Modulation of graft vascular in flow guided by flowmetry and manometry in liver transplantation

See Ching Chan, Chung Mau Lo, Kenneth SH Chok, William W Sharr, Tan To Cheung, Simon HY Tsang, Albert CY Chan and Sheung Tat Fan

Hong Kong, China

Case Report

Modulation of graft vascular in flow guided by flowmetry and manometry in liver transplantation

See Ching Chan, Chung Mau Lo, Kenneth SH Chok, William W Sharr, Tan To Cheung, Simon HY Tsang, Albert CY Chan and Sheung Tat Fan

Hong Kong, China

BACKGROUND:Survival of the partial graft after living donor liver transplantation owes much to its tremendous regenerative ability. With excellent venous outflow capacity, a graft within a wide range of graft-to-standard-liver-volume ratios can cope with portal hypertension that is common in liver transplant recipients. However, when the ratio range is exceeded, modulation of graft vascular inflow becomes necessary for graft survival. The interplay between graft-to-standardliver-volume ratio and portal pressure, in the presence of portosystemic shunt or otherwise, requires individualized modulation of graft portal and arterial inflows. Boosting of portal inflow by shunt ligation can be guided by transonic flowmetry, whereas muting of portal inflow by splenic artery ligation can be monitored by portal electronic manometry.

METHOD:We describe four cases to illustrate the above.

RESULTS:One patient had hepatic artery thrombosis resulting from splenic artery steal syndrome which was the sequela of small-for-size syndrome. Emergency splenic artery ligation and re-anastomosis of the hepatic artery successfully muted the portal inflow and boosted the hepatic arterial inflow. Another patient with portal vein thrombosis underwent thrombendvenectomy. Portal inflow was boosted with ligation of portosystemic shunt, which is often present in these patients with portal hypertension. The coexistence of splenic aneurysm and splenorenal shunt required ligation of both in the third patient. The fourth patient, with portal pressure and flow monitoring, avoided ligation of a coronary vein which became a main portal inflow after portal thrombendvenectomy.

CONCLUSION:Management of graft inflow modulation guided selectively by transonic flowmetry or portal manometry was described.

(Hepatobiliary Pancreat Dis Int 2011; 10: 649-656)

graft; in flow; liver transplantation; modulation

Introduction

The liver is a highly vascular vital organ with a dual portal and arterial inflow. As a replacement spare part in liver transplantation, though orthotopic in location, a liver graft often has to settle in an environment very different from before. In living donor liver transplantation (LDLT), a partial graft is used. It is often less than half of the recipient standard liver volume yet under much higher portal pressure than in its home environment of the donor. This taxes the coping ability of the partial graft to the extreme. Furthermore, there is often coexistence of extensive portosystemic shunts in the case of long-standing portal hypertension. The whole graft used in deceased donor liver transplantation (DDLT) can be functionally large for its size.

Portal inflow, when extensive and inadequate, can compromise graft function and graft survival. We have previously described how portal hypertension after graft implantation was modulated by muting portal inflow by splenic artery ligation.[1]We have also described how a small-for-size graft of 28% of the standard liver volume could still suffer from portal hypoperfusion in the presence of a spontaneous splenorenal shunt. Ligation of the shunt boosted the portal inflow.[2]In order to clarify the concept of modulation of graft inflow according to various clinical situations, here we describe four cases of liver transplantation performed in our hospital to illustrate how optimal graft inflow can be attained for graft survival.

