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Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome

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Hepatoma Res 2024;10:11.
10.20517/2394-5079.2023.97 |  © The Author(s) 2024.
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Abstract

Liver resection stands as the gold-standard therapeutic approach for selected cases of hepatocellular carcinoma (HCC). The extent of resectable parenchyma hinges upon the underlying liver function and its regenerative potential. Consequently, cirrhosis may impede access to potentially curative interventions for HCC arising within this context. Cirrhotic patients undergoing liver resection face heightened susceptibility to post-hepatectomy liver failure (PHLF). The clinical profile of PHLF bears a resemblance to a well-documented syndrome within the liver transplant (LT) domain: Small-for-size syndrome (SFSS), a form of graft failure observed in the postoperative phase following LT with undersized or partial organs. Management of SFSS targets mitigating the overflow syndrome, achievable through diverse portal diversion techniques. Portal vein flow diversion encompasses procedures redirecting a variable proportion of portal vein flow towards systemic circulation. Consequently, derivative procedures aim to directly alleviate portal hypertension. Side-to-side portocaval shunts emerge as the most straightforward and efficacious means of decompressing the portal system. Furthermore, they afford flow calibration to diminish the incidence and severity of steal syndrome and hepatic encephalopathy, without compromising efficacy or hepatic function. Translating insights gleaned from LT complexities involving SFSS to liver resection, strategies involving portal flow diversion warrant consideration in efforts to forestall PHLF. This approach aims to extend the frontiers of liver surgery, broadening access to hepatectomy with curative intent, either as a standalone intervention or as part of a comprehensive treatment regimen where LT serves as a secondary option.

Keywords

Portosystemic shunts, liver resection, cirrhosis, post-hepatectomy liver failure, small-for-size

INTRODUCTION

Liver resection stands as the benchmark treatment for carefully chosen cases of hepatocellular carcinoma (HCC), contingent upon the disease stage and liver function[1,2]. Surgeons prioritize considerations of tumor burden and the quality of liver tissue when strategizing hepatectomy. The volume of resectable parenchyma depends on underlying liver function and its regenerative capacity; hence, cirrhosis can limit access to potentially curative treatments of HCC arising in this context. Cirrhotic individuals undergoing liver resection face heightened susceptibility to post-hepatectomy liver failure (PHLF), wherein the future liver remnant (FLR) fails to meet the patient's metabolic demands. PHLF manifests through progressive organ dysfunction, accentuated by metabolite accumulation (bilirubin, ammonia, etc.) and complications such as ascites, hemorrhage attributable to diminished coagulation factor synthesis, septic infections, and renal impairment. The rapid progression from liver failure to multi-organ failure underscores the urgency in managing this condition to avert patient mortality[3].

Pathophysiology of post-hepatectomy liver failure

Cumulating evidence supports the hypothesis that the functional failure of the remnant liver after hepatectomy may be caused by alterations in the hepatic microvascular bed[4-8]. A critical factor in this process is the wedge pressure at the sinusoidal level. In cirrhotic livers, the control mechanisms of sinusoidal flow are compromised. Relative portal hyperperfusion, characteristic of cirrhosis and exacerbated by reduced vascular bed post-hepatectomy, leads to microcirculatory trauma and subsequent inhibition of organ functions. Experimental studies indicate that while some degree of portal hyperperfusion stimulates hepatic regeneration, excessive increases may cause hepatocellular damage[9,10].

Intrahepatic flow and its composition, particularly the proportion of venous and arterial blood, are vital for organ homeostasis[11-14]. The Hepatic Arterial Buffer Response (HABR) plays a key role in maintaining hepatic blood flow stability. The physiological basis of HABR involves adenosine clearance, a potent vasodilator, predominantly for the hepatic artery[15]. Decreased portal flow increases intrahepatic adenosine concentration, stimulating hepatic arterial flow to maintain overall organ blood flow[12].

Conversely, increased portal flow post-hepatectomy reduces arterial supply[16], potentially impacting bile duct perfusion. Research using techniques like portal vein ligation in animal models reveals that substantial portal stenosis triggers HABR[11].

The increase in portal flow resulting from parenchyma removal causes an important decrease in the arterial supply to the organ; the consequences of this alteration lead to relative ischemia of the biliary tree and a decrease in the regenerative capacity of the liver. Microscopic changes include endothelial and sinusoidal alterations, hepatocyte degeneration, mitochondrial swelling, thrombotic events in small portal branches, occasional recanalization, regenerative hyperplasia, and biliary stenosis in later stages[11,17,18].

Limits of current strategies to increase FLR in cirrhotic patients

Understanding the significance of a small future liver remnant (FRL) and its impact on the feasibility of curative liver tumor resection has been pivotal. Strategies to increase so-called functional resectability have been investigated over the last 15 years[19]. Portal vein embolization (PVE) or ligation (PVL) stands out as a significant advancement, enabling preoperative modulation of liver volume. The evolution of this concept has led to two-stage hepatectomy (TSH) and, more recently, associated liver partition and portal vein ligation for staged hepatectomy (ALPPS). These techniques have facilitated extensive hepatectomy, even for multiple or large HCCs, by augmenting the FLR[20,21]. However, the efficacy of liver volume modulation varies across different liver malignancies and is contingent upon liver parenchyma quality. TSH is hampered by an incompletion rate of over 30%, attributed to ineffective liver hypertrophy and potential tumor growth stimulation[22,23]. ALPPS initially promised nearly 100% resection rates for otherwise functionally irresectable tumors[24,25], but enthusiasm waned due to high morbidity and mortality rates, particularly in HCC patients[26,27]. The exact underlying causes remain elusive; however, the prolonged manipulation and permanence of the tumor for several days after the first-stage operation, coupled with a surge in cytokines and growth factors postoperatively, have been implicated in inter-stage tumor progression[26,28]. Moreover, FLR hypertrophy in fibrotic/cirrhotic livers appears suboptimal compared to noncirrhotic counterparts[29]. This concept is also reinforced by the evidence that the outcomes improved from the early phase, in which ALPSS was carried out in HCC patients regardless of the degree of underlying cirrhosis or concomitant portal hypertension[30], compared to the current era, when more stringent criteria are applied[31,32]. Consequently, advanced cirrhosis and portal hypertension emerge as limiting factors for liver volume modulation techniques.

