Minimally invasive surgery (MIS) has revolutionized many procedures in different surgical fields over the past three decades. However, the adoption of minimally invasive liver resection has been slow compared with the rate at which MIS approaches have been incorporated into luminal and other solid organ procedures (1–3). This slow adoption has persisted despite expanding indications and increasing experience in high volume centers (4).

Based on international data, primary liver cancer is the most common indication for laparoscopic liver resection (LLR), whereas metastatic disease may predominate as an indication in North America and Europe (5, 6). Of note, LLR is associated with a decrease in perioperative bleeding, faster mobilization, shorter hospital stays, and less morbidity, as well as being cost-effective (7–9). Furthermore, concerns on compromised short- and long-term oncological outcomes in LLR have been refuted by various studies (9–12).

For resection of colorectal liver metastases (CRLM), studies have shown that LLR results in superior perioperative outcomes and similar oncological outcomes (recurrence-free and overall survival) in selected patients compared to open liver resection (OLR) (9–12).

The Louisville consensus conference recommends laparoscopic liver resection for patients with a solitary lesion, 5 cm or less, located in the peripheral liver segments (13). However, in the Southampton guidelines (14) and after accumulated experience in laparoscopic liver surgery for colorectal liver metastases, the warnings and limitations were only for formal laparoscopic hemi-hepatectomy and for lesions in the postero-superior segments. These lesions (in segments 1, 4a, 7, and 8) have been considered especially challenging because of the limited surgical view and restricted handling of laparoscopic instruments (15, 16). However, recent progress in operative techniques, including the introduction of the transthoracic port placement, has reduced the difficulty of LLR for tumors in the posterosuperior liver (17).

Hand-assisted laparoscopic surgery (HALS) is defined as the placement of a hand port during laparoscopy. The main advantages of HALS are the possibility to control intraoperative bleeding via manual compression and the use of tactile sensation, to detect deeper intraparenchymal lesions, and provide better exposure of difficult tumor locations (13, 14, 18).

To date, there is no published comparison of the surgical and long-term results of HALS vs. OLR for CRLM in the postero-superior segments. The aim of this study was therefore to compare the perioperative and long-term outcomes of LLR (HALS) and OLR for CRLM in the postero-superior segments.

All consecutive patients who underwent either HALS or open resections with curative intent for CRLM located in posterior-superior liver segments (segments1, 4a, 7, and 8) between January 2008 and December 2018 were identified from prospectively maintained surgical databases at the Carmel and Rabin medical centers. Patients' data was collected by reviewing these electronic databases of both centers after receiving approval from their institutional review boards. Clinical data including demographic, perioperative and intraoperative variables, in addition to short- and long-term outcomes were collected retrospectively.

The indications for liver resection were determined during a weekly multidisciplinary meeting. Preoperatively the workup included blood tests, tumor markers, imaging modalities [computed tomography (CT), positron emission tomography CT (PET-CT) and magnetic resonance imaging (MRI)], and characterization of the liver metastases (number, location, size, and relation to intrahepatic vascular or biliary structures). All the patients were informed in detail about the procedure, including the risks and benefits, and written consent was obtained before surgery. All the HALS procedures were performed by the same surgical team under the direction of the same attending surgeon (R.H.). Open liver resection were performed by 3 HPB surgeons.

The findings of this study demonstrate that the laparoscopic approach is safe, feasible and preferable for resection of mCRC located in the postero-superior segments of the liver. This was shown by a significantly shorter hospital stay and lower complication rate in the laparoscopic group compared to the open surgery group. Liver metastases recurrence and 5-year survival were similar in both patient groups.

Surgical resection remains the only effective treatment for mCRC to the liver. In addition, in the last decade there has been a shift toward parenchymal-sparing surgery which has become the gold standard for the treatment of colorectal liver metastases. The advantages of this approach are in preserving healthy remnant liver parenchyma and maintaining the liver vasculature anatomy. Accordingly, multiple liver resections and repeated hepatectomies can be carried out if needed. Parenchymal-sparing surgery has subsequently decreased the rate of morbidity and mortality and repeated hepatectomies when needed are associated with improved long-term survival.

The three consensus guidelines [Louisville (13), Morioka (7) and Southampton (14)] on laparoscopic liver resections estimate that pure laparoscopic liver resection, HALS, and the hybrid technique appear to be equivalent and are just a matter of surgeon preference. It has also been suggested that the HALS technique may be used to manage intraoperative difficulties and act as a bridge from learning open procedures to laparoscopy surgeries.

