University of Groningen

Technical aspects of liver transplantationPolak, Wojciech Grzegorz

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CHAPTER 2

THE EVOLUTION OF SURGICAL TECHNIQUES IN LIVER TRANSPLANTATION - A REVIEW

Polak WG, Peeters PMJG, Slooff MJH

Submitted for publication

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12 | Chapter 2

ABSTRACT

Currently, liver transplantation (LT) is an accepted method of treatment of end-stage

liver disease, metabolic diseases with their primary defect in the liver and unresectable

primary liver tumors. Surgical techniques in liver transplantation have evolved

considerably over the past 40 years. The developments have led to a safer procedure for

the recipient reflected by continuously improving survival figures after LT. Also the new

techniques offer the possibility of tailoring the operation to the needs and condition

of the recipient as in partial grafting or in different revascularization techniques, or in

techniques of biliary reconstructions. Additionally the new techniques such as split LT,

domino transplantation and LRLT have also brought about an increase in the available

grafts. In this review the evolution of surgical techniques in LT over the past 40 years

and their contribution to the current results are discussed.

The evolution of surgical techniques in liver transplantation - a review | 13

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INTRODUCTION

Currently, liver transplantation (LT) is an accepted method of treatment of end-stage

liver disease, metabolic diseases with their primary defect in the liver and unresectable

primary liver tumors. The first attempt of LT in humans was done by Thomas Starzl at

the University of Colorado in Denver, in 1963 1. The recipient was a three-years-old

boy with biliary atresia. The child died during transplantation, because of coagulopathy

and bleeding. After several unsuccessful LTs in Denver, Boston and Paris, a voluntary

worldwide moratorium discouraged liver transplantation until 1967 2-4. On July 23,

1967 Thomas Starzl performed the first successful LT. The recipient was 19-month-old

girl with hepatocellular carcinoma 5. One year later, Sir Roy Calne successfully launched

LT in Cambridge, UK 6. Despite the fact that at least the operation seemed to be feasible,

LT remained an experimental procedure until 1983 due to its low one year survival rate,

which at that time was around 30% 7,8. In that year a National Institute of Health

Consensus Development was held in Washington DC. Based on the experiences from

four liver transplant centers in Pittsburgh (US), Cambridge (UK), Hannover (Germany)

and Groningen (the Netherlands) a consensus document was published stating that LT

could be recognized as an accepted method of treatment for patients with end-stage

liver disease 9. By that time the first improved one year survival rate approaching 60%

were reported 10.

From the first successful LT until now many details of the surgical technique of LT have

been improved and adopted in order to achieve a superior outcome. Currently, one year

patient survival after LT is about 85-90% and long-term survival is about 70% 11,12.

In this review the evolution of surgical techniques in LT over the past 40 years and their

contribution to the current results are discussed.

IMPLANTATION TECHNIQUES

Conventional LT

In the early days of LT, the technique in which the native liver is removed together with

the retrohepatic part of the inferior vena cava (IVC) and orthotopically replaced by a

donor liver including the IVC with supra- and infrahepatic IVC anastomoses, was the

standard technique of LT 13. This technique is called the conventional technique and it

was exclusively used until the early 1980’s. The results of the procedure improved over

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14 | Chapter 2

the years from the poor survival during the early days to 60% one year survival reported

in the early 1980’s 10. The conventional technique requires temporary cross-clamping

of the IVC and portal vein (PV) with important hemodynamic consequences as reduced

back-flow to the heart, congestion in the caval and splanchic bed as well as a reduction

of renal function. The congestion leads to increased bleeding during hepatectomy. To

solve this problems a veno-venous by-pass (VVB) was introduced in the mid 1980’s 14-

15.

Venous-venous by-pass

The first clinical attempts with a passive by-pass from the IVC to the superior vena cava

via the internal jugular vein were often complicated by fatal pulmonary embolism due

to clotting in the plastic cannulae 1. To avoid thrombotic complications Calne et al.

introduced a femoro-femoral partial cardiopulmonary bypass with a pump oxygenator.

This provided the wanted hemodynamic stability 16. However, the need for systemic

heparinisation often led to uncontrolled bleeding. In 1983 Griffith et al. introduced a

VVB with the use of centrifugal pump and heparin coated cannulae 14. Shaw described

the first LT with this type of VVB without the need of systemic heparinization 15.

As shown by several studies the benefits of the VVB include: (1) reduction of hemodynamic

instability in the anhepatic phase; (2) preservation of renal function; (3) reduction of

blood loss and (4) prevention of portal and systemic cogestion 15,17,18. The complication

rate of the VVB varies between 10-30% 19. The most common complications include

wound infection, hematoma, lymphocoele, deep vein thrombosis, and nerve injuries

and they are associated with the insertion of cannulae 19-21. Severe complications as

hypothermia, bleeding complications as a result of hemolysis and platelet depletion or

pulmonary embolism can be life-threatening 22-25. Additionally, the use of the VVB is

associated with higher costs.

Over time modifications of the standard VVB were introduced in order to simplify its use

and reduce complications. In the presence of porto-caval or mesenterico-caval shunts

single-limb bypass from the IVC was used 26. Also cannulation of the PV was replaced in

some centers by cannulation of the inferior mesenteric vein 27. A percutaneous technique

for establishing the VVB for femoral and axillary cannula was introduced in 1994 by

Oken et al. to reduce complications due to the dissection in the axilla and in the groin 28. A prospective randomized study showed that this percutaneous technique shortens

operative time, provides better shunt flow and is associated with a lower complication

rate in comparison to the open technique 29.

The evolution of surgical techniques in liver transplantation - a review | 15

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Despite the advantages of the VVB several centers reported excellent results of LT

without the VVB and recommended to use it selectively 30-33. The development of an

alternative graft implantation technique technique with preservation of the IVC, the so

called piggyback technique ultimately made the VVB redundant.

