Ultrasound-guided parenchima-sparing liver surgery: is it feasible by laparoscopy? Personal experience and narrative review of the literature

Introduction

Liver resection (LR) remains the gold standard of choice for curative treatment of both primary and secondary liver tumors. Much progress has been made particularly in the treatment of colorectal liver metastases (CLM), also thanks to the improvement of systemic therapies in the recent years (1-3).

Surgical strategy should aim to achieve oncological radicality while preserving enough liver parenchyma (4). Given these mainstreams, the future liver remnant (FLR) has represented a major limitation for expanding resectability particularly in case of multiple CLM. The two stage hepatectomy (TSH) (4,5) and ALPPS (associated liver partition and portal vein ligation for staged hepatectomy) (6) have been proposed to maximize liver regeneration and allow for major hepatectomies in these cases. The not negligible drop out of TSH and the relatively high mortality and morbidity of ALPPS (7) are the principal limits of these approaches.

In early 2000 the so-called radical but conservative policy was introduced based on the guidance of intraoperative ultrasound (IOUS) (8-10). This strategy aimed to challenge deeply located lesions in a conservative way with the aim of sparing the vascular-biliary architecture of the liver. The encouraging preliminary results (11), more recently confirmed on larger series (12,13) showing a similar risk of relapse between R0 resections and detachment of tumors from the vessels, known as R1vasc surgery, reinforced the effectiveness of the parenchymal sparing philosophy. Laparoscopic resective surgery has been shown to be safe and effective in the treatment of CLM, however the real feasibility of laparoscopic parenchyma-sparing hepatectomies (l-PSH) is still a matter of debate: mostly small series with a limited number of patients have been up to now published, mainly because of the technical difficulty of the procedure making the indication to the laparoscopic approach infrequent in bilobar multiple disease. Some advantage in terms of complications and cost-effectiveness have been demonstrated for l-PSH over open PSH in a RCT (14). Few studies to date has addressed whether l-PSH for multiple CRLMs leads to improved outcomes, better survival, or increased likelihood of repeat salvage hepatectomy compared with l-MH (15,16). The results of the published studies are reported and commented here together with personal experience relating to laparoscopic R1vasc surgery. We present the following article in accordance with the Narrative Review reporting checklist (available at https://dmr.amegroups.com/article/view/10.21037/dmr-22-12/rc).

Methods

A review of the literature was performed on September 30th, 2021 by searching Medline/PubMed using the terms “Laparoscopic liver resection” and “Parenchymal sparing hepatectomy” from January, 1st 2000 through September, 30th 2021. The titles and abstracts of all pieces of literature were screened for relevance. The research included clinical trials, randomized controlled trials, reviews, systematic reviews and meta-analysis. Books and documents, case reports, letters and commentary articles were excluded. Only publications in English were considered. The search among the references of the articles that were retrieved was also used. Among the articles retrieved, only those focused on l-PSH for CLM and providing results about R1vasc resections were considered eligible for the review. Articles not including laparoscopic R1vasc resections or not providing informations about laparoscopic R1vasc resections were excluded. The detailed search strategy is presented in Table 1.

In our personal case series, among a total of 81 laparoscopic liver resections for CLM performed between January 2015 and September 2021, 8 cases met the review criteria mentioned above. Surgical information of these patients are summarized in Table 2.

Surgical technique

The preferred approach is with the patient placed in supine position with the legs split and the surgeon standing between the legs. For tumors located in the right postero-lateral segments, a pillow can be placed behind the patient›s back and the bed can be turned sideways.

Intraoperative ultrasound (IOUS) is performed with two main purposes: stage the disease (identification of the target lesions and exclude preoperatively undetected additional lesions) and guide the resection. Laparoscopic and also robotic multifrequency probes (Figure 1) can be used, which today provide high quality images and allow the use of color-flow modalities and ultrasound contrast medium.

Figure 1 4-Way Laparoscopic transducer (BK Medical, Peabody, MA, USA) angled for transvers scan of the liver (A); the convex array combined with the high frequency of ultrasound enables high resolution images with panoramic vision (C). Robotic transducer (Hitachi Aloka Medical Ltd., Tokyo, Japan) grasped with a laparoscopic forceps (B) showing a small metastasis in segment 8 with very detailed image resolution (D).

For all resections in the right postero-lateral segments, the right hemiliver must be mobilized sufficiently to allow reaching the target lesion and obtaining a flat resection surface. In case of segment 8 resections, also for deeply located tumors (Figures 2,3), extensive mobilization of the right hemiliver can be avoided. Once the liver mobilization is completed, margins of resections are marked on the liver surface under guidance of IOUS. The IOUS-guided parenchyma-sparing approach has been sistematically described (8), the same criteria apply to laparoscopic surgery: whenever CLM are in contact with major intrahepatic vessels, vascular detachment can be performed if no signs of infiltration are evident at laparoscopic ultrasound (LUS).