Similarities between post-hepatectomy liver failure and small-for-size syndrome

The clinical features of post-hepatectomy liver failure (PHLF) bear a resemblance to a well-recognized syndrome in liver transplant (LT) practice: the Small-For-Size Syndrome (SFSS). SFSS denotes early graft failure following LT with undersized or partial organs[17,18]. Optimal graft-recipient size matching is crucial for LT success, with inadequate grafts typically characterized by a graft-recipient weight ratio of less than 0.8% (GRWR < 0.8%) or a graft-native liver weight ratio of less than 40%[33-36]. Undersized grafts fail to meet postoperative metabolic demands, resulting in organ dysfunction marked by hyperbilirubinemia, coagulopathy, and refractory ascites. Sepsis often complicates SFSS, leading to alarmingly high mortality rates[36]. While the etiology of SFSS is multifactorial, both graft and recipient factors contribute. Persistent elevated perfusion pressures and portal hypertension post-revascularization are implicated in SFSS-related organ injury, underscoring the complex interplay between graft and recipient factors in the development of this syndrome[37].

Mechanisms involved in the development of small-for-size syndrome

There is an agreement in attributing the cause of this syndrome to portal hyper-inflow[18], manifesting through various mechanisms:

● Shear Stress: Elevated portal pressure in the reduced-size liver induces mechanical trauma at the endothelial level, leading to extensive sinusoidal damage, endothelial cell destruction, and microhemorrhages at portal triads[36].

● Relative Decrease in Arterial Blood Supply: Compared to portal flow, reduced arterial blood supply compromises hepatocyte regeneration, hindering metabolic support crucial for regeneration[38,39].

Ito et al. demonstrated a significant incidence of SFSS in living donor liver transplantation (LDLT), particularly with left lobe partial grafts, correlating with portal pressure[40]. Portal vein pressure exceeding 20 mmHg post-LDLT predicts high morbidity and poor graft functional recovery.

Small for size syndrome treatment

Glanemann et al. conducted experiments demonstrating that diverting portal flow significantly enhances outcomes in animal models undergoing 90% liver parenchymal resection[4]. Rats subjected to hepatectomy with splenectomy exhibited minimal hepatocyte damage, evidenced by transaminase levels at least three times lower than controls. This improvement was attributed to reduced portal hyperflow post-surgery, evident just 15 min after the procedure, with rates notably lower in the study group (3.5 ± 0.4 mL/min) compared to controls (5.4 ± 0.4 mL/min). Portal diversion also enhances hepatic artery blood flow via HABR activation, arterializing liver-directed blood flow[4]. Treatment of SFSS aims to reduce the portal overflow that is characteristic of this syndrome, which is achievable through various portal diversion methods.

DEFINITION OF PORTAL VEIN FLOW DIVERSION AND TYPES OF PROCEDURES

Portal vein flow diversion encompasses procedures aimed at redirecting a variable portion of portal vein flow towards systemic circulation, directly targeting portal hypertension. These procedures include:

● Ligation or embolization of the splenic artery[41,42]

● Splenectomy[36]

● Preemptive portal branch ligation or embolization before hepatectomy, promoting compensatory hypertrophy and enhancing potential functional reserve[43]

● Porto-Systemic Shunts (PSS): including portocaval and splenorenal shunts[44-46]

The primary objectives of these interventions are twofold. Firstly, to diminish portal inflow by splenic artery embolization or ligation, addressing the significant yet fluctuating splenic component of portal hypertension. This approach has proven effective in managing esophageal variceal bleeding and small-for-size syndrome (SFSS), with reported post-surgical reductions in splenic flow of up to 52%[47,48].

Alternatively, diversion of portal blood flow can be achieved through PSS.

Both surgical and radiological portosystemic shunt procedures create a circuit allowing portal blood to bypass the liver, reducing both flow and portal pressure.

Transjugular Intrahepatic Portosystemic Stent Shunt (TIPSS) involves connecting an intrahepatic portal branch to a hepatic vein via a conduit, positioned percutaneously using interventional radiology. Advancements in this radiological method, particularly using covered stents, have improved outcomes in TIPSS patients, reducing interest in surgical shunts[49]. However, TIPSS may lead to hepatic encephalopathy and hinder future liver interventions due to the intrahepatic conduit. While indicated for cirrhotic patients with recurrent variceal bleeding and refractory ascites, TIPSS is contraindicated in those with HCC. Thus, it is not suitable for managing portal hypertension during HCC hepatectomy[50].

Surgical portosystemic shunts

The portocaval anastomosis, known as the Eck fistula, first described by T.E. Starzl in 1983[51], rapidly decompresses the portal system and achieves immediate decompression of the portal vein vascular bed[44-48]. Subsequently, various types of portosystemic shunts (PSS) have been described. These include connections between portal vein and caval systems through anastomoses between tributary vessels, with or without interposition of human iliac grafts from deceased donors or synthetic vascular prostheses made of Dacron or Goretex®-PTFE (Polytetrafluoroethylene).

Common surgical portosystemic shunts include:

● End-to-side portocaval shunts

● Mesenteric-caval shunts (with prosthesis interposition)

● Proximal (Linton procedure), central (Cooley procedure), and distal (Warren procedure) splenorenal shunts

● Speno-caval shunt (Orozco procedure)

● Side-to-side portocaval shunts, with or without interposition graft/prosthesis (H-graft portocaval shunt)

These procedures alter portal hemodynamics, reducing portocaval pressure gradients, but may cause varying degrees of portal flow inversion, depending on shunt type and dimension.

