Dong Zhao,Yi-Ming Huang,Zi-Ming Liang,Kang-Jun Zhang,Tai-Shi Fang,Xu Yan,Xin Jin,Yi Zhang,Jian-Xin Tang,Lin-Jie Xie,Xin-Chen Zeng

Dong Zhao,Yi-Ming Huang,Zi-Ming Liang,Kang-Jun Zhang,Tai-Shi Fang,Xu Yan,Xin Jin,Yi Zhang,Jian-Xin Tang,Lin-Jie Xie,Xin-Chen Zeng,Department of Liver Surgery and Organ Transplantation Center,The Third People’s Hospital of Shenzhen,The Second Affiliated Hospital of Southern University of Science and Technology,National Clinical Research Center for Ⅰnfectious Disease,Shenzhen 518000,Guangdong Province,China

Abstract BACKGROUND Thrombectomy and anatomical anastomosis (TAA) has long been considered the optimal approach to portal vein thrombosis (PVT) in liver transplantation (LT).However,TAA and the current approach for non-physiological portal reconstructions are associated with a higher rate of complications and mortality in some cases.AIM To describe a new choice for reconstructing the portal vein through a posterior pancreatic tunnel (RPVPPT) to address cases of unresectable PVT.METHODS Between August 2019 and August 2021,245 adult LTs were performed.Forty-five (18.4%) patients were confirmed to have PVT before surgery,among which seven underwent PV reconstruction via the RPVPPT approach.We retrospectively analyzed the surgical procedure and postoperative complications of these seven recipients that underwent PV reconstruction due to PVT.RESULTS During the procedure,PVT was found in all the seven cases with significant adhesion to the vascular wall and could not be dissected.The portal vein proximal to the superior mesenteric vein was damaged in one case when attempting thrombolectomy,resulting in massive bleeding.LT was successfully performed in all patients with a mean duration of 585 min (range 491-756 min) and mean intraoperative blood loss of 800 mL (range 500-3000 mL).Postoperative complications consisted of chylous leakage (n = 3),insufficient portal venous flow to the graft (n = 1),intra-abdominal hemorrhage (n = 1),pulmonary infection (n = 1),and perioperative death (n = 1).The remaining six patients survived at 12-17 mo follow-up.CONCLUSION The RPVPPT technique might be a safe and effective surgical procedure during LT for complex PVT.However,follow-up studies with large samples are still warranted due to the relatively small number of cases.

Key Words: Liver transplantation;Portal vein thrombosis;Portal vein reconstruction;Retropancreatic tunnel;Computer tomography angiography;Three-dimensional visualization

INTRODUCTION

Liver transplantation (LT) remains the mainstay treatment for end-stage liver disease.However,the incidence of portal vein thrombosis (PVT) in patients on the waiting list for transplantation has been reported to range from 5% to 26%.Due to the complexity of treatment techniques,PVT has long been regarded as a contraindication of LT until the 1980s[1-3].However,the past decade has witnessed unprecedented progress achieved in surgical techniques,leading to the advent of many surgical approaches for recipients with PVT,including physiological portal reconstruction (such as thrombectomy,interposition venous grafts,and mesoportal jump grafts) and non-physiological portal reconstruction (such as cavoportal hemitransposition,renoportal anastomosis,and arterialization of PV flow)[4,5].Importantly,physiological reconstruction can restore the anatomical structure of the portal venous system and ensure adequate blood flow to the graft.In contrast,non-physiological reconstruction exhibits limited ability to resolve portal hypertension due to the inability to drain visceral blood into the liver,resulting in a higher incidence of postoperative complications and mortality than physiological reconstruction[6-10].Most recipients with PVT can undergo thrombectomy and anatomical anastomosis (TAA),yielding satisfactory results.However,in clinical practice,some patients with PVT present with organized thrombi adhering to vascular walls that cannot be completely removed intraoperatively,compromising blood flow to the graft.Non-physiological reconstruction methods are indicated in such cases,including portal-renal vein anastomosis and bypass,portal vena cava semi-transposition,and portal vein arterialization.An increasing body of evidence suggests that this approach is ineffective and might lead to an insufficient blood supply to the portal vein or postoperative hepatic encephalopathy[10-12].