“Piggyback” technique

In the piggyback technique in the contrast to the conventional technique the native IVC

remains in situ during hepatectomy. To achieve this, the native liver is dissected from

the IVC.

Although this technique was already used in the pioneering period of

clinical LT in Denver (US) and Cambridge (UK), it was popularized by Tzakis et al. in 1989 5,6,34.

In the original report of Tzakis piggyback LT was still performed with the use of a

VVB [34]. Venous outflow reconstruction was done between the suprahepatic end of

the donor IVC and a common orifice created of two or three hepatic veins (left and

middle hepatic vein or right and middle hepatic vein). This is the “classical” piggyback

technique 34.

Currently, the piggyback technique is the dominating one in LT and it is feasible in most

of the cases 35-37. Several studies, including one randomized trial compared the results

of the conventional technique and the piggyback technique. The results of these studies

showed shorter operation time, shorter warm ischemia time, shorter anhepatic phase,

reduction of blood loss and reduction of the cost of the procedure in favour of the

piggyback technique 38-42.

Modifications of the piggyback technique

The “Achilles heel” of the piggyback technique is the venous outflow reconstruction.

Many reports about outflow problems are published, showing a frequency of outflow

complications of 2.5-4.6% 43,44. This includes major graft congestion, caval stenosis or

thrombosis, acute and chronic Budd-Chiari syndrome, and torsion or stenosis of caval

anastomosis.

Belghitti et al. described a side-to-side anastomosis between donor and recipient IVC

without the routine use of VVB 45. In this modification both supra- and infrahepatic

end of the donor IVC is closed and the anastomosis is created between two new

incisions, one made on the recipient IVC and another on the donor IVC. Cherqui et al.

introduced another venous outflow reconstruction. He enlarged the common orifice of

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16 | Chapter 2

three hepatic veins by the caudal incision on the anterior wall of the recipient IVC and

anastomosed it with the suprahepatic end of the donor IVC (end-to-side anastomosis) 46. This technique was further modified by closing all hepatic veins and creating an

anastomosis between a new incision on the anterior wall of recipient IVC and a V-shape

incision on the donor IVC 47,48.

In some particular situations leading to a short suprahepatic IVC cuff such as in domino

liver transplantation or in case of outflow complications after piggyback implantation

some authors advocated the use of the infrahepatic cavo-caval anastomosis 49,50.

All these modifications of venous outflow reconstruction were meant to improve the

venous outflow from the graft and to reduce outflow complications.

There are few studies comparing different techniques of venous outflow reconstruction

in piggyback LT 44,51,52. A French retrospective, multicenter study showed that the

“classical” piggyback technique was associated with a higher bleeding complication

from the caval anastomosis as well as with a higher incidence of Budd-Chiari syndrome

in comparison to the side-to-side or end-to-side cavocavostomy 44. In contrast, the

result of a prospective study from Belgium demonstrated that although the “classical”

piggyback technique was associated with a higher incidence of bleeding complications

compared to the side-to-side technique, all outflow complications occurred only in the

latter technique 51. In a recent study Cescon et al. compared three types of orifices used

for caval anastomosis in “classical” piggyback LT and he found that a cuff of left and

middle hepatic veins with a >1 cm transversal cavoplasty was associated with the lowest

rate of complications related to caval anastomosis (stenosis, thrombosis or kinking) 52.

Temporary portocaval shunt (TPCS)

As an alternative to the VVB authors recommended the use of a TPCS with the

piggyback technique in order to provide better hemodynamic stability and decompress

the splanchic area during the anhepatic phase 53,54. A prospective randomized trial

assessing the use of TPCS in piggy-back LT demonstrated improvement of hemodynamic

status, reduction of intraoperative transfusion requirements and preservation of renal

function 55. Molmenti et al. reported good results with a novel technique facilitating

TPCS when a direct shunt could not be created 56,57. Either a donor iliac vein or plastic

cannula was used to bridge the distance between portal vein and the IVC.

In contrast, several reports demonstrated that excellent results with piggyback LT are

feasible without a TPCS 41,47,58.

The TPCS probably has its own indication field in patients tending to hemodynamic

The evolution of surgical techniques in liver transplantation - a review | 17

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instability, patients with a difficult hepatectomy (i.e. large caudate lobe) or patients with

few portosystemic collaterals.

Pre-reperfusion flushing and IVC venting

Liver grafts need to be flushed before reperfusion to prevent air emboli and to remove

toxic products from the graft after the preservation period. If too high concentration of

vasoactive substances and potassium enters the systematic circulation after reperfusion

it may cause a variety of hemodynamic changes ranging from arrhythmias, hypotension

to cardiac arrest, known as postreperfusion syndrome 59. This syndrome occurs in

approximately 30% of all transplant patients 59,60.

Flushing solutions

Ringer’s solution has been the most common flushing solution since the early years of

LT 3. However, experimental as well as clinical studies showed that rinsing with cold

Ringer’s solution causes endothelial cell swelling, cellular rounding, protrusion of cells

into the sinusoidal space, which can be deleterious for graft function 61,62. Therefore,

some centers replaced Ringer’s solution with other flushing solutions as saline, serum

albumin, plasmanate (serum substitute), Carolina Rinse Solution or autologous blood 60,63,64.

