance, a consensus was reached after discussion with two senior authors (LV and JG). The present review aimed to provide an overview of the current results of minimally invasive repeat hepatectomy for recurrent HCC. Accordingly, we decided not to formulate a specific Problem, Intervention, Comparison, Outcome (PICO). The present review was not registered in the PROSPERO database.

Data extraction and quality assessment

For each study we collected the following data: (I) name and institution of the authors, country, journal, and year of publication; (II) type of minimally invasive approach, i.e., laparoscopic, robotic, or both; (III) study design (e.g., retrospective, prospective, etc.); (IV) presence of a comparative cohort, its characteristics and matching technique for comparison; (V) sample size; (VI) patients and tumor characteristics; (VII) details of the surgical procedure and intraoperative data; (VIII) short- and long-term outcomes. All data were cross-checked by at least four authors. In studies using a propensity score matching, we analyzed the following data: the characteristics of the whole population undergoing a minimally invasive repeat resection; the characteristics of the population undergoing a minimally invasive repeat resection selected after matching; the characteristics of the matched population in the comparison group (open repeat resection or first minimally invasive resection). Two reviewers (LV and JG) independently assessed the quality of comparative studies using the Newcastle-Ottawa Scale (NOS), which was developed for non-randomized studies considered for systematic reviews and meta-analyses (29).

Results

After screening for duplicates and eligibility, 18 papers were included in the review (30-47). Figure 1 depicts the selection process. The study by Miyama et al. (47) is a subgroup analysis of the study by Morise et al. (40), i.e., the patients with tumors far from major vessels. Despite this, the paper was retained in the review because it provided original data about those patients, comparing laparoscopic and open repeat resections in the analyzed subgroup. Accordingly, only the data of the comparative analysis was considered for the review.

Figure 1 PRISMA flowchart of study selection. HCC, hepatocellular carcinoma.

All studies but one (35) were retrospective, and two were multicenter (40,44). The first series of laparoscopic repeat hepatectomy for HCC was published in 2009 by an Italian group (30), but most papers come from Far East centers (14/17, 82%). Fifteen studies included only laparoscopic resections, while two included both laparoscopic and robotic procedures (38,44).

The overall number of laparoscopic repeats hepatectomies for HCC was 1,143 with a mean of 67 patients per study. However, only five papers (including the two multicenter studies) collected more than 50 patients (39,40,44-46). Of note, 492 (43%) minimally invasive repeat resections were performed after a previous open hepatectomy.

All studies analyzed the intraoperative data and short-term outcomes, while only 10 considered the margin status and six the long-term results. The outcomes of laparoscopic repeat hepatectomy were compared with those of open repeat resection for recurrent HCC in 10 studies and with those of laparoscopic first resection for HCC in four. The quality of the comparative studies was evaluated according to the NOS and is summarized in Table S1.

The characteristics of the included studies are summarized in Table 1.

Indications & intraoperative data

Patients and tumor characteristics are detailed in Table 2. The proportion of cirrhotic patients varied among studies, ranging from 20% to 100%, but it was not detailed in 8 papers. Liver function was normal (Child-Pugh A class) in the vast majority of cases (80–100%). Only one author detailed the presence of portal hypertension (16 patients, 20%) (44).

Considering the characteristics of HCC, the median time interval from the first resection ranged from 14 to 47 months (range of values, 3–192 months). Most patients had solitary small recurrence: only 12 had multifocal HCC (32,33,37,38,43); the median tumor size exceeded 30 mm in one study (40 mm, range, 30–48 mm) (30), while it ranged between 12.5 and 25 mm in the remaining ones; only one paper reported the resection of HCC larger than 50 mm (46). Two studies did not detail the tumor size (39,42).

Considering the performed procedures, 33/1,065 patients (3%, missing data in 78 patients) underwent a major hepatectomy, 303/1,046 (29%, missing data in 97 patients) a resection involving posterosuperior segments (Segment 7, 8, 4s or 1), and 92/475 (19%, missing data in 668 patients) an anatomic resection (a left lateral sectionectomy in several cases). The Iwate difficulty score (48) was computed in three studies: Onoe et al. reported a median value of 5 (range, 1–9) (41); Kinoshita et al. classified the difficulty of resections as low in 31 cases, intermediate in 28, and difficult in one (39), while Takase in 29, 27, and two cases, respectively (45).

The median operative time ranged from 72.5 to 398 min and the median blood loss ranged from 50 to 200 mL. The conversion rate was detailed in all but one study (40): overall, 32 conversions occurred in 495 (6%) resections, including three conversions from laparoscopy to hand-assisted procedures. The conversion rate was 0% in 6 series and ranged from 7% to 15% in the remaining ten.

