In situ liver resection under venovenous bypass (LR-VVB) or venoarterial bypass (LR-VAB) adjunct to total vascular exclusion (TVE) as extreme liver surgery

Introduction

Highly technique-demanding liver resections (LRs) associated with multiple vascular reconstructions under total vascular exclusion (TVE) with/without hypothermic perfusion or using extracorporeal approaches (ante situm, ex situ) have been incorporated within the scope of extreme liver surgery (1,2). From our perspective, in situ liver resection under venovenous bypass (LR-VVB) or venoarterial bypass (LR-VAB), adjunct to TVE, also qualifies as extreme liver surgery. To comprehend this, understanding their current technical foundations is necessary.

Classification of external bypasses

Classic VVB technique (femoral/portal-to-axillary VVB), which drains caval and splanchnic veins and pumps into the axillary vein, was initially introduced in liver transplant by the University of Pittsburgh team (3). This method facilitates safe total hepatectomy and maintains hemodynamic stability during the anhepatic phase. In non-transplant liver surgery, several VVB or VAB approaches have been reported, and they can be classified as follows (Figure 1).

• Model 1: this easy-to-establish basic model was initially introduced to manage juxtahepatic caval injuries (4) and is applicable for resecting tumors involving the inferior vena cava (IVC). The limitations of this approach include inevitable splanchnic congestion and hepatic ischemia when portal clamping exceeds the tolerance threshold.
• Model 2a: the classic model was innovatively adapted for major hepatectomies involving retrohepatic IVC reconstruction in hepatocellular carcinoma at the hepatocaval confluence with underlying cirrhosis (5,6). This approach was demonstrated to be safe and effective for expanding resection criteria for previously unresectable tumors (6) and has since been applied in juxtahepatic caval injuries (7). However, prolonged use may compromise liver function due to warm ischemia.
• Model 2b: this technique was developed to enable safe and radical resection of a metastatic tumor occupying the entire right lobe and partial left medial section (8). Postoperative recovery showed mild liver injury, and the technique was believed as a novel strategy for complex resections deemed otherwise unresectable. Probably, it may be applicable in Budd-Chiari syndrome secondary to lesion involvement of the hepatic veins, which was also managed by preoperative percutaneous venous stenting (9).
• Model 3: this was a newly established strategy used to achieve safe and radical resection of a recurrent leiomyosarcoma at the hepatocaval confluence and reconstruction of both middle and left hepatic veins using a cryopreserved venous graft (10).
• Model 4a: this sternotomy-avoiding minimally invasive peripheral approach was also a newly proposed solution for managing tumors extending to the suprahepatic IVC, right atrium or pulmonary artery (11). This model was considered advantageous over traditional cardiopulmonary support by significantly reducing surgical invasiveness.
• Model 4b: the sternotomy-based conventional approach currently serves as a standard solution for tumoral and complex vascular accesses—ascending aorta, superior and IVC (12). It remains a complete cardiopulmonary support, as it presents significant challenges with exceptionally high technical demands and an absolute requirement for multidisciplinary collaboration, and it is typically reserved for tumors with atrial extension or pulmonary tumor thrombi.