In a randomized prospective study Adam et al. investigated two flushing protocols,

one with Ringer’s lactate and another with human albumin 63. The results of this study

showed that the degree of hepatocellular injury was significantly lower in grafts flushed

with human albumin probably due to their protective effects as oxygen radicals scavenger

and by the maintenance of normal oncotic pressure. Bachmann et al. compared in a

prospective randomized trial three different flushing protocols using human albumin,

Carolina Rinse solution and blood 64. In this study Carolina Rinse Solution proved to

prevent reperfusion injury and improve graft function compared to human albumin and

blood, which is explained by protection of sinusoidal endothelial cells and decreased

activation of Kupfer cells. In all aforementioned studies the liver graft was flushed when

the caval anastomosis was made and subsequently it was reperfused. The liver is not

uniformly rinsed by this technique 65,66. Therefore, toxic products such as potassium

can still enter the systematic circulation after recirculation in too high concentration. To

prevent this some authors proposed additional flush with portal or arterial blood and

the use of vena cava venting.

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18 | Chapter 2

IVC venting

The technique of additional flushing with portal blood was already mentioned in the

late 1970s by Wall et al., however in his report only the first 100 ml of portal blood

reperfusing the graft was discarded 67. This technique was refreshed by Fukuzawa et al.,

who showed that additional flush with 500 ml of portal blood was associated with better

early graft function, better hemodynamic stability and smaller shifts in serum potassium

compared to Ringer’s solution alone 60. Additionally, Fukuzawa et al. proposed IVC

venting with a catheter placed through the infrahepatic anastomosis, which allowed

the external drainage of the effluent before the caval clamp was released. Another

study showed also that portal blood flush alone together with IVC venting prior to

reperfusion was sufficient and optimized graft function without risk of hyperkalemia 68. The advantage of IVC venting was shown in a prospective study by Brems et al. 69. He showed that graft flushing with crystalloid solution and afterwards portal blood

with IVC venting resulted in stable serum potassium and lower rate of postreperfusion

syndrome in comparison to the technique without IVC venting.

However, different results were obtained in two other studies. In a randomized study,

Millis et al. compared four different flushing techniques with a solution of Ringer’s

lactate and serum albumin: initial portal flush with or without IVC venting, and initial

arterial flush with or without IVC venting 70. In both groups with IVC venting additional

flush with 500 ml portal blood was performed. He did not find any differences in

postoperative graft function between the four groups, however the lowest incidence

of postreperfusion syndrome was observed in the group of portal flush without

IVC venting. Similarly, in a more recent retrospective study comparing two flushing

techniques, portal vein flush with Ringer’s without IVC venting and portal blood flush

with IVC venting, the authors demonstrated that the first technique was associated with

better hemodynamic recovery, higher lactate clearance and better early postoperative

graft function compared to the second one 71.

Based on the available data it seems that flushing alone provides inadequate cleaning

of the liver with increased possibility of an unwanted high potassium influx in the

systematic circulation. Addition of venting seems to be more effective with lower

chances of deleterious effects after reperfusion. The debate about which solution is

superior for flushing is still not definitely concluded.

The evolution of surgical techniques in liver transplantation - a review | 19

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REVASCULARIZATION PROTOCOLS

During the first attempts of LT in humans the liver grafts were reperfused first via hepatic

artery 5. Nowadays, the most commonly used sequence of revascularization is initial

reperfusion via the PV (initial portal reperfusion – IPR) and subsequent reconstruction

of the hepatic artery. This order is based on the experience from liver surgery that

portal blood flow alone can provide adequate hepatocellular function 72. However, IPR

increases the risk of warm ischemic damage to the bile ducts, which depend solely on

arterial blood supply. Due to the increasing incidence of ischemic biliary complications

the order of revascularization protocols during LT became subject of investigation.

Sequential revascularization

Sequential revascularization techniques can start either in anterograde fashion via PV or

hepatic artery (HA), or in retrograde fashion via the inferior vena cava (IVC) (retrograde

reperfusion).

Several authors advocated the use of sequential revascularization with arterial blood first

(initial arterial reperfusion – IAR) 73-76. In a prospective randomized study, Durcef et al.

showed more stable hemodynamics, better graft reperfusion and lower peak value of

serum aspartate aminotranferase in patients with IAR compared to patients with IPR 73.

The result of a recent prospective, randomized study comparing hemodynamic profile

and tissue oxygenation during IPR and IAR showed in contrast to the previous study that

IPR offers better graft perfusion and metabolic function than IAR 74. Due to the larger

blood volume IPR causes an acute increase in pulmonary vascular load, which can be

detrimental in patients with pulmonary hypertension or cardiomyopathy. IAR, therefore

may be indicated in patients with poor pulmonary and cardiac reserve. In another

study, Noun et al. demonstrated that IAR provides better graft reperfusion and lower

requirements of blood transfusion as well as shorter postreperfusion fase in comparison

to IPR 75. However, no differences in postoperative aspartate aminotransferase, bile

flow and early vascular and biliary complications were observed between these two

revascularization protocols. Similar results were obtained by Sadler et al., who showed

no differences in the postoperative liver function, intraoperative blood products use and

30-day and 1-year mortality between IPR and IAR 76.

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20 | Chapter 2

Retrograde reperfusion

A new technique of retrograde reperfusion via the IVC followed by subsequent anterograde

reperfusion via PV has recently been proposed 77. In this technique the vascular clamp

on the IVC is removed immediately after completing the IVC anastomosis, allowing

retrograde reperfusion while the PV anastomosis is being constructed. The rationale for

this technique is that it shortens the warm ischemia time (WIT) and efficiently removes

perfusion fluid from the graft before anterograde blood flow is reestablished. The results

of a recent prospective, randomized clinical trial comparing retrograde revascularization

with simultaneous revascularization demonstrated significantly reduction of serum

transaminases and bilirubin levels in the first week posttransplantation as well as lower

incidence of primary non-function and initial poor function in the retrograde reperfused

grafts compared to simultaneously reperfused grafts 78. However, this novel technique

of reperfusion was associated with a higher incidence of ischemic-type biliary lesions

(ITBL).