Kasaharaet al[13] reported a “pullout technique” for portal vein reconstruction in ten pediatric cases of LT.The portal vein was first pulled out from the back of the pancreas and resected.Then the portal vein reconstruction was completed by bridging the back of the pancreas with allograft or autologous blood vessels.However,this technique has not been widely used,and no relevant reports of its application during adult LT have been documented.Therefore,based on the “pullout technique”,our center explored the technique of reconstructing the portal vein through a posterior pancreatic tunnel (RPVPPT) in adult LT recipients where PVT could not be resolved.

MATERIALS AND METHODS

General clinical data

A retrospective analysis was performed on 245 cases of LT at Shenzhen Third People’s Hospital from August 2019 to August 2021.PVT was documented in 45 cases,of which 7 underwent RPVPPT for PVT and portal vein reconstruction (6 males,1 female;age 48-65 years,mean 54 years).All patients in this study underwent LT with the approval of the Ethics Committee of Shenzhen Third People’s Hospital,and livers were donated after the death of healthy citizens.

Preoperative assessment method

Before surgery,each patient underwent Doppler ultrasound and abdominal computed tomography angiography (CTA) to determine the incidence of complications such as PVT.Three-dimensional (3D) visualization models were reconstructed according to the DICOM format data of CTA,as previously described in the literature[14],and surgery was simulated on the model.

Main surgical methods of RPVPPT technique

Dissection of the hepatic hilum:First,the varicose veins of the hepatic hilum were separated and ligated successively,the common hepatic artery and the proper hepatic artery were dissected,and the left hepatic artery and the right hepatic artery were separated.The main portal vein was dissected from the caudal to the cephalad direction along the trunk to the left and right branches of the portal vein.Finally,the bile duct was isolated and severed near the hilum.

Establishment of the retropancreatic tunnel:First,the main portal vein was dissected from the cephalad to the caudal direction,and the left gastric vein (coronary vein) and the portal vein branch vessels were ligated successively.When the upper edge of the pancreas was reached,dissection started from the lower edge of the pancreas.The superior mesenteric vein (SMV) and splenic vein (SpV) were first separated and lifted with vascular slings.Then,dissection continued from the back of the pancreas to the cephalic side along the main portal vein to establish a retropancreatic tunnel.Subsequently,the pancreas was lifted with a vascular sling or a fine urinary catheter.Finally,the portal vein and its tributary branches behind the pancreas were completely severed and “naked”.

Resection of the main portal vein of the recipient:The severed main portal vein was pulled out from the retropancreatic tunnel to the lower edge of the pancreas.The main portal vein containing the thrombus was removed after interrupting blood flow in the SMV and SpV.If the left gastric vein drained into the SpV or the superior mesenteric-portal vein (SMPV) confluence,it was ligated and severed first to avoid insufficient portal venous flow to the graft due to blood shunting.

Portal vein reconstruction:After the donor-recipient inferior vena cava anastomosis was completed,the donor’s portal vein was pulled to the lower edge of the pancreas through the retropancreatic tunnel,and the portal vein reconstruction was conducted at the SMPV confluence (Figure 1).

Main evaluation indicators

The clinical data of each LT recipient with PVT were collected,including the medical history and laboratory,imaging,and 3D reconstruction results.The surgical methods and operation-related indicators were analyzed,including the operation time,bleeding volume,amount of blood transfusion,and surgical complications.

RESULTS

General clinical data

Patients with PVT included in the present study were cases with a preoperative diagnosis of decompensated hepatitis B virus (HBV)-related cirrhosis (n= 3) and hepatocellular carcinoma with decompensated HBV-related cirrhosis (n= 4).Five cases had a history of gastrointestinal bleeding before the operation.All patients underwent preoperative 3D reconstructions to visually assess blood vessels and simulate surgery,and LT was successfully conducted.The mean operation time was 585 min (range 491-756 min),and the mean intraoperative blood loss was 800 mL (range 500-3000 mL).More details are provided in Table 1.