Case reports

Case 1

A 6-year-old girl had undergone the Kasai operation on day 56 after birth for biliary atresia. She remained jaundiced with splenomegaly. Despite repeated endoscopic banding and sclerotherapy, she had repeated bleeding from the esophageal varices. She underwent LDLT using a left liver graft including the middle hepatic vein from her 59-year-old grandmother. The graft was smaller than predicted preoperatively and was only 220 g, corresponding to only 1.2% of her body weight (19 kg). After transplantation, she continued to have jaundice, coagulopathy, and thrombocytopenia. On postoperative day 7, left hepatic artery thrombosis was identified by ultrasonography and confirmed by computed tomography. She thus underwent emergency laparotomy. There was 2lof straw-colored ascitic fluid. The liver graft was swollen, stiff, and with cholestasis (Fig. 1A). The native common hepatic artery, which was proximal to the anastomosis, was discolored (Fig. 1B). After the anastomosis had been taken down, a fresh clot was identified and removed. The splenic artery was 7 mm in diameter and was strongly pulsatile (Fig. 1C). Hepatic artery re-anastomosis was performed under operating microscopy. Portal pressure was measured by electronic manometry via a cannula in the inferior mesenteric vein (Fig. 1D). On temporary clamping of the splenic artery, the portal pressure dropped from 22 mmHg to 15 mmHg. Portal flow assessed by intraoperative ultrasonography also dropped from 1816 mL/min (825 mL/min per 100 g) to 536 mL/min (244 mL/min per 100 g). The hepatic artery flow improved from 34 mL/min to 42 mL/min. These were features of splenic artery steal syndrome. The splenic artery was thus ligated. Her liver function improved subsequently and she was discharged from the hospital on day 19 after LDLT.

Case 2

Fig. 1. A: Left liver graft including the middle hepatic vein on postoperative day 7 with features of cholestasis; B: left hepatic artery thrombosis; C: computed tomography of recipient on postoperative day 7 showing a prominent splenic artery; D: cannulation of inferior mesenteric vein for electronic manometry of portal pressure.

Fig. 2. A: Computed tomography revealed a large coronary vein, moderate splenomegaly, and a prominent splenic vein; B: thrombendvenectomy in the recipient; C: portal flow was only 344 mL/min (39 mL/min per 100 g). Temporary clamping of the coronary vein improved the portal flow to 1.5 L/min (169 mL/min per 100 g); D: temporary clamping of the coronary vein and measurement of portal flow by transonic flowmeter; E: the large coronary vein isolated; F: the coronary vein ligated.

A 54-year-old man, weighing 60 kg with hepatitisB, Child-Pugh C cirrhosis and a 2-cm hepatocellular carcinoma in segment 7, was allocated a deceased donor whole liver graft. He had thrombosis of the portal vein and a large number of varices in the liver hilum (Fig. 2A). The portal vein was exposed near its junction with the splenic vein (Fig. 2B) and thrombendvenectomy was performed (Fig. 2B).[3]A whole liver graft, which weighed 890 g, was implanted. On reperfusion, the portal inflow was only 344 mL/min (39 mL/min per 100 g) (Fig. 2C) as measured by a transonic flowmeter with an ultrasonic probe encircling the main portal vein (Fig. 2D). A large coronary vein was isolated (Fig. 2E). Temporary clamping of the coronary vein improved the portal inflow to 1.5 L/min (169 mL/min per 100 g) (Fig. 2C). The coronary vein was thus ligated (Fig. 2F). He made a satisfactory recovery and was discharged from the hospital on day 11 after transplantation.

Case 3

A 61-year-old man with Child-Pugh C hepatitis B cirrhosis was listed for DDLT. Computed tomography 5 months prior to DDLT showed a splenic artery aneurysm (Fig. 3A) and multiple spontaneous splenorenal shunts (Fig. 3B). He was admitted to the hospital for grade III hepatic encephalopathy a week prior to the DDLT.

On laparotomy, the liver was found to be cirrhotic and shrunken with moderate splenomegaly. There was 400 mL of clear straw-colored ascitic fluid. A portal vein thrombus extending to the splenic vein was present. The splenic artery aneurysm was 8 cm in diameter. After isolation and division of the main portal vein, thrombendvenectomy was performed. Satisfactory portal inflow was ascertained. Total hepatectomy of the native liver was performed.

A whole liver graft weighing 1060 g was implanted with the standard technique into this 54 kg recipient. The splenic artery proximal to the aneurysm was isolated (Fig. 3C). Trial clamping of the splenic artery resulted in very poor portal inflow (228 mL/min; 22 mL/min per 100 g) (Fig. 3D). Simultaneous clamping of the splenorenal shunt improved the portal flow to 720 mL/min (68 mL/min per 100 g) (Fig. 3E). The splenorenal shunt was thus ligated. In order to prevent rupture of the splenic artery aneurysm, the splenic artery was also ligated. He developed right pleural effusion and ascites. The spleen was infarcted and an abscess was formed. The abscess was drained percutaneously. Enterococcus faecium sensitive to vancomycin was cultured. A 4-week course of intravenous vancomycin was administered. He was discharged from the hospital 6 weeks after transplantation.