Performed procedures and intraoperative data are detailed in Table 3.

Short-term results

Only three patients (0.3%) had 90-day mortality, and they were all included in the multicenter international study (0.5% of the study). Overall, 121 postoperative complications, including 44 severe ones [according to Clavien-Dindo classification (49)], were reported. Focusing on series with at least 10 patients, the overall and severe morbidity rates ranged from 5% to 27% and from 0% to 9%, respectively. Five studies reported no severe morbidity (30,31,35,36,38). Liver failure was anecdotal (two patients) as well as hemorrhagic complications (one patient). Fourteen patients had ascites (/1,024, 1.4%), and 20 (/1,021, 2%) had a bile leak. The median hospital stay ranged from 3.5 to 10 days. The short-term results are summarized in Table 4.

Margin status and oncological outcome

Ten studies reported the margin status (30,32-38,44,45), but only five detailed both the surgical margin width and the proportion of patients with a 0-mm margin (32-35,44). The remaining five analyses only reported the R1 resection rate. The median surgical margin ranged from 3 to 5 mm. Only 7 out of 273 (2.6%) patients had a 0-mm margin, and eight out of ten series reported a 100% rate of R0 resection.

The long-term outcomes were detailed in six studies (31,33,35-37,40). Morise et al. reported a median overall survival (OS) of 10.0 years for the 648 analyzed patients; in the subgroup of patients selected by the propensity score matching (n=238), median OS and disease-free survival (DFS) were 12.6 and 1.8 years, respectively (40). Liu et al. reported the following data: in the 30 analyzed patients (median follow-up 35 months), the one-, three-, and five-year OS rates were 96.7%, 85.0%, and 74.4%, while the DFS rates were 78.3%, 57.4%, and 43.0%, respectively (37). Chan et al. reported three-year OS and DFS rates of 60.0% and 18.9%, respectively (11 patients) (33). The remaining studies only depicted the recurrence rate: one out of six patients in Hu et al. (31); one out of 8 in Goh et al. (36), and five out of 31 in Zhang et al. (35).

Comparison with repeat open resections

Ten studies compared the outcome of laparoscopic vs. open repeat resection (32,33,35,37,38,40,41,43,46,47). Seven adopted a propensity score matching (33,37,38,40,43,46,47). Of those, four studies compared very small cohorts of patients (20 to 31 repeat laparoscopic resections) (33,37,38,43). The remaining three analyzed a more adequate population: Morise et al. compared 238 pairs of patients (multicenter database) (40), Miyama et al. 115 pairs (subgroup analysis of Morise et al.) (47), and Chen et al. 57 pairs (46). Table 5 summarizes the results of all comparative analyses. We will comment only on the results of the matched series.

In comparison with open repeat resections, the operative time of laparoscopic repeat procedures was longer in two studies (38,40), similar in four (33,37,46,47), and shorter in one (43). The latter result was observed in the subgroup of patients with an HCC recurrence contralateral to the first tumor. Blood loss was lower in the laparoscopic group in all studies, with a significant difference in six (33,37,40,43,46,47). Five out of seven studies reported similar overall morbidity rates between the two groups (33,38,40,43,46). Liu et al. observed a reduced number of complications (7% vs. 30%) and bile leaks (3% vs. 10%) in the laparoscopic group in comparison with the open one (37). Miyama et al. (subgroup analysis of the series by Morise et al. focused on patients with tumors far from major vessels) reported a significantly lower rate of complications of grade >1 and severe complications in the laparoscopic group in comparison with the open one (9% vs. 18%, P=0.034 and 4% vs. 12%, P=0.031, respectively) (47). No further differences were evident in terms of severe morbidity, liver failure, and ascites rates. The laparoscopic approach was associated with a shorter hospital stay in five studies (37,38,43,46,47), but not in the largest series (Morise et al., mean hospital stay 10.4 vs. 9.6 days) (40). Chen et al. analyzed the inflammation-based markers (monocyte-to-lymphocyte ratio, neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, and systemic immune-inflammation index) and reported a lower value on postoperative day one in the laparoscopic group (46).

Considering long-term outcomes, six studies compared the two groups (33,35,37,38,40,47). Four papers analyzed OS rates and reported no differences between the laparoscopic and open groups (33,37,40,47). Five studies analyzed the DFS rates (33,35,37,38,40). Of those, four reported similar results between groups, while one (38) depicted a better DFS in the laparoscopic group (only the survival curves were provided, without data).