End-to-side shunts result in total portosystemic shunting with no remaining hepatopetal flow. It is associated with the development of refractory ascites in 5% of cases. The bleeding from rupture of esophageal varices is reduced to 5% after such interventions, but the rates of hepatic encephalopathy (which can reach 40%) and impaired liver and heart function (with possible development of high-flow heart failure) are quite high. Nowadays, it is almost abandoned, and it is only used in emergency settings due to its easy technical feasibility[52,53].

Mesenteric-caval and central splenorenal shunts, although effective, are considered secondary choices due to anastomoses on smaller, thrombosis-prone vessels. These procedures are preferred in the setting of portal hypertension due to portal vein thrombosis in non-cirrhotic patients[54-56]; in this setting, especially in pediatric extrahepatic portal vein occlusion, a modified mesenteric-caval shunt, named Meso-Rex Shunt, can be applied[57].

Warren procedure selectively targets esophageal varices, leaving portal flow largely unaffected[56,58-60].

Side-to-side portocaval shunts, whether H-shaped with graft/prosthesis interposition or not, are favored for their simplicity and efficacy in decompressing the portal system. These shunts offer flow calibration to reduce steal syndrome[61-63], and hepatic encephalopathy risk without compromising effectiveness or liver function. The H-graft interposition shunt preserves hepatopetal flow by approximately 80% with low encephalopathy rates (about 5%), and 5% rebleeding from gastroesophageal varices, with shunt patency of about 95% over 7 years[56,58,64,65]. Figure 1 provides a comparative overview of outcomes for the main portosystemic shunting techniques.

Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome

Figure 1. Visual comparison of various portosystemic shunt techniques alongside their primary pathophysiological consequences.

Applying the portosystemic surgical shunt to liver resection

In cirrhotic patients with HCC, treatment strategy hinges on a delicate balance between tumor-related and cirrhosis-related factors, profoundly impacting patient prognosis[1]. Essentially, the severity of cirrhosis diminishes the significance of HCC for long-term survival, prioritizing tumor control over disease clearance. Additionally, cirrhosis poses constraints on surgical options, heightening susceptibility to post-procedural or drug-induced liver failure. The barcelona clinic liver cancer (BCLC) staging system[66] initially developed and validated for HCC management, has become somewhat static over time, particularly inadequate for intermediate and advanced stages and decompensated cirrhotic patients due to evolving medical management and tumor biology understanding[67,68]. Increasing evidence demonstrates differences between BCLC recommendations and real-life approaches in HCC treatment[69,70]. In response to the limitations of the BCLC system, alternative staging concepts and treatment stage migration strategies have emerged, but these still focus on stage-oriented HCC treatment strategies[71].

A novel patient-oriented approach, termed “therapeutic hierarchy,” prioritizes treatment feasibility assessment to determine the optimal therapy for each patient at each stage[72,73].

Clinically significant portal hypertension (CSPH), often indicated by imaging findings of splenomegaly, varices, ascites, or a platelet count < 100,000/mL[74], marks decompensated cirrhosis and has historically contraindicated hepatic resections. However, cirrhotic patients with CSPH and HCC within Milan criteria[75] or extended validated criteria[76-79] stand to benefit most from liver transplantation (LT)[72,80]. If contraindications to LT arise, these patients, excluded from potentially curative treatments, often receive loco-regional therapy (LRT) or best supportive care (BSC), both yielding dismal prognoses. Despite long-standing contraindications, many tertiary hepatobiliary centers have successfully performed hepatectomy in cirrhotic patients with portal hypertension, reporting acceptable mortality rates, favorable long-term outcomes, and oncologic benefits[81-84]. Portal hypertension is not prognostic for perioperative mortality or long-term survival, according to multivariable analyses[83]. Moreover, updated guidelines from the European association for the study of the liver (EASL)[1] endorse liver resection in the presence of portal hypertension for patients at low risk of liver decompensation post-surgery[85].

Drawing lessons from LT complicated by SFSS, portal flow diversion strategies, such as portosystemic shunts, may prevent PHLF and expand the boundaries of liver surgery, increasing the number of those who can access hepatectomy with curative intent[86] or as a part of a wider treatment strategy that considers LT a second-line treatment. These shunts reduce sinusoidal wedge pressure post-hepatectomy, potentially preserving residual organ function and enhancing regenerative capacity while minimizing intra- and postoperative morbidity, including bleeding and ascites-major components of PHLF. Intraoperative bleeding, coagulopathy, and new onset ascites are indeed some of the major challenges cirrhotic patients face when undergoing surgery, and the mortality rates have been described as high as 10%-57%[87]. Portosystemic shunts have proven safe and effective in facilitating major abdominal surgery in cirrhotic patients. In the first pioneering experiences, it has been noted that patients with previous portocaval shunt performed better following non-hepatic surgery as compared to those without[88,89]. In the era of expanded-polytetrafluoroethylene (e-PTFE) covered stents, TIPSS occlusion rates dropped markedly, as well as the incidence of post-procedural hepatic encephalopathy when smaller stents were applied[90-92]. These results pushed surgeons to explore non-standard TIPSS applications more. Nowadays, both surgical shunt and TIPSS have been shown to increase the resection rate of gastrointestinal tumors in cirrhotic patients without increasing complication rates, and with less incidence of decompensated ascites after surgery[93-97]. In particular, TIPSS followed by surgery after a 30-day interval showed good portal hypertension control, 100% planned surgery completion rate, ascites and encephalopathy both in 12.5% of cases, and 80% overall survival at 1 year[98]. However, the TIPSS procedure is difficult to reverse in case of inefficacy or complications[90,92], with poor cost-effectiveness in this scenario[99]. Notably, the first case of liver resection for HCC in a patient who had previously placed a TIPSS for decompensated cirrhosis was recently published, and an uneventful postoperative course was reported[100]. Nonetheless, TIPSS has several contraindications related to high peri-procedural bleeding and cancer dissemination risk, particularly in HCC patients. Conversely, surgical shunts afford full control of the operating site, minimizing risks. In other words, when TIPSS is contraindicated, surgical portosystemic shunts are still an option.

