From liver surgery to liver transplant surgery: new developments in autotransplantation

INTRODUCTION

Given the anatomical and physiological background of the human liver, performing hepatectomy while guaranteeing future liver remnant's (FLR) vasculature and sufficient functional volume are the current standards in practical hepatobiliary surgery [1▪▪,2▪,3]. Surgical safety and efficacy have been improved well in this century, and more techniques are being applied to utilize FLR both preoperatively and intraoperatively [4,5▪,6]. However, despite substantial technical improvements and conceptual revolutions in advanced liver surgery, there are still straitened circumstances that pose difficulties for in-vivo and/or in-situ surgery, especially when space-occupying lesions invade major vasculatures, including the hepato-caval confluence [7,8▪,9]. Radical resection is the best method to treat the vast majority of those conditions and to provide long-term survival. Unfortunately, not all patients are eligible for resection by such conventional techniques. Ex-vivo liver resection and autotransplantation (ELRA) applies mainly to those patients presenting with lesions in difficult anatomic locations, especially when involving major blood vessels. In these situations surgeons may encounter uncontrollable bleeding in situ, which impose prolonged vascular occlusion to avoid hemorrhagic damage and hemodynamic problems during liver surgery. Prolonged vascular occlusion may however cause severe ischemia-reperfusion injury. In addition, insufficient surgical exposure and limited operative space are factors that may make safe and successful in-situ liver resection difficult.

Conversely, ex-vivo hypothermic perfusion during ELRA provides voluntary and perfect surgical exposure as well as longer duration of ischemia time (up to several hours), conditions that are necessary to do a safe restoration of vascular structures at the bench-table. ELRA has been proved to be a superior technique, allowing to avoid posttransplant immunosuppression and reduce the pressure on the scarce organ donor pool, and therefore becomes an emerging and promising surgical technique [10]. 

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EARLY HISTORY OF EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

The concept and practice of organ ex-vivo surgery and autotransplantation started in 1963 with a renal autotransplantation done to resect a high ureteral injury [11]. In the 1980s, innovative liver transplantation techniques were introduced by Prof. H. Bismuth (Paris, France), Prof. R. Pichlmayr (Hannover, Germany) and others. These included reduced- size, split, and auxiliary liver transplantation, all done under ex-vivo hypothermic perfusing conditions [12▪,13▪,14▪,15,16]. Splitting the liver at bench provides an excellent view of the liver anatomy, a better structural exposure and evidently a bloodless hepatectomy. These techniques correspond in fact to the fundamentals of ex-vivo liver surgery. In 1988, ELRA was first reported, by Prof. R. Pichlmayr, to treat an advanced cancer that was judged to be conventionally unresectable and also represented a questionable indication for liver transplantation [17▪▪]. From then onward, the Hannover team extended their experience of ex-situ liver resection [18,19▪,20]. Afterward the technique has been taken up by other teams from Norway and France [21–23], in patients presenting other types of tumors, including hepatocellular/cholangio-cancer, colorectal liver metastases, and even nonmalignant lesions, such as giant focal nodular hyperplasia and hemangioma. However, the perioperative mortality was high (30%) and long-term survival time poor (< 2 years) [20]. In summary, a huge effort but a disappointing, risky, poor efficacious undertaking. Even after one decade of development, it was believed that this type of surgery seemed to be justified only in desperate situations of conventionally irresectable cancers [20]. The unsatisfactory results somehow casted a shadow to this potentially powerful surgery. Therefore, the technique did not take off and remained of interest for some very specialized hepatobiliary centers around the world looking for technical improvements or modifications of performance.

Since the technique struggled to prove its’ value, conventional advanced liver surgery continuously developed into a more controllable level. Prof. D. Azoulay (Paris, France) has put much effort by utilizing many techniques, including in-situ/ex-situ in-vivo liver resection with total vascular exclusion and/or hypothermic perfusion (in-situ liver cooling) with/without temporarily portocaval shunting [8▪,24,25▪]. Indeed, these are positive contributions aiming at extending the potential of conventional liver surgery. Nonetheless, still some situations remained that could not be safely dealt with even by such advanced resection strategies.