Figure 2 CLM located in segment 4 superior between the MHV and LHV near to their caval confluence; (A) CT scan; (B,C) intraoperative ultrasound; (D) laparoscopic ultrasound-guided R1vasc resection of part of segments 2, 4 superior and 8 with exposure of LHV and MHV. MHV, middle hepatic vein; LHV, left hepatic vein; RHV, right hepatic vein; CLM, colorectal liver metastases.

Figure 3 CT scan showing a CLM located in segment 8 between the MHV and RHV near to their caval confluence and additional FL in segment 8 dorsal (A); laparoscopic ultrasoundguided R1vasc resection of part of segment 8 with exposure of MHV (taped on yellow vessel loop) and RHV (B). MHV, middle hepatic vein; IVC, inferior vena cava; RHV, right hepatic vein; FL, focal lesion; CT, computed tomography; CLM, colorectal liver metastases.

Parenchymal transection can be performed using a sealing device in combination with an ultrasonic surgical aspirator, which is particularly useful, in addition to blunt dissection, also to expose the vessels and detach them from the tumor (Figure 4).

Figure 4 Photographic sequence showing the detachment of a CLM from the left (C,D) and middle (E,F) hepatic veins. The dissection starts from the medial side (A), exposing the peripheral branches of the left hepatic vein (B) which are followed up to the main trunk. CLM, colorectal liver metastases.

Discussion

Liver resection remains the only treatment for patients with CLM, offering a relatively favorable 5-year overall survival (17), nowadays further improved by the effective association with systemic therapies.

Empowering liver regeneration has been considered the most suitable path to address successfully both surgical radicality and safety in case of extensive neoplastic involvement of the liver, particularly in complex conditions such as multiple bilobar CLM. Following this philosophy the TSH, a temporary debulking surgery splitting into two operations the organ clearance with or without portal vein embolization (PVE), and ALPPS have been introduced (4-6). Liver venous deprivation (LVD) and Radiological Simultaneous Portohepatic Vein Embolization (RASPE) followed by major hepatectomy are the latest techniques aiming to enhance liver regeneration (18,19). All these solutions, boosting the FLR, are conceived for the sacrifice of major vessels, which reduces the chance of redo surgery in case of recurrence compared to the parenchyma sparing approach. Conversely, the philosophy of parenchymal sparing hepatectomies (PSH), avoiding major vessel amputation, increase the surgical salvageability in case of relapses (20,21), resulting in lower rate of surgical mortality without change in disease-specific survival or liver recurrence (22). Indeed, it may be logical that the highest possible integrity of the liver anatomy can offer more technical solutions rather than an “amputated” organ.

Among the predictors of survival after resection, the state of resection margins remains a measure of the oncological adequacy of surgery, still targeted to R0 resections. Furthermore, oncologically suitable tumor-free margin width has progressively reduced from 1-cm to 1-mm (23-26), strengthening the rationale for PSH.

The detachment of colorectal metastases from the vessels, known as R1vasc surgery, also has an anatomical rationale. Major intrahepatic Glissonean pedicles (GP) and hepatic veins (HV) can be considered a kind of barrier separating totally distinct parts of the liver, and they are further separated from the parenchyma not only by the Glissonean sheath and the vascular wall, but also by the Leannec capsule as well as the inferior vena cava itself (27).

In 2008, de Haas et al. reported similar overall survivals for patients undergoing R0 and R1 resections, explaining those findings as the consequence of a more aggressive strategy combining chemotherapy and surgery (28). Subsequently other papers have overcome the paradigm according to which the impossibility of obtaining healthy margins should be a contraindication to surgery (29-32).

More recently, an international survey pointed out that tumor exposure is widely accepted by hepatobiliary surgeons as an alternative approach to non-resection (33) and Adam et al. have shown that R2 surgery can also be proposed in selected cases (34).

As previously mentioned, the parenchyma sparing approach was pushed for multiple bilobar CLM (22,35), commonly resected by an open approach. As for the HCC, the R1vasc policy was adopted according to imaging findings: after an initial encouraging experience (11), further validations on large series with long-term follow-up were subsequently published, showing similar results for R1vasc and R0 resections in term of long-term local control and outcome concerning both the general series (12) and also the subsetting of tumors in contact with major hepatic veins close to the caval confluence (13).