Expanding liver resection to patients with CSPH serves as both a downstaging strategy before LT and the best alternative for those ineligible for LT, potentially enhancing overall survival in this population[2,72].

Technical aspects of liver resection with portocaval shunt

In liver surgery in general, but even more so in HCC, it is necessary to consider the extent of hepatic resection (minor resection versus major resection) based on the number of liver segments to be removed. It is now clear that preoperative assessment of hepatic resection safety relies on FRL volume and liver function, but safety limits for hepatic resection remain a debated issue in the literature. In the scenario we have described, and based on previous evidence, we suggest performing a surgical shunt when hepatic resection in a cirrhotic patient exceeds 40% of the total liver volume (FRL < 60%)[101].

A different issue concerns the theme of anatomical resections compared to non-anatomical resections. The evidence available so far suggests that non-anatomical hepatic resection can lead to an ischemic area in the residual part of the adjacent liver with a higher amount of debris from the resection edge; this increases the risk of infectious complications in the postoperative course[102]. The cirrhotic patient with portal hypertension is more exposed and susceptible to infectious events, so it is useful to minimize this risk in every phase, including the surgical procedure. Since anatomical resection is associated with less debris from the resection site, we recommend this type of procedure when deciding to perform a surgical portosystemic shunt.

One potential drawback of expanding the HCC resection pool through liver resection preceded by a surgical portocaval shunting is the requirement for an open abdomen procedure. However, minimally invasive approaches for HCC resection in cirrhotic patients have shown a more favorable outcome, with lower rates of blood transfusion and complications compared to open surgery[103,104]. Nevertheless, in highly selected cases where clinically significant portal hypertension (CSPH) limits access to liver resection as a potentially curative treatment or as part of a downstaging protocol, performing a calibrated portocaval shunt before liver resection has been described[86]. Our group has demonstrated the safety and effectiveness of this technique in selected cases, as evidenced by our case series results [Table 1] [Figure 2]. Remarkably, a patient underwent LT four years after liver resection and remains free of HCC recurrence, even eight years post-surgery (four years post-LT).

Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome

Figure 2. Kaplan-Meier survival curves of 15 HCC patients who underwent liver resection with H-graft portocaval shunt. Overall survival rates at 1, 2, and 3 years were 84.8%, 67.9%, and 33.9%, respectively (unpublished data, Author’s personal experience).

Table 1

Case series of 15 liver resections for HCC on cirrhosis with portocaval shunt during surgery. Demographic characteristics, disease burden, type of surgery, and postoperative outcomes. (Unpublished data, Author’s personal experience)

Characteristicn = 151
Age65.61 (60.38, 67.77)
Female5 (33.33%)
ASA Grade 3 *missing8 (66.67%) *3
Child-Pugh B2 (13.33%)
MELD7.80 (7-9)
Alpha-Fetoprotein (ug/L)38.60 (8.20, 2,109.00)
Platelets count (109/L)114.00 (75.50, 137.00)
Diameter of largest lesion (mm)75.00 (50.00, 80.00)
Number of lesions1 (1-3.75)
Major resection12 (80.00%)
Anatomical resection14 (93.33%)
LOS (days)11 (9.00, 20.00)
Clavien-Dindo 36 (40.00%)
Ascites8 (53.33%)
AKI2 (13.33%)
HE0 (0.00%)
Postoperative PVT2 (13.33%)
PHLF (ISGLS definition)4 (26.6%)
PHLF grading
● A
● B
● C

● 1/4 (25%)
● 2/4 (50%)
● 1/4 (25%)
90-Day Mortality2 (13.33%)

Surgical technique

H-graft portocaval shunt

Surgical exposure is achieved by a transverse upper abdominal or reverse “L” incision. Retrograde cholecystectomy is performed, and the hepatoduodenal ligament is approached. Dissection of the retro-portal lymph nodes is carried out to expose the portal vein and common bile duct. Careful dissection is carried out to allow for medial retraction of the common bile duct, and the right hepatic artery, in case of aberrant anatomy of the latter. The axis of the portocaval shunt and the portal vein should be parallel for the technical success of the shunt. Hence, an oblique incision should be made on the inferior vena cava (IVC). Caudate lobectomy or transection of the caudate process might be required to expose a sufficient length of the IVC and to achieve the desirable orientation, which, along with sufficient mobility of the portal vein, assures a tension-free anastomosis. For H-type shunts, we opt for a 0.6 cm diameter Goretex® vascular prosthesis; eventually, free iliac cadaveric vein graft of compatible blood group. In the latter scenario, the cadaveric vein graft is surgically calibrated to 6 mm [Figure 3]. The portocaval shunt is carried with partially occluding vascular clamps (Satinsky) and 6-0 running Prolene suture. Intraoperative Doppler ultrasound is carried out at the completion of the shunt to check the portal, arterial, and shunt flows. If necessary, invasive measurement of portal pressure is carried out (with the use of a 25-G needle attached to a water pressure gauge with saline).

Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome

Figure 3. During surgery in a patient from the authors' series, an intraoperative photograph depicts the H-graft portocaval shunt constructed using a free iliac vein graft. (PV portal vein, PCS portocaval shunt, IVC inferior vena cava).

Pathophysiological consequences of the surgical portacaval shunt

The surgical portocaval shunt presents certain pathophysiological consequences owing to its efficacy and rapid hemodynamic alterations. Competition for portal flow between the remnant liver and the shunt may lead to organ failure due to hypoperfusion[105]. This diversion of blood flow into the systemic circulation reduces pressure both at the sinusoidal level and in the portal vein, as well as within the collateral circulation. However, a surgical portosystemic shunt utilized in liver resection may be functionally temporary. As the future liver remnant (FLR) regenerates, the sinusoidal vascular bed re-establishes, potentially leading to spontaneous late thrombosis of the shunt when no longer required. Nevertheless, these benefits may be accompanied by complications such as transient exacerbation of liver function and hepatic encephalopathy, with side-to-side portacaval shunts more prone to such issues compared to H-graft shunts[45,106]. Consequently, the H-graft shunt is the Authors’ procedure of choice.