TECHNICAL EVOLUTION OF EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

Prof. J.H. Dong advocated the concept of Precision Liver Surgery and began to extend this concept in clinical practice at the end of last century. Along with this development, he also pioneered technical innovations and modifications from the 1990s to the first decade of the 21st century leading to procedural modularization, simplification, standardization and control of operative risks [26▪,27,28]. Later on, ELRA has been turned into a more systematic pattern and comprehensively applied technique with curative intent based on precise evaluation and operative performance.

Precision preoperative evaluation

Prof. Dong's team established a precision preoperative evaluation protocol for ELRA. One of the main pre-ELRA assessments focused on surgical indication. These included FLR's structure identification using both conventional radiological methods and three-dimensional evaluation focusing on length and range of the invaded vascular structures and pre-ELRA virtual surgery simulation to improve operative performance. These innovations and the integration of relevant techniques regarding assessment improved overall predictability and successfulness of the surgical procedure. Evaluation of FLR's volume and function was also targeted using quantitative methods commonly used on the field of living donor liver transplantation (LDLT). It is well known that one of the key points in LDLT is to stick to a minimal functional liver volume of the liver allograft in order to guarantee a successful transplant. The concept of the minimal functional liver volume required for basic body needs was introduced in this type of advanced liver surgery; this was termed as essential functional liver volume (EFLV). The determination of EFLV became later on a routine part of the preELRA assessment.

’None veno-venous bypass’ surgery

Remarkably, this team further introduced the none veno-venous bypass (NVVB). This approach significantly simplified ELRA surgery, eliminated bypass-related morbidity and transformed the procedure into a more controllable status [29▪▪,30,31▪]. Explanting the liver en bloc along with retro-hepatic inferior vena cava (RHIVC), restoring temporary caval blood flow using an autogenic/allogenic or prosthetic vascular graft and performing an end-to-side porto-caval shunting greatly changed this intervention.

By offering both hemodynamic stability and coagulative hemostasis for up to 8–12 h, NVVB renders the anhepatic phase much easier. NVVB hepatectomy represented a milestone in the developmental phase of ELRA because reducing significantly morbidity and mortality [31▪,32,33▪▪]. Later on, some NVVB variants were developed according to the presence of collateral circulation and specific explant procedures.

Outflow-centered systemic optimization

In 2010, advanced hepatic alveolar echinococcosis was introduced in the context of a collaborative effort of the Beijing (from Tsinghua University) and an Urumqi (from Xinjiang Medical University) teams as a new indication for ELRA [34▪]. Over the years, the obtained clinical results of ELRA for alveolar echinococcosis were very encouraging [35]. Indeed, alveolar echinococcosis allowed to uncover the potential power of this technique. With growing ELRA-alveolar echinococcosis experience, increasing challenges in reconstructing autograft outflow had to be taken up due to the frequent infiltrative invasion of the hepato-caval venous area. The need for precision evaluation as well as for tailored surgical strategy of the outflow reconstruction became all the time greater. Based on our previous accumulative and comprehensive experience, a useful classification of the surgical indications based on outflow invasion and pattern was made in order to orchestrate pre-ERLA evaluation and surgical planning with the aim to improve predictability and safety of the procedure. Such systemic optimization also continuously influenced practices in other centers. Here some relevant technical advances are presented.

DISEASE SELECTION FOR EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

Initially, ELRA was chosen to treat a conventionally unresectable liver malignancy [17▪▪]. Until the end of the 20th century, ELRA procedures were reported as case reports dealing with malignant tumors. The experience within liver surgical and transplantation community was indeed scarce. Oldhafer, a mentee of the Pichlmayr school, concluded in a report that the long-term results of the procedure were unsatisfactory: 8 (36.3%) of their 22 patients, six patients treated for colorectal liver metastases (CRLM) had a median survival of 21 months; the two patients treated for a benign tumor were alive at 5 and 9 years [19▪]. Taking into account the prevalence of early deaths and high recurrence rates in patients with malignant tumors, the indication for ELRA was considered very cautiously [20].