Simultaneous revascularization

In the simultaneous revascularization the liver graft is reperfused simultaneously via

PV and HA. The motivation for this approach is the same as for the IAR: to reduce

the incidence of biliary complications 79. An additional advantage of simultaneous

reperfusion is that, in case of a problem with one of the two anastomoses, this can

be repaired without completely interrupting blood flow to the graft. The disadvantage

of simultaneous revascularization is prolongation of the WIT and the anhepatic phase,

which can be detrimental to postoperative graft function, survival and morbidity 80,81.

Two retrospective studies compared IPR with simultaneous reperfusion 79,82. No

differences were found in patient and graft survival rates and the incidence of primary non-

function between both techniques of reperfusion. However, simultaneously reperfused

grafts showed significantly lower incidence of biliary complications. In contrast to these

studies, the results of a recent retrospective study showed no differences in patient and

graft survival, morbidity rates, incidence and severity of acute rejection, recuperation

of liver function, or the incidence of ITBL, when comparing IPR versus simultaneous

reperfusion 83.

From the data published to date it is clear that further randomized studies are needed to

prove the exact value of each revascularization technique. So far IPR remains the main

technique of revascularization, except for specific conditions, where IAR or simultaneous

revascularization can be used. The role of retrograde revascularization remains to be

established.

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TECHNIQUES OF VASCULAR RECONSTRUCTIONS

Portal vein reconstruction

PV reconstruction is usually performed in end-to-end fashion. It is very important to

prevent stenosis in the portal anastomosis in order to avoid portal hypertension 84. To

achieve this goal different techniques can be used. Starzl et al. proposed a so called

“growth factor”, which allows portal anastomosis to distend to its maximal diameter

after releasing a clamp from the PV and estabilishing portal flow 85. To increase this

effect it is helpful to clamp the donor PV for a short period as described by Calleja et

al. 86. In cases with a size discrepancy between donor and recipient PV (pediatric LT,

partial grafts) or PV hypoplasia the reconstruction of the PV vein can be challenging and

requires special techniques. The same is true for portal vein thrombosis.

Size mismatch or hypoplasia of the native PV

The size mismatch between donor and recipient PV is frequently located at the smaller

recipient side. In such cases the donor PV can be anastomosed to a branch patch of

left and right recipient PV or even to the branch patch of recipient PV and coronary

vein 87. If this is not possible such as in hypoplastic PV, an incision on the ventral side

of the native PV over the full length of the narrowing enlarges the opening on the PV 88. This defect can be covered by a patch or if not too ong covered by the end-to-end

anastomosis.

If the donor PV is long enough, the narrow or hypoplastic recipient portal vein can

be resected and the anastomosis is made at the level of the confluence of splenic and

superior mesenteric vein 88. If the donor PV is too short an interposition graft fashioned

from the donor iliac vein can be used 88,89.

Portal vein thrombosis

PV thrombosis used to be an absolute contraindication for LT. However, several groups

started to perform eversion thrombectomy in case of PV thrombosis with a success

rate of 95% and one-year patient survival above 80% 90-92. If PV thrombosis is not

only restricted to the PV, but involves the portal confluence, there is necessary to use

a “jump-graft” with a donor iliac vein between recipient superior mesenteric vein and

donor PV 93,94. All recipients after thrombectomy of the PV as well as after a “jump-

graft” reconstruction require anticoagulation therapy to prevent recurrent thrombosis 95,96. However, the 5-year patient survival in patients with PV reconstruction for massive

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22 | Chapter 2

PV thrombosis is still inferior compared to the patients without it 97 .

In case of massive portal system thrombosis special, so called salvage revascularization

techniques were introduced. Cavoportal hemitransposition was proposed by Tzakis et al.

in cases where no portal inflow could be achieved 98. In this technique the infrahepatic

part of the recipient IVC is ligated and the donor PV is anastomosed to the recipient

IVC 98,99.

Sheil et al. described another salvage technique; renoportal anastomosis 100. This

technique is preferably used in patients with preexistent patent distal splenorenal shunt

either spontaneous or after shunt surgery 101. A recent meta-analysis of cavoportal

hemitransposition and renoportal anastomosis showed a high postoperative complication

rate in this procedures and an actuarial patient survival of 74% 102.

Arterialization of the portal vein is the third technique used to provide adequate portal

blood inflow 103. In this technique, the graft receives blood inflow to the portal vein

from the aorta via an iliac conduit or from the common hepatic artery 104,105. The

experiences with this technique are still limited and modest results are reported 105.

The ultimate refugium in cases where no portal flow can be established is multivisceral

organ transplantation. However, so far one and five year patient survival of 65% and

49% are reported 106.

Portal hyperpefusion

A particular complication of partial LT is the “small-for-size-syndrome”. This syndrome

can range from mild hepatic dysfunction with hyperbilirubinemia to the graft failure

leading to retransplantation or death. The problem occurs when a too small for size

graft receives all native portal inflow. Increased portal flow results in the subsequent

reduction of hepatic arterial inflow by the so-called hepatic arterial buffer response,

which can increase the risk for hepatic artery thrombosis (HAT) and ITBL 107. The most

important measure to prevent this syndrome is adequate size matching based on volume

measurements 108. Surgically portal hyperperfusion can be reduced either by splenic

artery ligation combined with portal vein banding or by partial portosystemic shunting

as reported by the Ghent group 109.