Table 1 Basic demographics and clinical data of cases with portal vein thrombosis (n = 7)

Changes in the structure of the portal vein system

Anatomical structure of the PVT:One patient presented with complete portal vein occlusion with thrombosis proximal to the SMPV confluence,four cases with portal vein stenosis greater than 70% and thrombosis extending to the SMPV confluence,and two cases with portal vein stenosis greater than 70% and thrombosis extending to the proximal segment of the SMV.All seven patients with PVT presented with organized thrombi that could be completely removed intraoperatively during surgery.Moreover,the proximal portal vein was damaged near the SMPV confluence in one case when attempting thrombolectomy,resulting in massive bleeding.

Anatomical structure of varicose vessels:The left gastric vein drained into the main portal vein (n= 3),SpV (n= 3),and SMPV confluence (n= 1),and the maximum diameter of the left gastric vein was greater than 1 cm in four cases.All cases presented with esophageal and gastric fundal varices and splenorenal shunt;the maximum diameter of the splenorenal shunt was 24 mm,and an umbilical vein opening was found in two cases.More details are provided in Table 2.

Surgical results and complications

Portal vein reconstruction and LT were successfully conducted in all cases,with patent and sufficient portal vein flow documented by intraoperative color Doppler ultrasonography.Six patients recovered smoothly after the surgery,and one patient died.The liver and coagulation function indicators are shown in Tables 3 and 4.Postoperative complications consisted of chylous leakage (n= 3),insufficient portal venous flow to the graft (n= 1),intra-abdominal hemorrhage (n= 1),pulmonary infection (n= 1),and perioperative death (n= 1).

Table 2 Vascular anatomical changes in the portal vein system of cases with portal vein thrombosis (n = 7)

Table 3 Laboratory examination indicators on postoperative day 7

Table 4 Laboratory examination indicators on postoperative day 14

Management of postoperative complications included conservative medical treatment for chylous leaks and antibiotics for pulmonary infection.In cases of insufficient portal venous flow,embolization of splenorenal shunt vessels under digital subtraction angiography (DSA) was used to improve portal venous blood flow (Figure 2).An exploratory laparotomy was performed on a patient with postoperative intra-abdominal bleeding (postoperative day 7) that was attributed to multiple blood vessels at the lower margin of the pancreas.Liver ischemia and hypoxia occurred due to hemorrhagic shock after surgery.The patient died 15 d after LT due to liver failure.At 12-17 mo follow-up,six of the seven cases in this study survived.

DISCUSSION

Management of PVT

PVT refers to thrombosis occurring in the main portal vein and its associated venous system (SMV,inferior mesenteric vein,and SpV).It is one of the most common complications of end-stage liver disease,with an incidence of about 5%-26%[1,15,16].In the present study,the incidence of PVT was 18.4% (45/245).PVT has long been considered a contraindication for LT due to limited surgical techniques and poor understanding of PVT[17].With significant inroads achieved in recent years,various innovative surgical approaches are now available.

Hibiet al[10] performed LT in 174 cases of PVT,among which 83 (47.7%) and 91 (52.3%) presented with complete and partial PVT,respectively.In terms of portal vein reconstruction,149 cases underwent physiological reconstruction [thrombolectomy (n= 123),interposition vein grafts (n= 16),and mesoportal jump grafts (n= 10)].There were 25 cases of non-physiological reconstruction [cavoportal hemitranspositions (n= 18),renoportal anastomoses (n= 6),and arterialization (n= 1)].The study found that the non-physiological group suffered a significantly increased incidence of rethrombosis of the portomesenteric veins and gastrointestinal bleeding,with a dismal 10-year overall survival rate of 42% (vsno PVT,61%;P= 0.002 andvsPVT: Physiological group,55%;P= 0.043).Rodríguez-Castroet al[12] reported that of 25753 liver transplants,2004 were performed in patients with PVT (7.78%),and complete thrombosis was observed in nearly 50%.TAA was performed in 75% of patients;other techniques included venous graft interposition and portocaval hemitransposition.It was found that PVT significantly increased post-LT mortality at 30 d (10.5%) and 1 year (18.8%) when compared to patients without PVT (7.7% and 15.4%,respectively).Moreover,rethrombosis occurred in up to 13% of patients with complete PVT,whereby no preventive strategies were used,leading to increased morbidity and mortality.In the present study,there was no recurrence of PVT,but one patient had portal venous insufficiency after LT.Accordingly,the optimal approach for portal vein reconstruction is the restoration of the physiological anatomy of the portal vein system while ensuring adequate portal venous flow[10,18].