A recent systematic review and meta-analysis done in accordance with the PRISMA-search guidelines analyzed the results of ELRA in the treatment of 244 malignant (34.4%) and benign (65.6%) diseases [36▪]. The main indications for ELRA were alveolar echinococcosis, CRLM, and cholangiocarcinoma. Patients undergoing ELRA for benign tumors had a significantly better outcome than those which had a malignant tumor: the 30-day mortality rate was similar between the two groups (6.3% benign tumor patients vs. 11.3% malignant tumor patients, P > 0.05) but major surgical complications were less frequent (21.0% vs. 50.0% in malignant tumor patients, P < 0.001) and 1-year survival was better (89.7% vs. 65.0%, in malignant tumor patients, P < 0.001). Regression analysis confirmed that the outcomes of patients with benign tumors were better compared to those with malignant tumors (odds ratio: 4.629; 95% confidence interval/CI: 2.181–10.097, P < 0.001). Alveolar echinococcosis is a malignant-like growing benign disease (biologically benign but clinically malignant), that not only frequently invades major hepatic vessels and RHIVC but also infiltrates upwards the right atrium and downwards reno-caval confluence. The chronic and space-occupying progression of alveolar echinococcosis together with the regeneration capacity of the underlying normal liver parenchyma, creates special anatomic and functional conditions allowing this disease to be suitable for ELRA. Given these bio-clinical features, alveolar echinococcosis proved it's superiority over other diseases regarding long-term prognosis after ELRA [36▪]. The above mentioned literature review along with recent publications, allowed to identify over 200 alveolar echinococcosis cases treated by ELRA with good long-term outcome data [36▪,37▪,38]. Alveolar echinococcosis has become not only the most important indication for ELRA but this disease allowed to foster again the interest of the surgical hepatobiliary community for this technique.

Particular conditions, such as cavernous transformation of portal vein (CTPV), also can be managed well by this technique. In 2017, our team performed the world first ELRA for CTPV, the patient is well and alive 5-year after surgery. Recently, ELRA was also successfully performed as radical treatment for well differentiated and less aggressive malignant tumors, such as hepatic neuroendocrine tumor and perivascular epithelioid cell tumor. These patients also had very encouraging outcomes with good follow-up results.

From a prospective view, malignant tumors also have the potential to be selected for ELRA in near future seen the fact that systematic therapies are able to better and faster control cancer progression, even achieving in some cases a complete response. Especially, the combination of locoregional treatment and immunotherapy or targeted medical treatments allows to obtain remarkable response rates. It is to be expected that the indications for ELRA will be expanded in a near future allowing more patients to benefit from this procedure.

SURGICAL INDICATIONS OF EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

ELRA is an aggressive approach that should only be used when conventional in-vivo surgery poses too high risks even in experienced hands. Up to now, no widely accepted algorithm exists in relation to applicability of this procedure.

As mentioned previously, ELRA was performed in cases with conventionally (in situ approach) unresectable tumors that invaded hepato-caval venous confluence and portal vein [39].

Some years ago, W.T. Wang's team from West China Hospital of Sichuan University, Chengdu linked the surgical planning of ELRA to the type and extension of infiltration of IVC, portal and hepatic veins [40▪]. Four types of anatomic lesion features were identified: type I is characterized by the most severe invasion of the first porta hepatis with varying degrees of IVC and outflow tract violations; type II focuses on IVC invasion including diaphragm or even right atrium; (the more common) type III applies to cases with multiple sites of vascular infiltration, but none of them are extremely infiltrated and type IV presented with less vascular infiltrations. Type I and II represent definite and type III relative indications for ELRA; type IV is considered as a relative indication for ELRA seen the possibility to still do in vivo surgery. In type III the indication is more related to the space-occupying effect of the tumor or to high probability of massive hemorrhage. This effort to stratify the indications of ELRA should be encouraged even if there were no obvious prognostic differences between the different type.