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ARTERIAL RECONSTRUCTION

Standard arterial reconstruction

To avoid early HAT, which ultimately requires retransplantation, a patent arterial

anastomosis is mandatory. The preferred method for standard arterial reconstruction is

a direct anastomosis between donor and recipient HA in end-to-end fashion. Whenever

possible it should be done with Carrel patches on donor and recipient side, as arterial

anastomoses without patches was found to be associated with a significantly higher

incidence of HAT 110,111. In order to further decrease the incidence of HAT a branch-patch

technique was introduced 112. In this technique the arterial anastomosis is performed

between bifurcations of the donor and recipient artery (i.e. bifurcation of the proper

HA to the left and right HA or bifurcation of the common HA to the proper HA and the

gastroduodenal artery) 113,114.

Unsuitable recipient artery

In some cases the standard arterial anastomosis cannot be made because of unsuitable

recipient arteries due to stenosis, thrombosis, atherosclerosis, intimal dissection or other

pathology.

In order to overcome these problems alternative methods of arterial reconstruction

have been developed. One of these methods is the use of an arterial conduit from

the donor iliac artery directly to the aorta 115,116. The conduit can be anastomosed

either to the infrarenal or to supratruncal aorta 117-119. If the donor iliac artery is not

available some authors recommended use of saphenous vein, autologous radial artery

or donor superior mesenteric artery (SMA) as the conduit for arterial revascularization 120-122. The use of cryopreserved grafts as the conduit has been abandoned, because

of the high complication rate (stenosis, aneurysm formation) 123. Two studies indicated

that use of donor arterial conduits was associated with excellent long term outcomes 124,125. However, several other studies confirmed that independently of the site of

anastomosis, the use of conduits significantly increases the risk of HAT, especially in

the later posttransplant period 126-129. Therefore, other authors recommended direct

anastomosis between an aortic Carrel patch of the donor celiac axis to the recipient

supratruncal aorta or use the recipient’s splenic artery for arterial reconstruction with

the similar results as the standard anastomosis 119,130,131.

The arterial inflow from the recipient side may be compromised by celiac trunk

compression by the arcuate ligament. This can be diagnosed intraoperatively either

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24 | Chapter 2

by pressure or flow measurements and it can be solved by cleavage of the ligament 132,133. When there is still low arterial inflow, an arterial conduit directly to the aorta is

recommended.

Size discrepancy and multiple arteries

Partial grafting and living donor liver transplantation (LDLT) brought new challenges for

arterial reconstruction with newer techniques and instruments.

In order to overcome size discrepancies between donor and recipient HA the Kyoto

group recommended several techniques for arterial reconstruction 134. In case of a small

caliber difference an undersized artery is cut obliquely or by fish-mouth method, whereas

in a case of a marked diameter difference a funnelization technique is preferred. In the

fish-mouth method two longitudinal contralateral (180° apart) incisions are made on the

undersized artery, whereas in the funnelization technique the caliber of the oversized

artery is reduced gradually with vascular sutures. Testa et al. adopted the fish-mouth

technique 135. The arteriotomy is performed on the posterior wall of donor artery and

on the arterior wall of the recipient artery (mirror incision). Then the back wall is sutured

first from the inside with the running suture followed by running suture on the anterior

wall, which prevents turnover of the anastomosed arteries. Okazaki et al. introduced

the double-needle microsuture technique to avoid the intimal dissection due to turning

over the microclamps on the anastomosed arteries 136. In this technique the back wall

of the anastomosis is suture first with the use of double needle microsuture allowing

the optimal adaptation of the intima. The double-needle technique is especially useful

for arteries in which the tunica intima is separated from tunica media.

In a substantial number of donor livers (24-32%) variant arterial anatomy is present 132,137,138. The presence of aberrant arterial anatomy was found to be a risk factor for

arterial injuries during liver procurement with subsequently increased risk for HAT after

LT 139.

If an accessory artery is present it usually has to be reconstructed on the back-table

prior to implantation. Depending of the length and size of the accessory HA it can

be reinserted to the stump of splenic artery or gastroduodenal artery, or in case of

accessory right HA from the SMA a “fold-over” technique can be used in which the

anastomosis between patches of SMA and celiac trunk is made with a subsequent

anastomosis of the distal end of splenic artery to the recipient artery 140.

The presence of multiple arteries posed another problem for arterial reconstruction in

LDLT. It is not always necessary to reconstruct all arteries, as sometimes the reconstruction

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of the dominant artery is sufficient when a pulsatile back-bleeding from the stumps of

other artery/arteries is confirmed. In the absence of such backflow all arteries need

to be reconstructed 141,142. Marcos et al. demonstrated in a recent report of arterial

reconstruction in adult right lobe LDLT excellent results with a novel technique using

an “Y” extension graft or a reversed extension bifurcated graft from the recipient

proper HA with its bifurcation 143. All aforementioned microsurgical techniques are

routinely performed with the use of either surgical loupes or a surgical microscope,

which substantially decreased the number of arterial complications 144,145. Although

meticulous arterial reconstruction and introduction of microsurgical techniques were

recommended by pioneers of LT, the development of partial liver grafts and especially

LDLT established a place for microsurgical techniques in LT 7.

BILIARY ANASTOMOSIS

The biliary anastomosis is called the “Achilles heel” of LT, because biliary and biliary

related complications are the most common source of morbidity and mortality after LT 146,147. Depending on the definition and diagnostics as well as type of the liver graft

the reported incidence of biliary complications varies from 7-38% 148-156.

During the first human LT a loop cholecystojejunostomy with ligation of the donor

common bile duct was used 5. Many different types of bilio-digestive anastomoses

such as a loop cholecystojejunostomy, Roux-en-Y cholecystojejunostomy and

cholecystoduodenostomy have been used over the years 7,8,157-159. All this techniques

were abandoned because of a high rate of biliary complications (obstructions and

leakage), which were mostly related to obstruction of the cystic duct, “the locus minoris

resistentiae” of those techniques.