In cases of persistent encephalopathy unresponsive to medical treatment, closure of the surgical shunt may be considered once liver regeneration is complete[45,105].

CONCLUSIONS

Portal flow diversion and surgical portosystemic shunts in patients with CSPH present an intriguing avenue for expanding the indications for liver resection in select HCC patients once deemed unresectable due to portal hypertension-associated risks of postoperative liver failure. Advanced liver cirrhosis and portal hypertension should not be viewed as absolute contraindications for liver resection. Instead, they warrant individual evaluation for each patient, weighing the survival benefits offered by available treatment options on a case-by-case basis. This evaluation process should occur within a multidisciplinary framework to ensure comprehensive and tailored management strategies.

DECLARATIONS

Authors’ Contributions

Performed the literature research and wrote the paper: Lanari J, Polacco M

Designed the paper and reviewed the final draft: Cillo U

Availability of data and materials

Author data are only available upon appropriate and reasoned request.

Financial support and sponsorship

None.

Conflicts of interest

All authors declared that there are no conflicts of interest.

Ethical approval and consent to participate

Patients’ data were handled in accordance with the ethical guidelines of the 2013 revised Declaration of Helsinki. Each patient signed a consent for every procedure performed in the hospital, and for the collection and use of data anonymously for research and publication purposes, and all procedures were performed in accordance with the Declaration of Istanbul. No one received compensation or was offered any incentive.

Consent for publication

All patients sign an informed consent at the presentation in which they agree to collect and use their personal data anonymously for research purposes.

Copyright

© The Author(s) 2024.

REFERENCES

1. European association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2018;69:182-236.

2. Cillo U. Liver resection is a therapeutic option for highly selected BCLC C patients in the context of an expert multidisciplinary setting. Dig Liver Dis 2013;45:460-1.

3. Ray S, Mehta NN, Golhar A, Nundy S. Post hepatectomy liver failure - A comprehensive review of current concepts and controversies. Ann Med Surg 2018;34:4-10.

4. Glanemann M, Eipel C, Nussler AK, Vollmar B, Neuhaus P. Hyperperfusion syndrome in small-for-size livers. Eur Surg Res 2005;37:335-41.

5. Troisi R, Praet M, de Hemptinne B. Small-for-size syndrome: what is the problem? Liver Transpl 2003;9:S1.

6. Ueno S, Kobayashi Y, Kurita K, Tanabe G, Aikou T. Effect of prior portosystemic shunt on early hepatic hemodynamics and sinusoids following 84% hepatectomy in dogs. Res Exp Med 1995;195:1-8.

7. García-Valdecasas JC, Fuster J, Charco R, et al. Changes in portal vein flow after adult living-donor liver transplantation: does it influence postoperative liver function? Liver Transpl 2003;9:564-9.

8. Eguchi S, Yanaga K, Sugiyama N, Okudaira S, Furui J, Kanematsu T. Relationship between portal venous flow and liver regeneration in patients after living donor right-lobe liver transplantation. Liver Transpl 2003;9:547-51.

9. Marubashi S, Sakon M, Nagano H, et al. Effect of portal hemodynamics on liver regeneration studied in a novel portohepatic shunt rat model. Surgery 2004;136:1028-37.

10. Sato Y, Koyama S, Tsukada K, Hatakeyama K. Acute portal hypertension reflecting shear stress as a trigger of liver regeneration following partial hepatectomy. Surg Today 1997;27:518-26.

11. Rocheleau B, Ethier C, Houle R, Huet PM, Bilodeau M. Hepatic artery buffer response following left portal vein ligation: its role in liver tissue homeostasis. Am J Physiol 1999;277:G1000-7.

12. Lautt WW. Regulatory processes interacting to maintain hepatic blood flow constancy: Vascular compliance, hepatic arterial buffer response, hepatorenal reflex, liver regeneration, escape from vasoconstriction. Hepatol Res 2007;37:891-903.

13. Lautt WW. The 1995 Ciba-Geigy Award Lecture. Intrinsic regulation of hepatic blood flow. Can J Physiol Pharmacol 1996;74:223-33.

14. Gülberg V, Haag K, Rössle M, Gerbes AL. Hepatic arterial buffer response in patients with advanced cirrhosis. Hepatology 2002;35:630-4.

15. Ezzat WR, Lautt WW. Hepatic arterial pressure-flow autoregulation is adenosine mediated. Am J Physiol 1987;252:H836-45.

16. Demetris AJ, Kelly DM, Eghtesad B, et al. Pathophysiologic observations and histopathologic recognition of the portal hyperperfusion or small-for-size syndrome. J Surg Pathol 2006;30:986-93.

17. Man K, Lo CM, Ng IO, et al. Liver transplantation in rats using small-for-size grafts: a study of hemodynamic and morphological changes. Arch Surg 2001;136:280-5.

18. Man K, Fan ST, Lo CM, et al. Graft injury in relation to graft size in right lobe live donor liver transplantation: a study of hepatic sinusoidal injury in correlation with portal hemodynamics and intragraft gene expression. Ann Surg 2003;237:256-64.

19. Clavien PA, Petrowsky H, DeOliveira ML, Graf R. Strategies for safer liver surgery and partial liver transplantation. N Engl J Med 2007;356:1545-59.

20. Zhou Z, Xu M, Lin N, et al. Associating liver partition and portal vein ligation for staged hepatectomy versus conventional two-stage hepatectomy: a systematic review and meta-analysis. World J Surg Oncol 2017;15:227.

21. Lang H. ALPPS - Beneficial or detrimental? Surg Oncol 2020;33:249-53.

22. Kawaguchi Y, Lillemoe HA, Vauthey JN. Dealing with an insufficient future liver remnant: Portal vein embolization and two-stage hepatectomy. J Surg Oncol 2019;119:594-603.