Based on our nearly 3 decades’ experience and accumulative research, we consider three major aspects in the decision-making process: severe tumor/lesion invasion that poses anatomical impossibility for radical in-situ operation; uncontrollable massive bleeding or predicted hemodynamic unsafety; and sufficient, quality and quantity wise, essential liver parenchyma's for successful surgical performance. ELRA is definitely indicated in case the FLR's hepatic venous outflow, hepato-caval confluence area, the right atrium and the tertiary PV branch are invaded. ELRA is relatively indicated in case one foresees a probable risk for massive bleeding or impossibility to achieve radical in-vivo resection due to the space-occupying effect of the lesion(s). Of course, when dealing with complex situations, decision making may vary between ‘hands’ and centers. The most significant factor for success is the surgeons’ ability to control risks of the procedure, the major standard for surgical success. Effective organ preservation, hemodynamic stabilization and ideal reconstruction of FLR vasculature are key requirements to damage control. In case of clear cut indications, the realization of ELRA should be promoted, conversely in case of relative indications the number of ELRA procedures should be reduced. It is important to emphasize that nonradical ELRA attempts should be avoided at any time.

OUTFLOW RECONSTRUCTION IN EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

As far as outflow reconstruction is concerned, congestion, stretching or anastomotic stenosis of hepatic vein ostium should be, similarly to what is recommended in LDLT, avoided at any price [41]. The creation of a widely patent hepatic vein of the FLR must be guaranteed before implantation of the autograft. This can be done by performing an all-in-one back-table outflow reconstruction (Fig. 1a,b). This is particularly important when multiple orifices are present (as is frequently the case in LDLT) [41–43]. In this situation, venous graft is very useful to make a high quality end-to-side anastomosis with RHIVC (Fig. 1c). When the autograft including the RHIVC is prepared on the back-table, ex-vivo hepato-caval venous reconstruction is useful to avoid vascular twisting, outflow obstruction or occlusion. Due to the extended invasion of segmental tributaries of FLR in most ELRA cases, vascular patching or lengthening is utilized aiming at preservation of all significant venous outflow ostia (Fig. 1d). Ex-vivo hepato-caval venous reconstruction also allows to detect and manage possible anastomotic leaks prior to autograft implantation.

F1FIGURE 1:

Outflow reconstructions. a. Left lateral autograft with sub-segmental outflow orifices (V3 s). b. All-in-one reconstruction for V3 s using allogenic venous graft. c. Ex- vivo all-in-one reconstruction of outflows. d. Ex-vivo segemental outflow lengthening-e. Retroperitponeal collaterals sufficient to RHIVC. f. End-to-end revascularization of augograft outflow with supra-hepatic IVC. g. Supra-hepatic IVC and right atrium invasion. h. Right atirum and supra-hepatic IVC reconstruction with vascular engraftment. All images had been provided by Dr. Rui Tang.

In case a substitutional collateralization (usually via the dilated azygos veinous system), is present, the RHIVC can be abandoned (left unreconstructed). In this situation, the outflow restoration of the autograft differs from the classical ELRA procedure in the way that the hepatic venous outflow and supra-hepatic IVC will be anastomosed directly in an end-to-end fashion (Fig. 1e,f).

When the right atrium needs to be reconstructed, the autograft implantation and hepatic outflow management become even more complicated as sinoatrial node and interventricular septum need to be protected at any price (Fig. 1g,h). It might be necessary to use a lengthy venous graft to obtain a high quality anastomosis. Chronic Budd-Chiari syndrome (BCS) was initially considered in some advanced benign situations as a contraindication for ELRA [44▪]. The team of the Sichuan Provincial Hospital in Chengdu introduced a staged treatment for alveolar echinococcosis with BCS combining prior interventional radiologic stenting of the hepatic outflow (to improve hepatic venous outflow and quality of the FLR) and ELRA [45]. This successful approach should be encouraged because allowing to expand the indications for ELRA.