Figure 1 External VVB and VAB techniques in non-transplant liver surgeries. Model 1 (single-cannula): femoral-to-axillary VVB drains caval flow and pumps into axillary vein to reduce intraoperative bleeding, prevent renal injury, and maintain adequate central venous filling during TVE. Model 2a (dual-cannula): femoral/portal-to-axillary VVB drains caval plus portal flows and pumps into axillary vein to furtherly minimize splanchnic congestion during TVE, and it can extend hepatic tolerance when combined with hypothermic perfusion. Model 2b (dual-cannula): femoral/hepatic-to-axillary VVB drains caval plus hepatic flows and pumps into axillary vein, and it mitigates both splanchnic congestion and warm hepatic ischemia by combining intermittent TVE. Model 3 (triple-cannula): femoral/portal/hepatic-to-axillary VVB drains caval, portal plus hepatic flows and pumps into axillary vein to obtain enhanced hemodynamic stability by sequential control of the cannulas, and it could enable prolonged procedure duration if required and immediate access for supplemental hypothermic perfusion when indicated. Model 4a (venoarterial): femoral/jugular-to-femoral VAB drains both inferior and superior vena cava flow and pumps into the femoral artery, all through peripheral accesses, to safely resect tumors extending to suprahepatic IVC, right atrium and pulmonary artery. Model 4b (venoarterial): femoral/portal/caval-to-aorta VAB drains inferior and superior vena cava plus portal flow and pumps into ascending aorta, relying on sternotomy, to safely resect tumors extending to suprahepatic IVC, right atrium and pulmonary artery. IVC, inferior vena cava; TVE, total vascular exclusion; VAB, venoarterial bypass; VVB, venovenous bypass.

There are some complementary techniques and clinical considerations. For VVBs (models 1/2a/2b/3): hypothermic perfusion can be integrated with models 1/2a/3 when TVE exceeds 1-hour or complex vascular reconstruction is required (13); passive bypass may suffice in hemodynamically stable cases; models 1/2a demonstrates versatility, being combinable with in situ, ante situm, ex situ hypothermic liver surgeries (13-15). For VABs (models 4a/4b): primary objectives or indications could be safe extraction of cava-atrial tumor thrombi and converting high-risk scenarios into manageable procedures; key limitations (particularly model 4b) might be requirement for vascular/cardiothoracic surgical expertise, potential need for cardiac arrest in some cases, and mandatory systemic anticoagulation; model 4b could be used in in situ, ante situm, ex situ hypothermic LRs. In some cases, a transient porta-caval shunt is utilized in bypass-assisted liver surgery.

External bypass application

The complete procedural workflow for bypass installation, operation, and removal has been detailed in prior publications (4-8,10-12,16). Key components include vascular cannulation, circuit establishment, and bypass termination and decannulation (Table S1).

TVE

A team from Paul-Brousse Hospital has clearly presented three major approaches of TVE (13). State-of-the-art TVE should be planned ahead and performed sequentially to minimize organ injury and maintain hemodynamic stability (Table S2).

Discussion

As surgical and anesthetic techniques in LR and transplantation have improved, a wide variety of benign and malignant tumors have become surgically treatable. Basic strategies that have significantly increased safe resectability are TVE and hypothermic perfusion, which were established half a century ago (17). Considering that most candidates must undergo major hepatectomy and eventually recover with a limited future remnant liver volume, ischemia-reperfusion injury after prolonged cold ischemia cannot be underestimated (8). The decision to apply hypothermic perfusion is mainly based on the duration of TVE, with the threshold generally believed to be one hour in normal liver (12,13,18).

However, it is particularly difficult to predict exactly how long vascular exclusion will be needed, even when allowing for worst-case scenarios (19). Therefore, decision-making of supplement hypothermic perfusion to TVE poses difficulties during surgery. Utilizing LR-VVB while avoiding hypothermic perfusion and patient hypothermia can increase safety measures for both hepatic function and technical aspects, potentially mitigating associated risks (8,20).

We think that the underlying logic for applying TVE, hypothermic perfusion, VVB, and VAB techniques in non-transplant liver surgeries is no more than controlling intraoperative bleeding, maintaining hemodynamic stability, protecting organs, and enabling careful handling with less time pressure. Inherently, TVE and hypothermic perfusion could result in apparent ischemia-reperfusion injury and delayed organ recovery. In this context, hypothermic oxygenated machine perfusion technique has been tried in in situ, ante situm, and ex situ LRs, though their efficacy still needs large-scale assessment (21-23). In comparison, VVB and VAB might offer advantages with less ischemia-reperfusion injury, less circulatory disturbance, and better organ recovery in cases with limited future remnant liver volume and background pathology when used properly with careful coagulation/anticoagulation management.