Currently, two main techniques of biliary tract reconstruction are used:

choledochocholedochostomy (CDC) and Roux-en-Y hepatico-/choledochojejunostomy.

The choice of the technique depends mostly on the recipient’s bile duct status.

Duct-to-duct anastomosis

The first experiences with choledochocholedochostomy (CDC) were discouraging 7,158.

The CDC was associated with a high incidence of bile leak often due to ischemia of the

common bile duct. The role of the common bile duct vascularization was not realized

yet. However, after a pivotal report of Terblanche in 1983 clarifying the importance of

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26 | Chapter 2

the vascularization of the common bile duct, and its relevance for bile duct anastomosis

the results of CDC substantially improved 147,156,160,161.

If the recipient’s bile duct is normal the CDC is preferable, as it creates physiological bile

flow to the duodenum with preservation of the sphincter of Oddi function, it allows

endoscopic diagnostics and interventions, and it avoids intestinal contamination of the

bile ducts 161,162. It can be done in end-to-end or side-to-side fashion The side-to-side

technique seems to offer greater technical feasibility and easier reconstruction in the

presence of major discrepancy between donor and recipient bile duct, whereas the end-

to-end technique doesn’t require long bile ducts for anastomosis and it reported to be

safer in case of large choledochal varices 151.

A prospective randomized trial comparing end-to-end versus side-to-side biliary showed

no differences in the outcome and the incidence of biliary complication proving that

both techniques are equally effective 163.

Another prospective randomized trial comparing interrupted and continuous suture in

CDC, showed no differences between both suture types with respect to the incidence of

leaks and strictures 164. A new technique of end-to-end CDC using vascular staples was

proposed recently by Thomas et al. 165. In this study tissue everting clips were compared

to a conventional handsewn technique showing no differences in biliary complications

between both techniques.

Hepaticojejunostomy/choledochojejunostomy

The only bilo-digestive anastomosis, which routinely found a place in LT was the Roux-

en-Y hepaticojejunostomy or choledochojejunostomy 147,156.

Both techniques are indicated when the recipient bile duct is abnormal due to the

underlying disease (primary sclerosing cholangitis, cystic fibrosis) or absent as in biliary

atresia. Also when the distance between donor and recipient bile duct is too large

one of these techniques should be used in order to avoid traction on the anastomosis.

Taking into account blood supply of the bile ducts, hepaticojejunostomy as a high

bilodigestive anastomosis provides better conditions for preventing biliary strictures

than choledochojejunostomy 166,167.

A randomized trial comparing CDC with hepaticojejunostomy is not sensible, because

both techniques have their own indication field. In retrospective series both techniques

demonstrated similar outcome, however increased bacterial and fungal colonization

of biliary tract, bile leakage and biliary strictures were more common when Roux-en-Y

hepatico-/choledochojejunostomy was used 146,156,168,169.

J

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Although choledochoduodenostomy has almost been abandoned as a technique of

biliary reconstruction, it can play a role as an alternative or a rescue technique on rare

occasions. Such as in patients with difficult access due to previous operations or patients

with a relatively short bowel due to previous resections or in patients with primary

sclerosing cholangitis 170.

Biliary drainage

The possible benefits of the use of biliary drainage include monitoring of bile production,

decompression of the biliary tract and easy radiological access. On the other hand, the

use of biliary drainage needs an additional opening in the recipient bile duct with a risk

of exit site leakage and complications after biliary drain removal [168]. Moreover, a biliary

drain is a foreign body and it may cause partial obstruction by dislodgement, it may

increase bile sludge and stone formation, as well as risk for cholangitis 171. It also needs

to be present for 6-12 weeks after transplantation often to the patients’ discomfort. To

avoid complications associated with the use of biliary drainage several authors proposed

some technical modifications 172-176. Sawyer et al. used a polypropelene drainage

catheter introduced through the stump of cystic duct instead of standard T-tube,

showing significant reduction of tube-related complications, but not the frequency of

other biliary complications 172. Internal stenting was used by other authors 173,174. Johnson et al. recommended use of double-J catheter as an internal stent as a safe

alternative to standard T-tube 173. Other centres proposed a modified technique of

T-tube removal with radiological placing of a temporary catheter at the time of T-drain

removal or using the T-tube itself as a drain under fluoroscopy guidance at the level of

the former entrance place in the common bile duct 175,176. The results of two prospective randomized studies comparing the use of a T-tube in CDC

did not show any benefits of the use of the T-tube 177,178. In a French multicenter study

patients with the CDC over the T-tube had a significantly higher biliary complications

rate (33.3% vs 15.5%) compared to the patients without the T-tube 177. This was

mostly due to T-tube related complications. The results of the second study showed

that the use of a T-tube was associated with a significantly higher number of septic

complications 178. In a prospective randomized trial Bawa et al. compared CDC with

and without using polyvinyl internal stent 174. He found that patient with an internal

biliary stent had a significantly higher bilary complications rate compared to patients

without biliary stenting. Additionally, the use of T-tube was associated with significantly

higher cost as it was shown first in a retrospective study and then confirmed by results

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28 | Chapter 2

of randomized trial 179,180.

In summary the progress in biliary reconstruction was related to the recognition of the

importance of the arterial circulation of the bile ducts, which made a safe use of CDC

possible. Duct-to-duct anastomosis without routine use of biliary stenting is a preferable

technique of biliary reconstruction in LT. If it is not possible the hepaticojejunostomy is

an equivalent alternative.

PARTIAL LIVER TRANSPLANTATION

Extended waiting time and an unacceptable high mortality on the waiting list for LT in

children as a result of scarcity of pediatric donors were obvious reasons for searching

new techniques to obtain suitable grafts for this specific age group.