In case outflow reconstructions become necessary, we strongly recommend the use of human venous rather than prosthetic grafts in order to avoid relevant complications. Autologous jugular, saphenous, umbilical, cryopreserved allogenic iliac, portal, hepatic and caval veins procured during the surgery can all be used for this purpose.

In case outflow obstruction is diagnosed during the postoperative follow-up, vascular interventional therapy is very helpful to solve the problem. When obstruction is suspected and confirmed by imaging, early intervention and settlement is needed to improve long-term prognosis. The team from First Clinical Medical College of Xinjiang Medical University, Urumqi recently diagnosed in 11 (13.1%) of 84 post-ELRA hepatic venous outflow obstruction [38]. Balloon dilation with eventual vascular stenting allowed to achieve a good result in all but one patient who died of liver failure and salvage liver transplantation.

PROGNOSIS AND BENEFITS OF EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

The results of the 2020 systematic review and meta-analysis by Zawistowski et al. about 244 ELRA cases identified in 53 papers have already be mentioned above [36▪]. In 2018 our cumulative ELRA experience for hepatic alveolar echinococcosis has been published [44▪]. This paper grouped the experiences with 69 ELRA for alveolar echinococcosis performed by the Beijing Tsinghua Changgung Hospital Tsinghua and The First Affiliated Hospital of Xinjiang Medical University, Urumqi teams during the period 2010–2017 [34▪]. A total of 30 day and > 90 days mortality rates were 7.24% and 11.5%, respectively; all survivors were disease-free during median follow-up of 22.5 months.

Prof. M. Gillet and French surgeons started allogenic liver transplantation for advanced alveolar echinococcosis, first in Hôpital Cochin in Paris, later on in Besançon located in an endemic alveolar echinococcosis area in the South-east of France [46]. The analysis of the European Liver Transplant experience Registry identified 45 patients receiving a liver transplantation and pre- and post-liver transplantation benzimidazole treatment. Their 5-years overall survival and disease-free survival rates were 71% and 58%, respectively [47▪]. Further, according to a literature review by Aliakbarian et al. including 150 alveolar echinococcosis cases, the overall 1-, 5- and 10-year post-liver transplantation survival rates reached 60–100%, 67–85%, and 49–75%, respectively; recurrence rate varied between 0% and 60% [48▪].

For sure allogenic liver transplantation has the obvious drawbacks of life-long immunosuppressive treatment, considered as a risk factor for disease relapse. Given the above described historical background, the organ shortage and the high alveolar echinococcosis prevalence in China, ELRA successfully avoided a liver transplantation in a growing number alveolar echinococcosis patients who should have undergone allogenic liver transplantation before 2010 [49]. Recently, Wang's team from West China Hospital of Sichuan University, Chengdu retrospectively studied the benefits of ELRA in a cohort of 228 patients treated during the period 2014 to 2020 for end-stage hepatic alveolar echinococcosis [50▪]. The 5-year overall survival of the ELRA group was superior to that of the nonsurgical group (82.1% vs. 19.1%, P < 0.001). They also showed that, the basic risk of 12-month mortality had a significant effect in relation to the benefit of ELRA in the entire cohort: patients with a predicted 12-month mortality risk of >75% indeed significantly benefited from ELRA. Besides, combined resection and overall surgery time were identified as independent risk factors for major postoperative morbidities.

In Europe, ELRA might not be realized in large amounts due to the fact that there are less cases of advanced alveolar echinococcosis cases justifying ELRA also to the fact that alveolar echinococcosis disease control is remarkably good [51]. Conversely autotransplantation surgery serves well Chinese patients living in endemic areas and presenting an advanced parasitic disease. Taking into consideration epidemiological background, biological/clinical features of echinococcosis and disease burden, the Chinese government has deployed major efforts to eliminate echinococcosis in near future.