According to literature, LR-VVB and LR-VAB are neither new types of liver surgery nor single surgical scenarios, as different models exist (Figure 1) (4-8,10-12). However, careful attention needs to be paid during decision-making by considering potential risks and alternatives within a multidisciplinary framework, as implementing an additional bypass increases surgical invasiveness. Future studies may demonstrate their superiority over other techniques or identify hidden drawbacks.

In conclusion, LR-VVB and LR-VAB adjunct to TVE manage crucial situations requiring vascular resection-reconstruction, hepatectomy beyond anatomical boundaries, and borderline future liver remnant (2), qualifying them as a subcategory of extreme liver surgery. These techniques could become an alternative solution for lesions at hepatocaval confluence, paracaval area, caudate lobe, or cavoatrial junction, which are being treated primarily with in situ, ante situm, or ex situ LRs under hypothermic perfusion (13-15,24). This paper proposed a classification method for external bypasses (VVB and VAB) in non-transplant liver surgeries, summarized methodological aspects of bypass and TVE application, and evaluated the techniques’ potential advantages and disadvantages.

Acknowledgments

None.

Footnote

Provenance and Peer Review: This article was a standard submission to the journal. The article has undergone external peer review.

Peer Review File: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-2025-170/prf

Funding: This study was supported by grants from the Beijing Hospitals Authority Youth Program (No. 12022B4010), BTCH Young Talent Enlightenment Program (No. 2024QMRC24).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-2025-170/coif). The authors have no conflicts of interest to declare.