The realization of laparoscopic R1 vascular resection is a demanding procedure, requiring advanced minimally invasive surgical skills, such as the capability to manage large vessels bleeding, in addition to a thorough knowledge of liver anatomy, preoperative imaging and 3D-reconstruction, and a solid experience in intraoperative ultrasound. PSH for deeply located tumors in difficult-to-access areas sometimes requires intricate curved transection planes, which are technically more challenging in the laparoscopic approach in comparison with MH consisting of a single and straight transection plane (36,37).

For all the aforementioned reasons, l-MH (mainly right or left hepatectomy), which extensively sacrifices non-tumorous parenchyma beyond what is required to achieve tumor clearance, is often preferred when a laparoscopic approach is chosen. The technique in fact requires a long laparoscopic learning curve, which could make ineffective most of the advantages of laparoscopy, due to the extension of already long operating times, intraoperative complications and high risk of conversion. Nevertheless, the laparoscopic approach has managed to achieve comparable or improved short-term outcomes in liver surgery compared with the open approach, which has led to its increased implementation in the last 20 years (38-41); however, the role of laparoscopic parenchymal-sparing strategy in the treatment of multiple CRLMs has not been fully defined. L-PSH raises some concerns regarding technical feasibility and oncological outcome, mainly surgical margin status and liver recurrence rates (38). However, large experiences in that field reported similar survival and recurrence rate between patients with resection margins of ≥10 mm and <1 mm (42,43). Moreover, technical advancements and better understanding of hepatic anatomy allow to perform l-PSH even in difficult-to-access lesions (44), resulting in an increasingly frequent reduction in the rate of l-MH.

Some experiences on l-PSH have been published in recent years (14-16) showing favorable results both in terms of short- and long-term outcomes and cost-effectiveness.

The Oslo-CoMet trial (14) is the first published RCT aiming to compare l-PSH and open PSH. No significant differences about R0 and R1 surgical margin status were found between the two groups, and l-PSH showed a significantly lower morbidity rate and were cost-effective, with similar costs but higher QALYs than open liver resection. Nevertheless, no indications about the size, number or location of tumors was specified in the inclusion criteria; only the very limited average number of tumors (1.6 for open-PSH and 1.5 for l-PSH) is reported, suggesting that patient selection for surgery was less aggressive than can generally be done in open surgery. Furthermore, the endpoints did not include long-term oncological outcomes, which remain an open issue.

Two recent single-center retrospective studies compared l-PSH to l-MH (15) and l-PSH for bilobar CLM to laparoscopic liver resection for a single CRLM (16), both showing comparable rates of recurrence-free survival (RFS) and liver-specific RFS. Furthermore, as already reported in various open surgery experiences, l-PSH were associated with lower postoperative morbidity rates compared with l-MH, and l-PSH provided more frequent repeat salvage hepatectomy in case of liver recurrence. In both studies, R0 resections are largely more represented and the R1vasc rate is low, suggesting a large prevalence of patients without vascular contacts undergoing l-PSH. The low median number of resections for single procedure [1, range 1–6 (15) and 3, range 2–4 (16)] confirms the main limit of l-PSH due to the difficulty of the procedures which require prolonged operating times.

In conclusion, allowing for more tolerable large parenchymal removal with similar oncological results and greater chances of repeat liver resections in case of relapse, ultrasound-guided PSH should be the standard of care, even when using the laparoscopic approach, for the treatment of CLM. The limited experiences with the laparoscopic resection of multiple lesions, especially for bilobar disease, remains its main limitation. Based on our experience and published series, l-PSH can be considered indicated in cases where a limited number of resection areas (no more than 3) need to be performed, in order to avoid too long procedures burdened with a greater risk of complications.

Laparoscopic R1 vascular hepatectomy is a technical demanding technique, showing promising results in term of survival, but its evidence in literature remains scarce to draw firm conclusions. However, the technological improvements have played, and will continue to play in the future, a role in developing easier and safer procedures that will increasingly encourage the diffusion of the parenchymal sparing strategy in the modern laparoscopic era. Further studies with larger cohort of patients would be desirable for the future to confirm the oncologic adequacy and reproducibility of this technique.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer review: This article was commissioned by the Guest Editors (Edoardo Rosso and Santiago Azagra) for the series “Focus on Technical Advancement in Mini-invasive HPB Surgery” published in Digestive Medicine Research. The article has undergone external peer review.

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://dmr.amegroups.com/article/view/10.21037/dmr-22-12/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://dmr.amegroups.com/article/view/10.21037/dmr-22-12/coif). The series “Focus on Technical Advancement in Mini-invasive HPB 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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