At present,no consensus has been reached on the optimal reconstruction approach for different types of PVT during LT.Some scholars have formulated surgical methods according to Yerdel classification criteria[19-21].However,in some cases,this classification criteria cannot be used to guide clinical practice since the Yerdel standard is based on the extent that the thrombus occupies the portal vein lumen and does not take into account adhesion to the blood vessel wall.

Application and precautions of RPVPPT

The RPVPPT technique adopted by our team was mainly applied in patients with PVT contraindicated for routine thrombolectomy during the LT surgery.This approach restores the physiological anatomy of the portal vein system while ensuring adequate portal vein blood flow,which is hypothetically ideal for PVT patients.At 12-17 mo follow-up,six of the seven patients survived,preliminarily validating the feasibility and safety of RPVPPT.

However,severe portal hypertension in this patient population accounts for an increase in varicose vessels around the portal vein,or even cavernous transformation of the portal vein,leading to an increased risk of bleeding during the procedure[22,23].In addition,the RPVPPT technique requires the establishment of a retropancreatic tunnel behind the pancreas in these patients,increasing surgical risks.Accordingly,this surgical approach requires highly skilled surgeons and a transplant team.During the operation,it is recommended to dissect the hepatic hilum along the portal vein to the upper margin of the pancreas and then successively ligate each branch of the portal vein at the lower margin of the pancreas.When separating the lower edge of the pancreas,the SMV and SpV branches should be dissected first,and vascular slings should be placed to lift them for prompt hemostasis during the establishment of the retropancreatic tunnel or the separation of the surrounding tissues of the portal vein.After a successful retropancreatic tunnel is established,lifting the pancreas with a vascular sling or urinary tube is recommended to facilitate portal vein reconstruction (Figure 1).

Figure 1 Main steps of reconstructing the portal vein through the posterior pancreatic tunnel technique during portal vein reconstruction in liver transplantation recipients with complex portal vein thrombosis.

Figure 2 Embolization of large splenorenal shunt under digital subtraction angiography alleviates portal vein insufficiency after liver transplantation.

Intraoperative traction of the pancreas should be as gentle as possible to avoid pancreatic damage and pancreatitis.Based on our experience,we recommend successfully ligating the branches of the blood vessels that merge into the portal vein behind the pancreas.Given that the blood vessels in this region are very thin,hemostasis can be challenging once bleeding occurs.In this regard,given the narrow surgical view,it can be challenging to perform suture hemostasis,and the effect of electrocoagulation is often not satisfactory.In such circumstances,we can only resort to compression hemostasis.In addition,due to the brittleness of pancreatic tissue in patients with portal hypertension and the increase of surface varicose vessels,the risk of hemorrhagic shock is relatively high.Therefore,it is advisable to dissect the lower edge of the pancreas during surgery to prevent postoperative abdominal bleeding.In our study,one patient developed intra-abdominal hemorrhage on postoperative day 7.Exploratory laparotomy revealed that the source of the hemorrhage was at the lower edge of the pancreas,with multiple hemorrhagic foci observed.This finding could be attributed to postoperative pancreatitis since the amylase level in drain fluid from the lower edge of the pancreas was 700 U/L.It is highly likely that the extravasation of pancreatic fluid corroded the blood vessel,thus leading to rupture and bleeding.The patient died of liver failure due to hemorrhagic shock resulting in liver ischemia and hypoxia.Based on our experience,we recommend that the drainage tube should be indwelled at the lower margin of the pancreas and properly fixed.Importantly,the drain fluid amylase level should be assessed regularly after surgery.