Case 4

The recipient was a 65-year-old woman with Child-Pugh C cryptogenic cirrhosis. She was complicated with esophageal bleeding varices. Her son volunteered as the liver donor. Volumetric analysis of the son's computed tomography results indicated that his left liver accounted for 40% of her standard liver volume. He thus underwent donor left hepatectomy including the middle hepatic vein but not the caudate lobe. The graft weighed 415 g on the back table and was only 37% of her standard liver volume.[4]The recipient had a body weight of 58 kg and her standard liver volume was 1108 mL.

Fig. 3. A: Preoperative computed tomography showing an 8-cm splenic artery aneurysm; B: preoperative computed tomography showing a spontaneous splenorenal shunt and moderate splenomegaly; C: the proximal portion of the splenic artery which supplied the aneurysm was isolated; D: temporary clamping of the proximal splenic artery; E: simultaneous temporary clamping of the proximal splenic artery and splenic vein which drained into the spontaneous splenorenal shunt.

Fig. 4. A: Preoperative computed tomography showing a thrombus in the proximal main portal vein; B: preoperative computed tomography showing a large coronary vein connected to the main portal vein; C: preoperative computed tomography showing large varices connected to the left phrenic vein; D: computed tomography of the recipient on the first postoperative day showing collapse of the coronary vein and patent graft main portal vein.

Table 1. Reports of splenic artery occlusion

The recipient total hepatectomy of the native liver was unremarkable except that the main portal vein had an organized thrombus with limbs extending into the superior mesenteric vein (Fig. 4A). Partial thrombosis of the portal vein was already evident on preoperative computed tomography. A prominent coronary vein connected with a collateral in the splenic hilum was also evident (Fig. 4B). The collateral drained into the territories of the left phrenic vein and then the inferior vena cava (Fig. 4C). After delivery of the native liver, the thrombus was excised. Good portal blood flow was attained on release of the vascular clamp on the portal vein. The left liver graft was implanted. In view of the multiple varices along the lesser curvature of the stomach and the presence of a prominent coronary vein, venous shunting of portal blood was anticipated. Portal inflow was measured by flowmetry and was 1.8 L/min (434 mL/min per 100 g). The hepatic veinflow was triphasic as documented by intraoperative ultrasonography. The inferior mesenteric vein was isolated but was found to be atretic. Direct measurement of the portal pressure by puncturing the native portal vein with a 21-gauge needle connected to an electronic manometer gave a reading of 11 to 12 mmHg. The isolated coronary vein was temporarily clamped. Portal flow dropped to 900 mL/min (217 mL/min per 100 g) and the portal pressure was only 6 mmHg. In order to maintain adequate portal pressure for graft perfusion,the coronary vein was not ligated.

Table 2. Reports of portosystemic shunting

Fig. 5. Flowmetry- and manometry-guided portal inflow modulation.

Postoperative computed tomography was performed to confirm a patent left hepatic artery. It also showed a collapse of the coronary vein (Fig. 4D). No modulation of graft inflow was performed. She was discharged from the hospital on day 21 after transplantation.

Discussion

These four cases illustrated three indications for and a contraindication to liver graft inflow modulation. While addressing graft inflow issues, venous outflow must not be compromized in the first place. With excellent venous outflow and adequate graft size, portal hypertension of the recipient is often effectively relieved after graft implantation.

Splenic artery ligation

The indications, timing and techniques for splenic artery occlusion, either by embolization or by ligation, vary from center to center (Table 1). However, inflow modulation should be considered in extreme situations where recipient portal hypertension is severe, collaterals are not well developed, or the graft is small-for-size. It has been estimated that occlusion of the splenic artery and ligation of the coronary vein can result in a 52% reduction of portal inflow.[5]The drop in portal pressure is particularly significant in recipients with splenomegaly indicative of pre-existing portal hypertension.[6]Splenic artery ligation can decrease the portal inflow which is fed by the splenic vein[1,7]and boost the hepatic arterial flow. Lautt and Payen et al[8,9]described the effects of changes in portal flow on hepatic arterial flow, now known as the hepatic artery buffer response. Adenosine, a potent vasodilator, is released at a constant rate around terminal hepatic arterioles and portal venules. Portal flow at a high velocity washes out more adenosine, thereby causing hepatic artery vasoconstriction and hepatic artery flow reduction. In partial liver grafts, high portal flow results in exaggeration of this buffer response.[10]It is important that portal hypertension or splenic steal syndrome is detected immediately after graft implantation so that intraoperative splenic artery ligation, which should be done under portal pressure monitoring, can be carried out right away.