Taking into account technical advancements in the treatment of malignant and benign hepatic diseases, our continuously growing ELRA experience, the previous European liver transplantation experience for alveolar echinococcosis (with the unsatisfactory oncological or parasitological outcomes) and the recent comparison of results obtained after ELRA and observational treatment, it could be concluded that the results of ELRA are superior to those obtained after allogenic liver transplantation and observational treatment for well selected patients having similar hepatic conditions. Of course, in spite of these advantages, ELRA cannot fully replace allogenic liver transplantation, especially when an underlying liver disease or high-risk vasculature repair is present.

LEARNING CURVE OF EX-VIVO LIVER RESECTION AND AUTOTRANSPLANTATION

Recently, Wang et al. reported their ELRA learning curve based on more than 6 years’ experience [37▪]. Their risk-adjusted analysis (including age, disease course, liver function and remote metastasis) cumulative sum set the ELRA learning curve for major postoperative complications at 53 procedures. Significant factors were length of hemodynamic instability or prolonged anhepatic phase (hazards ratios/HR 30.29, 95% confidence interval, CI 43.32–17.25, P < 0.0001), reimplantation time (HR 13.92, 95% CI 23.17–4.67, P 0.004), total postoperative hospital stay (HR 6.87, 95% CI 11.33–2.41, P 0.0033), and major morbidities (HR 0.25, 95% CI 0.09–0.68, P 0.007).

This learning curve is longer than that reported for allogenic liver transplantation during fellowship (45 liver transplantation) [52]. Because ELRA represents a hybrid surgery including experiences obtained from advanced liver surgery and liver transplantation, it has not yet been widely performed globally. A relatively longer learning curve is therefore safer. Centers without a rich experience in both advanced liver surgery and liver transplantation should be cautious when applying this technique.

CONCLUSION

ELRA is a promising procedure that can render possible a potentially curative treatment to selected patients presenting conventionally unresectable tumors or space-occupying lesions. Benefits of ELRA are highest in benign diseases, but some well differentiated or less aggressive malignant tumors can also benefit from the technique. Surgical indications should synchronously take into account following three aspects: impossibility to totally eradicate the target lesion, impossibility to preserve enough FLR and to restore invaded vascular structures and finally possible instability due to high risk for massive hemorrhage or hemodynamic problems. Efficient outflow reconstruction during autograft reimplantation is an essential factor for surgical success. It should be emphasized that centers which do not have sufficient technical experience in complex liver surgery and liver transplantation must be cautious when performing this complex procedure. Collaboration between experienced centers is warranted to further optimize the outcome of this emerging technique and to develop practical guidelines which are necessary to develop this intervention on a global scale.

Acknowledgements

The authors thank Prof. Jan Lerut (Institut de Recherche Clinique et Expérimentale [IREC], Université Catholique de Louvain [UCL], Brussels) and Prof. Chen Chao-Long (Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung) for their encouragements on the continuous efforts in ex vivo liver surgery, inviting authors to contribute this paper and offering valuable advice in improving this review. Additionally, the authors want to thank their colleagues who have been cooperating with them: Prof. Yang Zhanyu & Prof. Duan Weidong (Chinese PLA General Hospital), Prof. Fan Haining (Qinghai University), Prof. Wang Wentao (West China Hospital), and Prof. Wen Hao (Xinjiang Medical University).

Financial support and sponsorship

National Natural Science Foundation of China (81930119, 82090050, 82090053); CAMS Innovation Fund for Medical Sciences (2019-I2M-5-056).

Conflicts of interest

There are no conflicts of interest.

REFERENCES AND RECOMMENDED READING

Papers of particular interest, published within the annual period of review, have been highlighted as:

▪ of special interest

▪▪ of outstanding interest

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