Reduced-size liver transplantation

The first reduced-size liver transplantation was performed in Denver in 1975, however

this case was not reported until description of a new technique for reducing adult donor

livers to a left lateral liver graft in 1984 by Bismuth in Paris and by Broelsch in Hannover 181-183. These techniques were rapidly implemented by several major pediatric transplant

centers 184,185.

The results of reduced-size LT were equal to the results of full-size LT and waiting time

and mortality on the waiting list for children were significantly reduced 186,187. As a

logical consequence of these favorable results of partial grafts and the fact that for that

purpose adult livers were withdrawn from the adult donor pool, the emergence of the

split liver technique became a fact 188.

Split liver transplantation

Split LT was first performed by Pichlmayr in Hannover and Bismuth in Paris in 1988 189,190. The technique of liver splitting allows the division of the adult donor liver

together with its vascular and biliary structures into two functional grafts, which can be

transplanted into two recipients. Usually grafts were split in a left or left lateral liver for

a child and a right lobe graft for an adult recipient.

The application of split LT was subject to important adaptations over the years. Two

important items emerged after the initial experiences 191-195. Firstly, applying the

technique in an emergency situation should be done with caution and secondly donor

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livers eligible for splitting should fulfill certain selection criteria as formulated by Ville de

Goyet 196. These criteria include: donors less that 45 years old, hemodynamically stable,

low or mild inotropic support, normal or slightly altered liver tests, less then five days in

the intensive care unit and normal macroscopic aspect at procurement. Only when such

conditions are met the results of split LT are equal to whole liver grafting 197,198.

A major debate in split LT concerned the subject of in situ or ex-situ splitting 199-201. In

the beginning the liver splitting was usually performed ex-situ, which means that the

whole liver was procured and subsequently divided into two grafts on the back-table 202. Rogiers et al. proposed a new technique, in which the liver is splitted during organ

procurement in the heart-beating donor 203. This technique was developed from left

lateral segmentectomy for living donation. The main advantage of the in-situ technique

is a shorter WIT, better hemostasis and lower rate of biliary complications 199,204.

However, this technique significantly prolongs the time of organ procurement and it

might cause hemodynamic instability during the donor procedure. Also procurement

teams may outstand their welcome in donor hospitals due to the prolonged operation

times. So far from the available literature there is no consensus which technique is

superior as both techniques demonstrate similar patient and graft survival compared

to whole liver grafting 200,201,204. In a retrospective study, Rayes et al. compared ex-

situ and in-situ splitting techniques with respect to patient and graft survival 205. He

found that the in-situ technique provided significantly higher one-year graft survival

in pediatric recipients compared to the ex-situ technique. However, this difference did

not translate in higher one-year patient survival in pediatric recipients. Moreover, there

were no differences in one-year patient and graft survival in adult recipients between

both techniques.

Nowadays split LT can be regarded as a routine procedure in experienced centers. The

application of this technique however is still developing.

Although liver splitting is used to be performed in adult donor livers Cescon et al. recently

reported also excellent results of split LT from pediatric donors below 40 kg 206.

Until 2005 only grafts from stable heart-beating donors were considered for splitting.

However, recently Muiesan et al. reported the first experiences with split and reduced-

size liver transplantation from non-heart beating donors 207.

Due to the increasing shortage of donor grafts especially for adults the technique of left/

right splitting of a graft for two adults re-emerged 208-211. The value of this technique is

currently under evaluation in experienced centers, as left lobe grafts in adult recipients

had inferior outcome in the past 212-214.

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30 | Chapter 2

Recently, left lateral graft procurement was further developed to create monosegmental

grafts and therefore facilitating LT in very small children 215-217.

Living donor liver transplantatation (LDLT)

Evolution of surgical techniques related to partial LT as well as the continuing shortage of

deceased donors led to the development of LDLT. Initially it was developed for pediatric

recipients as the mortality rate in children awaiting LT was high. The first attempts were

performed by Raia et al. in 1988 and 1989 218. The first successful LDLT was reported

in 1990 by Strong et al., who transplanted a left lateral segment from a mother to her

17-months-old son with biliary atresia 219. Since then many centers, especially in Japan

where liver grafts from deceased donors were not available, further developed LDLT 220. LDLT for pediatric recipients turned out to be a great success, as patient and graft

survival was comparable and in most centers superior to that in split and reduced size LT

and even in whole LT 12,221-223. At the same time it appeared a relatively safe procedure

for the donor, with a complications rate of 15-20% as reported in large series and a

mortality rate of between 0.1% and 0.4% 224-226.

The excellent results of LDLT in children together with increasing waiting time for adult

patients with malignant liver tumors prompted the use of living donor liver grafts also

for adults 227. First left lobe grafts were used 228. However, the volume of the left liver

lobe seemed not sufficient for adults and small-for-size syndrome appeared to be a

frequent complication as well as the results were not satisfactory 222,229. Nowadays left

lobes are only used for small adults or older adolescents, or they are used in a dual graft

setting 228,230,231. Therefore, right lobe grafting is the most applied technique for LDLT

in adults. The long-term results of LDLT for adults are nowadays approaching those

of whole LT. However, the rate of biliary complications is high 12,232-234. Additionally,

morbidity in living donors of right liver lobes is significantly higher than morbidity after

living donation for pediatric recipients 233-236.