During the establishment of the retropancreatic tunnel,the varicose vessels around the portal vein were ligated to create the posterior pancreatic tunnel and reduce the blood shunt of the portal vein system to avoid insufficient portal venous flow to the graft after surgery.However,it is often difficult to ligate splenorenal shunt vascular branches intraoperatively due to their deep location.In some cases,postoperative intervention may be required to manage shunt vessels.In this study,one patient developed insufficient portal venous flow to the graft after surgery,mainly due to significant splenicrenal shunting.DSA showed that most splenic venous flow drained into the inferior vena cava through the shunt rather than the portal vein.After shunt embolization,an immediate improvement in portal vein blood supply was observed.

CONCLUSION

With the increased number of LT cases,PVT has become a major conundrum that may be solved by portal vein reconstruction.The key point of this technique is to ensure sufficient portal venous blood flow and restore the physiological anatomy of the portal vein system as much as possible.The RPVPPT approach adopted in this study meets the above requirements,and our preliminary assessment yielded good results.We substantiated that the RPVPPT technique is a safe and effective surgical procedure in LT for complex PVT.However,follow-up studies with large samples are warranted due to the relatively small number of cases.

ARTICLE HIGHLIGHTS

Research background

Portal vein thrombosis (PVT) poses a great challenge in liver transplantation (LT).It has been established that thrombectomy and anatomical anastomosis (TAA) can restore the physiological anatomy of the portal vein by complete thrombus excision and has been considered the optimal solution to this problem;however,in some cases,PVT cannot be treated by TAA.

Research motivation

We describe our experience of reconstructing the portal vein through a posterior pancreatic tunnel(RPVPPT) to address the issue of unresectable PVT,which may achieve a similar effect to TAA and provide a new approach to solve this intricate clinical problem.

Research objectives

We sought to describe a new strategy of RPVPPT to address cases of unresectable PVT.

Research methods

A retrospective analysis was performed on 245 adult patients that underwent LT from August 2019 to August 2021.Forty-five (18.4%) patients presented with PVT before surgery,among which seven underwent portal vein reconstruction using RPVPPT.Preoperative clinical data,operation-related indicators,and postoperative complications were statistically analyzed.

Research results

During the operation,PVT was found in all seven cases with significant adhesion to the vascular wall and could not be dissected.LT was successfully performed in all patients without serious postoperative complications.At 12-17 mo follow-up,there were six patients who survived.

Research conclusions

The RPVPPT technique can restore the physiological anatomy of the portal vein system through a retropancreatic tunnel,which might be a safe and effective surgical procedure in LT for complex PVT.

Research perspectives

Due to the relatively small number of cases in the study,follow-up studies with large samples are still required.

ACKNOWLEDGEMENTS

We thank the professor Nan Jiang and the patients for cooperating with our investigation.

FOOTNOTES

Author contributions:Zhao D and Huang YM were involved in the conception and design of this study;Zhao D provided administrative support in this study;Tang JX,Zhang KJ,Fang TS,and Zeng XC contributed to the provision of study materials or patients;Liang ZM,Yan X,Jin X,and Xie LJ were involved in the collection and assembly of data;Zhang Y and Huang YM analysed and interpreted the data;and all authors approved this manuscript to publish.

Supported bythe Third People’s Hospital of Shenzhen Scientific Research Project,No.G2021008 and No.G2022008;Shenzhen Key Medical Discipline Construction Fund,No.SZXK079;Shenzhen Science and Technology Research and Development Fund,No.JCYJ20190809165813331 and No.JCYJ20210324131809027.

Institutional review board statement:The study was reviewed and approved by the Third People’s Hospital of Shenzhen Institutional Review Board (Approval No.2022-037-02).

Informed consent statement:All cases involved in this study proved written informed consent.

Conflict-of-interest statement:All the authors report no relevant conflicts of interest for this article.

Data sharing statement:No additional data are available.

Open-Access:This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers.It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BYNC 4.0) license,which permits others to distribute,remix,adapt,build upon this work non-commercially,and license their derivative works on different terms,provided the original work is properly cited and the use is noncommercial.See: https://creativecommons.org/Licenses/by-nc/4.0/

Country/Territory of origin:China

ORCID number:Dong Zhao 0000-0003-3773-721X;Jian-Xin Tang 0000-0003-4416-5336.

S-Editor:Wang JJ

L-Editor:Wang TQ

P-Editor:Wang JJ