Recipients with significant and long-standing portal hypertension usually have a thickened retroperitoneum and multiple venous collaterals, making cannulation of the inferior mesenteric vein for measuring portal pressure difficult. Therefore, routine cannulation of the inferior mesenteric vein is not recommended. However, a very high portal inflow detected by flowmetry or intraoperative ultrasonography indicates the need for portal manometry. In case 4, continuous measurement of portal pressure was not possible, and direct puncture of the portal vein obviated the need for cannulation of the inferior mesenteric vein.

Hepatic artery thrombosis following liver transplantation is a dire emergency. A faulty anastomosis, suboptimal alignment of the hepatic artery, or splenic artery steal syndrome predisposes the recipient to this complication. A faulty anastomosis and suboptimal alignment of the hepatic artery are results of technical faults. On the other hand, splenic artery steal syndrome can be caused by portal hypertension, significant splenomegaly, poor arterial flow, or a high resistance index. Case 1 was an illustration of these. The flow patterns of the hepatic artery and portal inflow during operation and from postoperative day 1 to day 4 may provide a clue to whether hepatic artery thrombosis is to occur. Early interceptive endovascular embolization of the splenic artery might prevent it.[11]In a series, delayed splenic artery ligation was performed for established small-for-size syndrome[1]and was effective in 6 out of 7 recipients, and subsequently splenic artery ligation was carried out as a proactive approach for recipients with portal hypertension identified at operation.[12]Such an approach is particularly of value for recipients with a high risk of developing small-for-size syndrome.[11]

Shunt ligation

The rate of portal perfusion of a small-for-size liver graft can be three to four times higher than that before its resection from the donor. And a portocaval shunt (Table 2) has been recommended for such grafts.[13]In a porcine model of 70% hepatectomy, shunting significantly reduced the development of hepatocyte ballooning, necrosis, and neutrophil aggregation.[14]Although it was found that graft atrophy occurred after shunting, ligation[13,15,16]or endovascular closure[17]of the shunt can induce graft regeneration.

In addition to hemi-portocaval shunt,[13]mesentericcaval shunt has also been described.[18]However, portal pressure data were not recorded in these studies. On the other hand, portal hypoperfusion can occur in cases where collaterals, e.g. spontaneous splenorenal shunt or coronary vein, are well developed. This is particularly common in recipients with portal vein thrombus, which is a warning sign. Portal hypoperfusion adversely affects graft survival, and therefore shunt ligation should be performed, ideally under flowmetry monitoring as in case 2. Case 4 highlighted that when the coronary vein is the major portal inflow, its ligation may result inportal hypoperfusion. In case 4, portal hypoperfusion was identified by flowmetry and trial clamping of the coronary vein.

Laplace's law states that the pressure inside an inflated elastic container with a curved surface, e.g. a bubble or a blood vessel, is inversely proportional to the radius as long as the surface tension is presumed to change little. A liver graft with very low resistance precipitously lowers the pressure in the collaterals. In most circumstances, they collapse as a result (case 4). When portal flow is preferentially diverted to the shunt instead of the graft, hypoperfusion occurs. To solve the problem, there is the practice of ligating the left renal vein into which the spontaneous splenorenal shunt drains.[19]A covered stent is also used to block the shunt, as deployed by interventional radiology.[20]It is nevertheless important to note that very often the collaterals drain portal blood into the systemic circulation via complicated courses, and portal steal syndrome may occur as a result. Thus, intraoperative cine-portogram-guided ligation or embolization of collaterals as well as portal vein stenting for residual portal vein stenosis may be necessary.[21]

Splenic artery ligation and shunt ligation

Over 10% of patients with long-standing cirrhosis have splenic artery aneurysm.[22]To prevent aneurysmal rupture, which is often fatal, ligation of the splenic artery is necessary.[22,23]In case 3, the ligation was unfortunately followed by splenic infarct and superinfection requiring percutaneous drainage of collection and antibiotic treatment. There were cases in which there was no splenic aneurysm and partial splenic embolization was performed for reduction of portal inflow.[24]Splenic aneurysm often coexists with venous collaterals, and ligation of these spontaneous shunts can aptly boost the portal flow of the recipient, as described in case 3.