The techniques of LT with living donor grafts are in essence the same as for implantation

of partial grafts from deceased donors. However, vascular and biliary reconstructions

are often more complex due to multiple vessels or ducts. Except for an adequate graft

size match in LDLT, good venous drainage of the anterior sector of the right liver lobe

was found to be extremely important for postoperative liver function 237. Many different

approaches have been adopted to avoid venous congestion of the anterior sector. These

include reconstruction of the hepatic veins of segment V and VIII into the recipient IVC

using an interposition vein graft or a routine inclusion of the middle hepatic vein in the

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graft 238-240. In LDLT the same techniques of biliary reconstructions can be used as in

LT from deceased donors. Roux-en-Y hepaticojejunostomy has been standard biliary

reconstruction in pediatric LDLT, however recently duct-to-duct reconstruction is used

more frequently, especially in adult LDLT 240-243. In case of multiple bile ducts if they

are close to each other they can be unified into a single orifice (ductoplasty) before

anastomosis 244-245.

OTHER LIVER TRANSPLANTATION TECHNIQUES

Domino liver transplantation (DLT)

The concept of DLT was first developed during the international workshop in liver

transplantation for familial amyloidosis polyneuropathy in Stockholm in 1993 246. Two

years later Furtado performed the first successful DLT in Portugal 247. This technique is

possible in patients with a primary genetic defect restricted to the liver with secondary

debilitating extrahepatic manifestations in vital organs such as kidneys, heart and brain.

In order to stop the progression of the disease the liver needs to be replaced 248. This

liver is suitable for donation to another patient with liver failure, because it takes one or

two decades, before the disease becomes symptomatic in a recipient 247-249. Therefore,

such domino livers are given to elderly patients or patients with a malignant disease in

the liver 250. The advantage for the domino recipients is that they can get a graft in

earlier course of their disease. Familial amyloid polyneuropathy is a classical example of

the disease, where domino LT can be used.

The results of DLT are rewarding. Furtado et al. reported one-year patients survival of

70% and 60% 3-year survival, however a recent report Yamamoto et al. showed 1-

year and 5-year patient survival of 95% and 92% in recipients transplanted in the last

decade 250-251 .

Domino donation evolved over the years. In the early years the liver was implanted with

the native IVC, while nowadays the domino liver is harvested without the IVC 252-254. This

requires reconstruction of the suprahepatic caval vein cuff for piggyback implantation 255,256. The advantage of leaving the native IVC in situ is the improved hemodynamic

stability in these already hemodynamic compromised patients. Azoulay et al. reported

also split LT from domino livers from patients with familial amyloid polyneuropathy 257.

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32 | Chapter 2

Auxiliary liver transplantation (ALT)

In the early days of LT the risks of the recipient hepatectomy were appreciated. This

caused an interest in ALT, in which the native liver remained in place and a new graft was

transplanted in a heterotopic position. This is the so called heterotopic auxiliary LT. The

first successful heterotopic auxiliary LT was reported by Fortner et al. in 1970, however

the long-term results were disappointing and inferior to orthotopic LT 258,259. The main

reasons for this were technical complications due to a high venous outflow pressure,

portal vein flow diversion as well as the high risks for the development of hepatocellular

carcinoma in the native liver. As showed in a recent case-control study comparing the

results ALT and orthotopic LT, ALT can not be an alternative for orthotopic LT for chronic

liver disease due to the inferior long-term outcome 260. Therefore, the technique of

heterotopic auxiliary LT has been abandoned for chronic liver diseases.

Terpstra et al. reintroduced the concept of heterotopic ALT for acute liver failure 261. It

based on the fact that after recuperation of the native liver the auxiliary graft could be

removed. This elegant concept was shown to be viable. However, it gained no support

in the transplant community, because of technical problems implied by portal vein

thrombosis and graft dysfunction, which led to the inferior patient survival compared

to orthotopic LT. To solve this problem in a recent report Ringers et al. described a

new technique of ALT in which dissection of the recipient hepatoduodenal ligament is

avoided 262. In this technique end-to-end anastomose was performed between donor

portal vein and recipient left renal vein, hepatic artery was anastomosed to the aorta

using an iliac arterial graft conduit and the bile duct was anastomosed to the stomach.

In 1991 Gubernatis et al. introduced a new technique of ALT for fulminant hepatic

failure, in which part of the native liver was removed and a partial liver graft was

implanted orthotopically (auxiliary partial orthotopic LT) 263. The technique of auxiliary

partial orthotopic LT tried to avoid the disadvantages of ALT while keeping the idea of a

temporary auxiliary graft. Several studies except for one from Japan reported favorable

outcome after auxiliary orthotopic LT for fulminant hepatic failure, however it was

associated with a higher postoperative morbidity 264-272. As shown in one study it

should be offered only for patients with high chances of liver regeneration 265.

Auxiliary orthotopic liver transplantation was also performed with good results for

metabolic liver disorders that cause life-threatening extrahepatic complications as for

example Crigler-Najjar syndrome type 1 273. The rationale for this treatment is to provide

sufficient liver mass to correct the metabolic disorder while keeping the majority of the

native liver.

The evolution of surgical techniques in liver transplantation - a review | 33

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An interesting variant of auxiliary orthotopic LT was developed in Japan to overcome

small-for-size syndrome in LRLT 274. First, a left hemihepatectomy is performed in the

recipient with subsequent implantation of the left lobe from the living donor. The right

part of the native liver is kept in place until sufficient graft regeneration. Subsequently

the remaining native liver is removed during a second-stage operation.

Although conceptually promising, the ALT plays a minimal role in the treatment of

patients with acute or chronic liver failure mostly because of the high complications

rate, its complexity as well as the fact that orthotopic LT remains a gold standard of the

treatment.

SUMMARY

Surgical techniques in liver transplantation have evolved considerably over the past

40 years. The developments have led to a safer procedure for the recipient reflected

by continuously improving survival figures after LT. Also the new techniques offer the

possibility of tailoring the operation to the needs and condition of the recipient as in

partial grafting or in different revascularization techniques, or in techniques of biliary

reconstructions. Additionally the new techniques such as split LT, domino transplantation

and LRLT have also brought about an increase in the available grafts.

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