Historically, LLR was advocated for liver lesions located in the anterolateral segments, while the open approach was preferred for posterosuperior lesions. With increasing experience, LLR of more challenging lesions in the postero-superior segments has become possible (20). However, in the Southampton 2018 guidelines there were warnings and limitations for formal laparoscopic hemi-hepatectomy and for lesions in the postero-superior segments (14). These warnings were because of concerns regarding the limited visualization of the posterior surface of the liver, the risks of bleeding since the postero-superior segments are adjacent to the major liver vasculature, and the difficulty to control bleeding.

In conventional open liver surgery for mCRC, large incisions are usually required. Whereas, the benefits of liver minimal-invasive surgery are mainly related to smaller incisions with less operative trauma, reduced levels of postoperative pain, and faster gain of functional recovery (20). These benefits are the main reason for shortening the time to resume the adjuvant chemotherapy.

In our experience, HALS has been used during the learning curve as a bridge to master the pure LLR. However, it has now been abandoned for minor hepatic resections while still being valuable for major resections and tumors located in the postero-superior segments. In addition, only after we gained experience in HALS-liver resections of “laparoscopic segments” and were comfortable with the technique, did we then begin to perform HALS-resections of mCRC in the postero-superior segments. The main advantages of HALS over LLS, especially in the parenchymal preserving resection of lesions in the poster-superior segments, are: (i) the faster mobilization of the liver; (ii) the better exposure of difficult metastases locations; (iii) the use of tactile sensation for the detection of subcapsular lesions or superficial small diminished lesions after neoadjuvant chemotherapy; (iv) the better identification of safe resection margins; and (v) the possibility to achieve faster hemostasis of intra-operative bleeding through manual compression. It is worth noting that in minimal invasive liver resections, a 6–8 cm incision is needed to retrieve the resected liver. In pure laparoscopy, a Pfannenstiel incision is made; whereas in HALS, a transverse incision in the upper right abdomen is required but the operative trauma remains significantly reduced compering to OLR. Indeed, Wabitsch et al. (21) reported no significant differences in HALS vs. LLR at operation time, postoperative complications, microscopic surgical margin involvement (R1) rate and general hospitalization time, but they did recommend the implementation of HALS before LLR in the postero-superior segments.

This study's findings showed that despite the technical difficulties of HALS-LLR for patients with postero-superior lesions, there were no significant differences compared to patients undergoing OLR in short-term outcomes, including global operative time and blood transfusion rates. However, there was a significant advantage of the HALS in terms of fewer total and major complications and shorter hospital stays. These results can be partly explained by the fact that LLR for posterosuperior segments were performed in our unit at a later stage of the implantation of the minimally invasive surgery (MIS) liver program. Notably, our findings are aligned with the results of a subgroup analysis of tumors in the postero-superior segments from the first randomized controlled trial, the OSLO-COMET, that compared the outcomes of laparoscopic and open parenchymal-sparing liver resections for mCRC (22). Our findings are also similar to the results of a meta-analysis of 11 studies to compare the outcomes of OLR vs. LLR for mCRC and primary liver tumors in the postero-superior segments (21). This meta-analysis found no group differences in the need for blood transfusions and mortality, but the LLR group had a lower risk of total and major complications and a shorter hospital stay compared to the OLR group. Several additional studies have also reported the advantage of LLR compared to open surgery in terms of lower rates of total and major complications (23–33).

One of the major concerns in MIS liver resection is oncological outcome, especially the achievement of adequate free surgical margins. We found that using the HALS combined with meticulous laparoscopic intraoperative ultrasonography did not compromise the early oncological outcomes, and the rate of R0 margin was not statistically different between the OLR and HALS groups. This is in line with the results reported in the OSLO-COMET study (22) and in a meta-analysis conducted by Hajibandeh et al. (34).

Notably, the safety and feasibility of the HALS did not compromise long-term outcomes. Furthermore, there were no significant differences between the OLR and LLR patient groups in their 3 and 5-year overall survival and in the rate of liver recurrence. This is again in line with the results reported in the OSLO-COMET study (22) and in the Hajibandeh et al. (34) meta-analysis.

There are a few limitations to the study. These include the retrospective data analysis and selection bias. In addition, all the LLR surgeries were performed by one hepatobiliary surgeon, while all the OLR operations were performed by three hepatobiliary surgeons. This creates some heterogenicity between the techniques employed for the parenchymal transections including the use of different devices.

HALS for CRLM in the postero-superior segments was associated with fewer total and major complications, a shorter hospital stay and similar oncological outcomes compared to open liver resection.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by Carmel Medical Canter and Rabin Medical Center. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements.

OA-Z, MS, NG, and RH contributed to conception and design of the study. OA-Z, MS, and YB organized the database. AM and NG performed the statistical analysis. OA-Z wrote the first draft of the manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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