Comparison with laparoscopic first resection

Four studies compared the outcome of laparoscopic repeat resections and laparoscopic first resections for HCC (38,42,44,45). Only one adopted a propensity score matching (44). The three unmatched analyses included 20, 28, and 58 patients in the laparoscopic repeat hepatectomy group, respectively (38,42,45). The study with a propensity score matching compared 74 laparoscopic repeat hepatectomies with 222 laparoscopic first resections (matching 1:3) (44).

All studies reported no differences between groups in terms of blood loss, conversion rate, morbidity rate, and hospital stay. The two unmatched analyses observed a longer operative time in the repeat resection group (38,45). The results are summarized in Table 6.

Further comparisons

Three studies evaluated the impact of the first resection’s approach (open vs. laparoscopic) on the outcome of a laparoscopic repeat resection (30,32,37). All authors reported similar blood loss, conversion rate, and postoperative outcomes between groups. Liu et al. (21 open first resections vs. 9 laparoscopic first ones) reported similar operative time, despite reporting more severe adhesions [Grade 3 and 4, according to Becker classification (50)] in patients with initial open resection (37). On the contrary, Belli et al. (4 open first hepatectomies vs. 8 laparoscopic first ones) and Kanazawa et al. (15 vs. 5) reported longer operative time after an open first resection (117.5 vs. 60 min, P<0.001; 287 vs. 199 min, P=0.005) (30,32).

Two studies analyzed the outcomes of a laparoscopic repeat resection for a recurrent HCC ipsilateral vs. contralateral to the first HCC (35,43). Zhang et al. demonstrated that patients with a contralateral recurrence (n=18) have less blood loss (mean, 97.7 vs. 186.3 mL, P=0.012), a shorter operative time (112.4 vs. 159.4 min, P=0.034), and a shorter hospital stay (4.2 vs. 6.1 days, P=0.021) in comparison with patients having an ipsilateral recurrence (n=13) (35). Gon et al. reported that patients with a contralateral recurrence (n=15) have a shorter operative time than those with an ipsilateral recurrence (n=15, median 252 vs. 398 min, P=0.008), but similar blood loss and length of hospital stay (43).

Discussion

The present review demonstrated that a minimally invasive repeat liver resection for recurrent HCC is feasible and safe. Although few large series have been published, overall more than 1,000 cases have been reported with excellent results. The laparoscopic approach to repeat hepatectomies showed some advantages over the standard open approach, achieving results similar to the laparoscopic first resections. The available data suggests the oncological adequacy of such an approach, but these are preliminary evaluations requiring further confirmations.

After the first laparoscopic hepatectomy was performed about 30 years ago (1), the minimally invasive approach to liver surgery has had a progressive diffusion worldwide and is now applied to all types of resection, even the most complex ones (3,5,11,51). In selected patients, it has been proposed also for repeat hepatectomies (52). One of the first series was published by Belli et al. in 2009 and included twelve patients with recurrent HCC (30). In the subsequent years, few studies have been reported and these mainly collected patients with heterogeneous diagnoses (53-55). However, since 2019 the minimally invasive repeat hepatectomy for recurrent HCC has been the object of renewed interest. Over the last three years, ten papers (two multicenter analyses) collecting a large number of patients (n=1,022) have been published.

The present review highlighted that the patients undergoing a laparoscopic repeat resection have some specific characteristics, i.e., preserved liver function and small solitary HCC requiring peripheral limited resection, mainly of anterolateral segments, or left lateral sectionectomy. Very few major hepatectomies have been reported (n=33). Such data is not surprising. Even at first resection, cirrhotic patients are preferentially scheduled for minor hepatectomies in both laparoscopic and open series (18,22,56). Furthermore, repeat surgery for recurrent HCC is considered in highly selected patients, usually with a low tumor burden and easily resectable disease (24,25). We also outlined that anatomic resection, which is theoretically a standard for HCC (57,58), was performed in only one-fifth of patients. The tumor spread along the portal pedicles requires the removal of the whole tumor-bearing portal territory (sub-segmentectomy or mono-/multi-segmentectomy) (59,60). However, except for major hepatectomies or sectionectomies, the true boundaries of the portal territories are difficult to identify. Several techniques have been proposed in open surgery, but their laparoscopic application is still an issue (11,61,62). The low rate of anatomic resection in laparoscopic repeat surgery likely reflects such difficulties but could also have another explanation. Anatomic resection is probably unnecessary for superficial HCC with a small size (57,63), i.e., most patients included in the current review.

The feasibility of minimally invasive repeat resection was unequivocally demonstrated by the high number of reported procedures and the low conversion rate (6%), in line with the standard data of laparoscopic surgery (3). In some series, the median operative time was longer than laparoscopic first resections or open repeat hepatectomies, but this did not correspond to a higher blood loss (38,40,45). The latter was even lower than the open repeat resections in six studies (33,37,40,43,46,47). Of note, the operative time was increased especially in patients with a laparoscopic redo procedure after a first open resection and in those with a recurrence ipsilateral to the first HCC (30,32,35,43).