23. Simoneau E, Hassanain M, Shaheen M, et al. Portal vein embolization and its effect on tumour progression for colorectal cancer liver metastases. Br J Surg 2015;102:1240-9.

24. Schnitzbauer AA, Lang SA, Goessmann H, et al. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings. Ann Surg 2012;255:405-14.

25. Schadde E, Ardiles V, Slankamenac K, et al. ALPPS offers a better chance of complete resection in patients with primarily unresectable liver tumors compared with conventional-staged hepatectomies: results of a multicenter analysis. World J Surg 2014;38:1510-9.

26. Aloia TA, Vauthey JN. Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): what is gained and what is lost? Ann Surg 2012;256:e9; author reply e16-9.

27. D'Haese JG, Neumann J, Weniger M, et al. Should ALPPS be used for liver resection in intermediate-stage HCC? Ann Surg Oncol 2016;23:1335-43.

28. Oldhafer KJ, Donati M, Jenner RM, Stang A, Stavrou GA. ALPPS for patients with colorectal liver metastases: effective liver hypertrophy, but early tumor recurrence. World J Surg 2014;38:1504-9.

29. Chia DKA, Yeo Z, Loh SEK, Iyer SG, Madhavan K, Kow AWC. ALPPS for hepatocellular carcinoma is associated with decreased liver remnant growth. J Gastrointest Surg 2018;22:973-80.

30. Schadde E, Ardiles V, Robles-Campos R, et al. ALPPS Registry Group. Early survival and safety of ALPPS: first report of the international ALPPS registry. Ann Surg 2014;260:829-36; discussion 836-8.

31. Chan ACY, Chok K, Dai JWC, Lo CM. Impact of split completeness on future liver remnant hypertrophy in associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) in hepatocellular carcinoma: complete-ALPPS versus partial-ALPPS. Surgery 2017;161:357-64.

32. Vennarecci G, Ferraro D, Tudisco A, et al. The ALPPS procedure: hepatocellular carcinoma as a main indication. An Italian single-center experience. Updates Surg 2019;71:67-75.

33. Kiuchi T, Kasahara M, Uryuhara K, et al. Impact of graft size mismatching on graft prognosis in liver transplantation from living donors. Available from: http://journals.lww.com/00007890-199901270-00024 [Last accessed on 12 Mar 2024].

34. Xu HS, Pruett TL, Jones RS. Study of donor-recipient liver size match for transplantation. Ann Surg 1994;219:46-50.

35. Sugawara Y, Makuuchi M, Takayama T, et al. Small-for-size grafts in living-related liver transplantation. J Am Coll Surg 2001;192:510-3.

36. Wang HS, Ohkohchi N, Enomoto Y, et al. Excessive portal flow causes graft failure in extremely small-for-size liver transplantation in pigs. World J Gastroenterol 2005;11:6954-9.

37. Hibi T, Kitagawa Y. Small-for-size syndrome in LT. Clin Liver Dis 2017;10:93-6.

38. Nardo B, Montalti R, Puviani L, et al. Portal vein arterialization in a patient with acute liver failure. Transplantation 2005;79:851-2.

39. Fan YD, Praet M, Van Huysse J, Lelie B, De Hemptinne B. Effects of portal vein arterialization on liver regeneration after partial hepatectomy in the rat. Liver Transpl 2002;8:146-52.

40. Ito T, Kiuchi T, Yamamoto H, et al. Changes in portal venous pressure in the early phase after living donor liver transplantation: pathogenesis and clinical implications. Transplantation 2003;75:1313-7.

41. Lo CM, Liu CL, Fan ST. Portal hyperperfusion injury as the cause of primary nonfunction in a small-for-size liver graft-successful treatment with splenic artery ligation. Liver Transpl 2003;9:626-8.

42. Yan L, Wang W, Chen Z, et al. Small-for-size syndrome secondary to outflow block of the segments V and VIII anastomoses--successful treatment with trans-splenic artery embolization: a case report. Transplant Proc 2007;39:1699-703.

43. Abdalla EK, Barnett CC, Doherty D, Curley SA, Vauthey JN. Extended hepatectomy in patients with hepatobiliary malignancies with and without preoperative portal vein embolization. Arch Surg 2002;137:675-80; discussion 680.

44. Adam R, Diamond T, Bismuth H. Partial portacaval shunt: renaissance of an old concept. Surgery 1992;111:610-6.

45. Batignani G, Vizzutti F, Rega L, et al. Small diameter H-graft porta-caval shunt performed at different stages of liver disease. Hepatobiliary Pancreat Dis Int 2004;3:516-21.

46. Hu HJ, Xu GL, Li JS, Yang SG, Chai ZP, Xu RN. Small-diameter prosthetic H-graft portacaval shunts in the treatment of portal hypertension. Chin Med J 2004;117:195-8.

47. Del Guercio LR, Cohn JD, Kazarian KK, Kinkhabwalla M. A shunt equation for estimating the splenic component of portal hypertension. Am J Surg 1978;135:70-5.

48. Sax FL, Cooperman AM. Bleeding esophageal varices. Surg Clin North Am 1981;61:209-19.

49. Brand M, Prodehl L, Ede CJ. Surgical portosystemic shunts versus transjugular intrahepatic portosystemic shunt for variceal haemorrhage in people with cirrhosis. Cochrane Database Syst Rev 2018;10:CD001023.

50. European Association for the Study of the Liver. EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis. J Hepatol 2018;69:406-60.

51. Starzl TE, Porter KA, Francavilla A. The Eck fistula in animals and humans. Curr Probl Surg 1983;20:687-752.

52. Rosemurgy AS, Zervos EE. Management of variceal hemorrhage. Curr Probl Surg 2003;40:263-343.

53. Wolff M, Kalff JC, Textor J, Hirner A. [Surgery for portal hypertension and transjugular intrahepatic portosystemic shunts in Germany: results of a national survey]. Chirurg 1999;70:447-52.