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References

1. Lopez-Lopez V, Lodge P, Oldhafer K, et al. Harmonizing Definitions and Perspectives in Extreme Liver Surgery: A Delphi Experts Consensus. Ann Surg 2024; Epub ahead of print. [Crossref] [PubMed]
2. Aini A, Lu Q, Wen H, et al. Particular Chinese contributions to extracorporeal liver surgery. Hepatobiliary Pancreat Dis Int 2025;24:57-66. [Crossref] [PubMed]
3. Shaw BW Jr, Martin DJ, Marquez JM, et al. Venous bypass in clinical liver transplantation. Ann Surg 1984;200:524-34. [Crossref] [PubMed]
4. Rogers FB, Reese J, Shackford SR, et al. The use of venovenous bypass and total vascular isolation of the liver in the surgical management of juxtahepatic venous injuries in blunt hepatic trauma. J Trauma 1997;43:530-3. [Crossref] [PubMed]
5. Kumada K, Shimahara Y, Fukui K, et al. Extended right hepatic lobectomy: combined resection of inferior vena cava and its reconstruction by EPTFE graft (Gore-Tex). Case report. Acta Chir Scand 1988;154:481-3. [PubMed]
6. Yamaoka Y, Ozawa K, Kumada K, et al. Total vascular exclusion for hepatic resection in cirrhotic patients. Application of venovenous bypass. Arch Surg 1992;127:276-80. [Crossref] [PubMed]
7. Biffl WL, Moore EE, Franciose RJ. Venovenous bypass and hepatic vascular isolation as adjuncts in the repair of destructive wounds to the retrohepatic inferior vena cava. J Trauma 1998;45:400-3. [Crossref] [PubMed]
8. Kim DS, Yu YD, Jung SW, et al. Extracorporeal hepatic venous bypass during en bloc resection of right trisection, caudate lobe, and inferior vena cava: a novel technique to avoid hypothermic perfusion. J Am Coll Surg 2013;216:e47-50. [Crossref] [PubMed]
9. Zhang Y, Xie P, Yang C, et al. The Value of Hepatic Vein Stent Placement as a Bridge Therapy on Treating Hepatic Alveolar Echinococcosis Presenting With Budd-Chiari Syndrome. Ann Surg 2021;273:e154-6. [Crossref] [PubMed]
10. Bachellier P, de Mathelin P, Addeo P. Hepatectomy with Hepatic Vein Resection and Reconstruction Under Total Vascular Exclusion and Venous Drainage via a Venovenous Bypass: An Additional Approach for Complex Hepatectomies. Ann Surg Oncol 2025;32:1896-7. [Crossref] [PubMed]
11. Maki R, Iwagami Y, Kobayashi S, et al. Minimally invasive approach of hepatectomy and thrombectomy for hepatocellular carcinoma with right atrial tumor thrombus without sternotomy using percutaneous cardiopulmonary bypass. J Hepatobiliary Pancreat Sci 2024;31:e62-5. [Crossref] [PubMed]
12. Nishiwaki Y, Kusano T, Hiraiwa T, et al. Fifteen-year survival of a hepatocellular carcinoma extending into the right atrium treated by surgical resection with the heart-first approach under cardiopulmonary bypass: a case report and review of the literature. Clin J Gastroenterol 2024;17:118-29. [Crossref] [PubMed]
13. Azoulay D, Andreani P, Maggi U, et al. Combined liver resection and reconstruction of the supra-renal vena cava: the Paul Brousse experience. Ann Surg 2006;244:80-8. [Crossref] [PubMed]
14. Raab R, Schlitt HJ, Oldhafer KJ, et al. Ex-vivo resection techniques in tissue-preserving surgery for liver malignancies. Langenbecks Arch Surg 2000;385:179-84. [Crossref] [PubMed]
15. Lodge JP, Ammori BJ, Prasad KR, et al. Ex vivo and in situ resection of inferior vena cava with hepatectomy for colorectal metastases. Ann Surg 2000;231:471-9. [Crossref] [PubMed]
16. Fabre D, Houballah R, Fadel E, et al. Surgical management of malignant tumours invading the inferior vena cava. Eur J Cardiothorac Surg 2014;45:537-42; discussion 542-3. [Crossref] [PubMed]
17. Fortner JG, Shiu MH, Kinne DW, et al. Major hepatic resection using vascular isolation and hypothermic perfusion. Ann Surg 1974;180:644-52. [Crossref] [PubMed]
18. Sadamori H, Monden K, Hioki M, et al. Liver Resection Under Total Hepatic Vascular Exclusion with In Situ Hypothermic Isolated Hepatic Perfusion for Advanced Liver Tumors. Ann Surg Oncol 2024;31:5638-9. [Crossref] [PubMed]
19. Dubay D, Gallinger S, Hawryluck L, et al. In situ hypothermic liver preservation during radical liver resection with major vascular reconstruction. Br J Surg 2009;96:1429-36. [Crossref] [PubMed]
20. Addeo P, de Mathelin P, Bachellier P. ASO Author Reflections: Venous Drainage Through a Veno-Venous Bypass in Complex Hepatectomies: Another Piece of the Puzzle. Ann Surg Oncol 2025;32:2864-5. [Crossref] [PubMed]
21. Tribolet A, Salloum C, Allard MA, et al. Left Hepatectomy Enlarged to Segment 1 with Total Vascular Exclusion of the Liver Preserving the Caval Flow with Temporary Portacaval Shunt and Hypothermic Oxygenated Portal Perfusion on Machine for Metastatic Recurrence of a Pleural Chondrosarcoma. Ann Surg Oncol 2025;32:4383-7. [Crossref] [PubMed]
22. Cillo U, Furlanetto A, Nieddu E, et al. Ante situm liver surgery using machine perfusion liver preservation: pilot human experience. Br J Surg 2021;108:e235-6. [Crossref] [PubMed]
23. Gringeri E, Auricchio P, Perin L, et al. A Translational Approach to Standardization of Machine Perfusion Adoption in Ex Vivo Liver Resection. Ann Surg Oncol 2020;27:1919. [Crossref] [PubMed]
24. Aini A, Lu Q, Chen Z, et al. Ex-vivo Liver Resection and Autotransplantation for Liver Malignancy: A Large Volume Retrospective Clinical Study. Ann Surg 2024;280:879-86. [Crossref] [PubMed]