The available literature also proved an excellent safety of the laparoscopic repeat hepatectomies: the 90-day mortality rate across all series was below 0.5% and was nil in most studies; severe morbidity occurred in less than 10% of patients. Such positive results have been achieved thanks to the strict selection of candidates and the low complexity of procedures. Nevertheless, the complication rate remained low even in series including a higher proportion of anatomic resections or resections of posterosuperior segments. The current standardization of the laparoscopic technique in high-volume centers guarantees a persistent high safety profile even for complex procedures (8-12,51,64). Viganò et al. recently demonstrated that the hospital volume influences the outcome of the most difficult laparoscopic procedures, with high-volume centers achieving better outcomes than low-volume ones (65). In most comparative analyses, the overall and severe morbidity rates of minimally invasive repeat surgery were similar to those of open repeat hepatectomies and laparoscopic first resections, even after a propensity score matching of patients. However, two papers opened the way to a different perspective: they reported a lower rate of complications in the laparoscopic group (37,47). Miyama et al., who focused on easy resections (tumors far from vessels), even depicted a lower rate of severe morbidity (9% vs. 18%) (47). Such data further encourages the adoption of a minimally invasive approach.

The present review demonstrated that a laparoscopic approach maintains its advantages over a standard open approach, even when applied to repeat resections. First, in cirrhotic patients, a minimally invasive resection has been associated with a reduced risk of postoperative liver decompensation and ascites (17-19). In comparison with the standard laparotomies, laparoscopy leads to restriction of fluid administration and less respiratory impairment and spares the collateral vessels along the abdominal wall. The same beneficial impact was observed at repeat surgery: liver failure occurred only in two patients out of more than 1,000, and less than 2% had postoperative ascites. Second, the anatomy magnification during minimally invasive procedures allows a more accurate parenchymal dissection. In the analyzed series of laparoscopic repeat hepatectomies, median blood loss was low, only one hemorrhagic complication occurred, and bile leak rate was 2%. However, such favorable results have to be weighed with the complexity of the procedures. After propensity score matching, the beneficial impact of laparoscopy on blood loss (lower than open repeat resections) was confirmed, while the one on bile leak was not (similar between groups). Finally, the minimally invasive approach led to a shorter hospital stay, as widely demonstrated in the literature at first resection (13-16).

Considering the oncological efficacy of the laparoscopic repeat resections for HCC, we can only provide a preliminary evaluation. As observed for laparoscopic first resections of HCC patients (13,15,17,19), a minimally invasive approach guarantees adequate margin width, low R1 resection rate, and adequate survival rates, non-inferior to open surgery. Nevertheless, most studies reported incomplete data, precluding any critical review and dictating the need for further accurate analyses.

Some major limitations of the available studies have to be mentioned. First, most studies collected a low number of patients, reflecting the limited number of candidates even in high-volume centers. Accordingly, the reproducibility of the procedure outside the expert and referral centers remains unclear. Second, all series but three (two Italian studies and one multicenter study) have been collected in Eastern centers, limiting the tout court transferability of results to all centers. The web sources were not included in the review process but the authors exclude that any relevant series have been missed. Third, all evaluations concern laparoscopic resections. Few robotic procedures have been included in two papers (38,44), and no specific analyses are available. Fourth, the Iwate difficulty score was reported by only three studies and classified very few procedures as difficult (39,41,45). The systematic adoption of a standardized and easy-to-apply score that adequately stratifies procedures and predicts intra- and postoperative outcomes is needed. As proposed by Okamura et al. (66), a specific difficulty scoring system for minimally invasive repeat hepatectomies could be considered. Finally, as previously reported, the oncological outcomes remain to be elucidated.

In conclusion, a minimally invasive approach should be considered in candidates for a repeat liver resection for recurrent HCC. A laparoscopic repeat hepatectomy guarantees the same benefits of a laparoscopic first resection in terms of reduced risk of liver failure and ascites, lower blood loss, and shorter hospital stay. More robust data is needed to confirm the oncological adequacy of a minimally invasive approach to recurrent disease.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Roberto Santambrogio and Marco Antonio Zappa) for the series “Laparoscopic Hepato-Biliary Surgery” published in Laparoscopic Surgery. The article has undergone external peer review.

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://ls.amegroups.com/article/view/10.21037/ls-22-8/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://ls.amegroups.com/article/view/10.21037/ls-22-8/coif). The series “Laparoscopic Hepato-Biliary Surgery” was commissioned by the editorial office without any funding or sponsorship. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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