54. Mitra SK, Rao KL, Narasimhan KL, et al. Side-to-side lienorenal shunt without splenectomy in noncirrhotic portal hypertension in children. J Pediatr Surg 1993;28:398-401; discussion 401.

55. Mercado MA, Orozco H, Guillén-Navarro E, et al. Small-diameter mesocaval shunts: a 10-year evaluation. J Gastrointest Surg 2000;4:453-7.

56. Glowka TR, Kalff JC, Manekeller S. Update on shunt surgery. Visc Med 2020;36:206-11.

57. di Francesco F, Grimaldi C, de Ville de Goyet J. Meso-rex bypass--a procedure to cure prehepatic portal hypertension: the insight and the inside. J Am Coll Surg 2014;218:e23-36.

58. Wolff M, Hirner A. Surgical treatment of portal hypertension. Zentralbl Chir 2005;130:238-45.

59. Henderson JM, Boyer TD, Kutner MH, et al. DIVERT Study Group. Distal splenorenal shunt versus transjugular intrahepatic portal systematic shunt for variceal bleeding: a randomized trial. Gastroenterology 2006;130:1643-51.

60. Khaitiyar JS, Luthra SK, Prasad N, Ratnakar N, Daruwala DK. Transjugular intrahepatic portosystemic shunt versus distal splenorenal shunt--a comparative study. Hepatogastroenterology 2020;47:492-7.

61. Lee M, Kim SK, Chung YE, et al. Portal venous perfusion steal causing graft dysfunction after orthotopic liver transplantation: serial imaging findings in a successfully treated patient. Ultrasonography 2016;35:78-82.

62. Lee SG, Moon DB, Ahn CS, et al. Ligation of left renal vein for large spontaneous splenorenal shunt to prevent portal flow steal in adult living donor liver transplantation. Transpl Int 2007;20:45-50.

63. Castillo-Suescun F, Oniscu GC, Hidalgo E. Hemodynamic consequences of spontaneous splenorenal shunts in deceased donor liver transplantation. Liver Transpl 2011;17:891-5.

64. Rosemurgy AS, Bloomston M, Clark WC, Thometz DP, Zervos EE. H-graft portacaval shunts versus TIPS: ten-year follow-up of a randomized trial with comparison to predicted survivals. Ann Surg 2005;241:238-46.

65. Rosemurgy AS, Frohman HA, Teta AF, Luberice K, Ross SB. Prosthetic H-graft portacaval shunts vs transjugular intrahepatic portasystemic stent shunts: 18-year follow-up of a randomized trial. J Am Coll Surg 2012;214:445-53; discussion 453.

66. Llovet JM, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999;19:329-38.

67. Vitale A, Morales RR, Zanus G, et al. Barcelona clinic liver cancer staging and transplant survival benefit for patients with hepatocellular carcinoma: a multicentre, cohort study. Lancet Oncol 2011;12:654-62.

68. Zhang ZY, Dong KS, Zhang EL, Zhang LW, Chen XP, Dong HH. Resection might be a meaningful choice for hepatocellular carcinoma with portal vein thrombosis: A systematic review and meta-analysis. Medicine 2019;98:e18362.

69. Sangiovanni A, Triolo M, Iavarone M, et al. Multimodality treatment of hepatocellular carcinoma: How field practice complies with international recommendations. Liver Int 2018;38:1624-34.

70. Wehling C, Dill MT, Olkus A, et al. Treatment stage migration and treatment sequences in patients with hepatocellular carcinoma: drawbacks and opportunities. J Cancer Res Clin Oncol 2021;147:2471-81.

71. Marrero JA, Kulik LM, Sirlin CB, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the american association for the study of liver diseases. Hepatology 2018;68:723-50.

72. Vitale A, Farinati F, Pawlik TM, et al. The concept of therapeutic hierarchy for patients with hepatocellular carcinoma: A multicenter cohort study. Liver Int 2019;39:1478-89.

73. Vitale A, Cabibbo G, Iavarone M, et al. HCC Special Interest Group of the Italian Association for the Study of the Liver. Personalised management of patients with hepatocellular carcinoma: a multiparametric therapeutic hierarchy concept. Lancet Oncol 2023;24:e312-22.

74. Roayaie S, Jibara G, Tabrizian P, et al. The role of hepatic resection in the treatment of hepatocellular cancer. Hepatology 2015;62:440-51.

75. Mazzaferro V, Regalia E, Doci R, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996;334:693-9.

76. Duvoux C, Roudot-Thoraval F, Decaens T, et al. Liver Transplantation French Study Group. Liver transplantation for hepatocellular carcinoma: a model including α-fetoprotein improves the performance of Milan criteria. Gastroenterology 2012;143:986-94.e3; quiz e14.

77. Toso C, Trotter J, Wei A, et al. Total tumor volume predicts risk of recurrence following liver transplantation in patients with hepatocellular carcinoma. Liver Transpl 2008;14:1107-15.

78. Lee SG, Hwang S, Moon DB, et al. Expanded indication criteria of living donor liver transplantation for hepatocellular carcinoma at one large-volume center. Liver Transpl 2008;14:935-45.

79. Mazzaferro V, Sposito C, Zhou J, et al. Metroticket 2.0 model for analysis of competing risks of death after liver transplantation for hepatocellular carcinoma. Gastroenterology 2018;154:128-39.

80. Cillo U, Vitale A, Polacco M, Fasolo E. Liver transplantation for hepatocellular carcinoma through the lens of transplant benefit. Hepatology 2017;65:1741-8.

81. Ishizawa T, Hasegawa K, Aoki T, et al. Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology 2008;134:1908-16.

82. Zhong JH, Ke Y, Gong WF, et al. Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma. Ann Surg 2014;260:329-40.

83. Cucchetti A, Ercolani G, Vivarelli M, et al. Is portal hypertension a contraindication to hepatic resection? Ann Surg 2009;250:922-8.