However, routine ligation of large venous collaterals may result in portal hypoperfusion and too low a portal pressure if the newly re-established portal inflow is mainly supplied by these collaterals. Graft regeneration relies on adequate portal flow[25]and pressure.[26]In case 4, portal flow in the opposite direction was verified by flowmetry and test clamping of the collateral, which was the much dilated coronary vein.

The patient in case 3 developed splenic infarction and abscess. It was reported that splenic abscess does not occur in patients with almost total infarction of the spleen.[22]In case 3, the infarcted volume after coil embolization of the splenic artery aneurysm was wider than the ligation of the splenic artery and was at most less than 70% of the spleen. It is believed that intraoperative ligation of the splenic artery caused less than 50% of the infarction. Simultaneous ligation of the splenic vein probably accounted for the formation of the splenic abscess.

Liver graft inflow management

In order to conceptualize the treatment policy of graft inflow modulation, a management schedule is depicted (Fig. 5). Of course, there are exceptions. Intraoperative ultrasonography is most handy for identifying cases with portal hypoperfusion, which is to be confirmed by flowmetry. Portal hyperperfusion is an indication of possible portal hypertension, which can be confirmed by manometry of the portal system. Portal manometry can be done with cannulation of the inferior mesenteric vein or by direct puncture of the portal vein. The latter, however, does not allow continuous monitoring, and portal pressure can vary with central venous pressure, which in turn can vary with the positions of the patient and the catheter tip. When a graft is smallfor-size and the recipient portal pressure is high, portal hypertension may persist. Splenic artery ligation, which should be monitored by portal manometry, can lower the portal pressure. If the recipient has a substantial amount of collaterals, graft hypoperfusion may occur after implantation. Correction of hypoperfusion by temporary clamping and then ligation of these collaterals is best monitored by portal flowmetry. Even though portal manometry and flowmetry are useful in inflow modulation, the final solution will be an intraoperative cine-portogram if the outflow is good. It is also important to identify hemodynamic variables potentially influencing the initial outcome and their optimal perioperative management prospectively.

In conclusion, graft inflow modulation is seldom required. Even a small-for-size graft can survive portal hypertension with ease if it has unimpeded venous outflow. On the other hand, venous collaterals like spontaneous splenorenal shunts may cause portal hypoperfusion in a large graft. Graft inflow regulation guided by transonic flowmetry and portal manometry selectively was illustrated by the four cases described.

Funding:None.

Ethical approval:Not needed.

Contributors:CSC designed the study, analyzed the data, and drafted the article. CKSH, SWW, CTT, TSHY and CACY revised the article. LCM and FST made critical revisions and approved the paper. CSC is the guarantor.

Competing interest:No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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35 Botha JF, Langnas AN, Campos BD, Grant WJ, Freise CE, Ascher NL, et al. Left lobe adult-to-adult living donor liver transplantation: small grafts and hemiportocaval shunts in the prevention of small-for-size syndrome. Liver Transpl 2010;16: 649-657.

Received October 28, 2010

Accepted after revision April 1, 2011

Author Affiliations: Department of Surgery (Chan SC, Lo CM, Chok KSH, Sharr WW, Cheung TT, Tsang SHY, Chan ACY and Fan ST), State Key Laboratory for Liver Research (Chan SC, Lo CM and Fan ST), The University of Hong Kong, 102 Pokfulam Road, Hong Kong, China

See Ching Chan, MD, Department of Surgery and State Key Laboratory for Liver Research, The University of Hong Kong, 102 Pokfulam Road, Hong Kong, China (Tel: 852-22553025; Fax: 852-28165284; Email: seechingchan@gmail.com)

? 2011, Hepatobiliary Pancreat Dis Int. All rights reserved.

10.1016/S1499-3872(11)60110-0