84. Azoulay D, Ramos E, Casellas-Robert M, et al. Liver resection for hepatocellular carcinoma in patients with clinically significant portal hypertension. JHEP Rep 2021;3:100190.

85. Citterio D, Facciorusso A, Sposito C, Rota R, Bhoori S, Mazzaferro V. Hierarchic interaction of factors associated with liver decompensation after resection for hepatocellular carcinoma. JAMA Surg 2016;151:846-53.

86. Polacco M, Vitale A, Valmasoni M, et al. Liver resection associated with mini porto-caval shunt as salvage treatment in patients with progression of hepatocellular carcinoma before liver transplantation: a case report. Transplant Proc 2010;42:1378-80.

87. Gil A, Martínez-Regueira F, Hernández-Lizoain JL, et al. The role of transjugular intrahepatic portosystemic shunt prior to abdominal tumoral surgery in cirrhotic patients with portal hypertension. Eur J Surg Oncol 2004;30:46-52.

88. Schwartz SI. Biliary tract surgery and cirrhosis: a critical combination. Surgery 1981;90:577-83.

89. Garrison RN, Cryer HM, Howard DA, Polk HC Jr. Clarification of risk factors for abdominal operations in patients with hepatic cirrhosis. Ann Surg 1984;199:648-55.

90. Rajesh S, George T, Philips CA, et al. Transjugular intrahepatic portosystemic shunt in cirrhosis: An exhaustive critical update. World J Gastroenterol 2020;26:5561-96.

91. Liu J, Wehrenberg-Klee EP, Bethea ED, Uppot RN, Yamada K, Ganguli S. Transjugular intrahepatic portosystemic shunt placement for portal hypertension: meta-analysis of safety and efficacy of 8 mm vs. 10 mm stents. Gastroenterol Res Pract 2020;2020:9149065.

92. Vizzutti F, Schepis F, Arena U, et al. Transjugular intrahepatic portosystemic shunt (TIPS): current indications and strategies to improve the outcomes. Intern Emerg Med 2020;15:37-48.

93. Menahem B, Lubrano J, Desjouis A, Lepennec V, Lebreton G, Alves A. Transjugular intrahepatic portosystemic shunt placement increases feasibility of colorectal surgery in cirrhotic patients with severe portal hypertension. Dig Liver Dis 2015;47:81-4.

94. Nacif LS, Zanini LY, Sartori VF, et al. Intraoperative surgical portosystemic shunt in liver transplantation: systematic review and meta-analysis. Ann Transplant 2018;23:721-32.

95. Tabchouri N, Barbier L, Menahem B, et al. Original study: transjugular intrahepatic portosystemic shunt as a bridge to abdominal surgery in cirrhotic patients. J Gastrointest Surg 2019;23:2383-90.

96. Pizanias M, Kontis E, Prassas E, Srinivasan P, Prachalias A. Surgical portosystemic shunts to facilitate major intrabdominal surgery. Hepatobiliary Pancreat Dis Int 2019;18:488-90.

97. Sen I, Yohanathan L, Kärkkäinen JM, Nagorney DM. Current indications and long-term outcomes of surgical portosystemic shunts in adults. J Gastrointest Surg 2021;25:1437-44.

98. Lahat E, Lim C, Bhangui P, et al. Transjugular intrahepatic portosystemic shunt as a bridge to non-hepatic surgery in cirrhotic patients with severe portal hypertension: a systematic review. HPB 2018;20:101-9.

99. Pierce DS, Sperry J, Nirula R. Cost-effective analysis of transjugular intrahepatic portosystemic shunt versus surgical portacaval shunt for variceal bleeding in early cirrhosis. Am Surg 2011;77:169-73.

100. Sliwinski S, Trojan J, Mader C, Vogl T, Bechstein W. Liver resection after transjugular portosystemic stent shunt (TIPSS). Z Gastroenterol 2023;61:390-3.

101. Guglielmi A, Ruzzenente A, Conci S, Valdegamberi A, Iacono C. How much remnant is enough in liver resection? Dig Surg 2012;29:6-17.

102. Gotohda N, Cherqui D, Geller DA, et al. Expert consensus guidelines: how to safely perform minimally invasive anatomic liver resection. J Hepatobiliary Pancreat Sci 2022;29:16-32.

103. Xing L, Guo HB, Kan JL, et al. Clinical outcome of open surgery versus laparoscopic surgery for cirrhotic hepatocellular carcinoma patients: a meta-analysis. Eur J Gastroenterol Hepatol 2020;32:239-45.

104. Ciria R, Gomez-Luque I, Ocaña S, et al. A Systematic Review and Meta-Analysis Comparing the Short- and Long-Term Outcomes for Laparoscopic and Open Liver Resections for hepatocellular carcinoma: updated results from the european guidelines meeting on laparoscopic liver surgery, southampton, UK, 2017. Ann Surg Oncol 2019;26:252-63.

105. Takada Y, Ueda M, Ishikawa Y, et al. End-to-side portocaval shunting for a small-for-size graft in living donor liver transplantation. Liver Transpl 2004;10:807-10.

106. Capussotti L, Vergara V, Polastri R, Bouzari H, Galatola G. Liver function and encephalopathy after partial vs direct side-to-side portacaval shunt: a prospective randomized clinical trial. Surgery 2000;127:614-21.

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Lanari J, Polacco M, Cillo U. Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome. Hepatoma Res 2024;10:11. http://dx.doi.org/10.20517/2394-5079.2023.97

AMA Style

Lanari J, Polacco M, Cillo U. Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome. Hepatoma Research. 2024; 10: 11. http://dx.doi.org/10.20517/2394-5079.2023.97

Chicago/Turabian Style

Jacopo Lanari, Marina Polacco, Umberto Cillo. 2024. "Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome" Hepatoma Research. 10: 11. http://dx.doi.org/10.20517/2394-5079.2023.97

ACS Style

Lanari, J.; Polacco M.; Cillo U. Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome. Hepatoma. Res. 2024, 10, 11. http://dx.doi.org/10.20517/2394-5079.2023.97

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