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Voramon Teranasthiarphan, M.D., Thakerng Pitakteerabundit, M.D., Nan-ak Wiboonkhwan, M.D.,
Tortrakoon ongkan,
M.D.
Department of Surgery, Prince of Songkla University, Hat Yai, Songkhla 90110, ailand.
The Evolution of Associating Liver Partition with
Portal Vein Ligation for Staged Hepatectomy
ABSTRACT
Associating Liver Partition with Portal Vein Ligation for Staged Hepatectomy is a cutting-edge surgical technique
for resection of hepatic malignancies that has piqued the interest of the international hepatobiliary community.
Patients with insucient future liver remnants, many of whom are considered unresectable via other methods,
have the possibility of being cured with this treatment. e main issues; howbeit include, increased perioperative
morbidity and mortality as well as both early and rapid disease recurrence. However, with continuous improving
of patient selection, optimizing stage 2 operation times and rened operative techniques this has led to reduced
morbidity and mortality rates. As for its usage, the most frequent indication is colorectal liver metastasis (CRLM);
in which, the results in CRLM have shown higher resectability; however, it has a comparable complication rate
to two-stage hepatectomy. Conversely, perihilar cholangiocarcinoma and hepatocellular carcinoma have terrible
outcomes; although, with technical renement and better patient selection good outcomes are achievable.
Herein, we summarized the current evidence based of the application of ALPPS in real-life practice, including
the potential complications related to this procedure.
Keywords: ALPPS; Future liver remnant; hepatectomy (Siriraj Med J 2022; 74: 266-273)
Corresponding author: Tortrakoon ongkan
E-mail: Ttortrak@medicine.psu.ac.th
Received 2 December 2021 Revised 20 February 2022 Accepted 7 March 2022
ORCID ID: https://orcid.org/0000-0002-8210-1459
http://dx.doi.org/10.33192/Smj.2022.33
INTRODUCTION
An insucient future liver remnant is a factor
excluding patients from curative intent liver resection,
as the low hepatic functional reserve of the small, future
liver remnant (FLR) can lead to post-hepatectomy liver
failure (PHLF). Portal vein embolization (PVE) results in
compensatory hypertrophy of FLR; however, the biggest
drawback of PVE is insucient FLR hypertrophy, or
subsequent disease progression; which aects roughly
20% of patients.
1
Recently, Two-stage hepatectomy (TSH) has been
introduced for patients with bilateral multinodular colorectal
liver metastases.
2
is can be used in conjunction with
Portal vein occlusion (PVO); either portal vein ligation
(PVL) or percutaneous PVE. e main idea being that the
liver grows in the interval between sequential resection,
and the risk of PHLF is presumably reduced due to
this staged approach.
3,4
However, although TSH is well
established, failure to proceed to stage 2 is reported as
being a problem in up to one-third of patients.
Dr. Hans Schlitt discovered the Associating
Liver Partition with Portal Vein Ligation for Staged
Hepatectomy (ALPPS) by chance. He noticed a small
liver remnant during an extended right hepatectomy for
hilar cholangiocarcinoma. So, he decided to perform a
hepaticojejunostomy and right PVL aer parenchymal
Teranasthiarphan et al.
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Review Article
SMJ
transection for enhancing exposure. Fortunately, computed
tomography (CT) scanning revealed extensive hypertrophy
of the remnant segments one week later. Hence, the right
liver was subsequently removed.
5
ALPPS is based on the
fast hypertrophy of remnant segments. It can enhance the
remaining liver by up to 80% over an average duration
of 1-2 weeks compared to 20-45% in 2-8 weeks in PVE
patients.
6,7
e possible mechanism of rapid hypertrophy
in ALPPS is based on the increase of portal ow in the
disconnection of the interlobar perfusion, accompanied
by the increased level of inammatory cytokines that
induce liver regeneration. e disadvantage is a high
procedure-related morbidity and mortality rate of roughly
40% and 15%, respectively, mainly from liver failure
and bile leakage.
8
As a result, the safety of ALPPS in
comparison to standard techniques is still debatable.
Pathophysiology of liver regeneration in ALPPS
There are two proposed mechanisms for rapid
hypertrophy aer the rst stage of ALPPS. Firstly, the
parenchymal transection will not allow communication
of interlobar collateral circulation. e portal ow can
maximize the shearing force to the hepatocyte that causes
the liver to regenerate. e later mechanism is based on
the increased level of inammatory mediators that drive
liver regeneration.
9
e disparity between the size and function of a remnant
could explain the high risk of ALPPS complications. e
regenerate hepatocyte shows edema and expansion, but is
still partly immature within the rst two weeks aer the
procedure, albeit from unknown causes.
10
Histologically,
the hepatocyte has greater cell density, is smaller in
size, brighter and has narrower sinusoidal compared to
PVE.
11
In electron microscopy, the FLR area is frequently
shown as being vacant in appearance. is is caused
by hepatocytic cytoplasm lled with glycogen granules
and fewer cytoplasmic organelles, lipofuscin granules.
To date, all of these properties can be interpreted as
immature cells.
Technical considerations (right trisectionectomy ALPPS)
The liver was examined with intraoperative
ultrasonography to conrm the number and location
of the tumor. e liver was fully mobilized, and the
hepatoduodenal ligament was skeletonized. e right portal
vein was ligated with non-absorbable suture material.
e parenchymal transection was carried down along the
falciform ligament (Fig 1). Most of the authors advocated
for using a plastic bag for covering the deportalized liver,
so as to control bile leakage. CT scanning was performed
at 9 days on average, postoperatively. e right hepatic
artery, right hepatic duct, right, and middle hepatic vein
were then divided in the second stage operation.
5,12
Modications to the initial techniques
Bile duct ligation
Recent studies have suggested against routine bile
duct ligation.
13,14
Many published reports have reported
complications; such as, a higher rate of bile leakage,
biloma formation and severe, dense adhesion at the porta
hepatis during second stage operations. e previous
hypothesis was that by increasing the biliary obstruction
response in obstructed livers, right bile duct ligation
could promote additional FLR hypertrophy.
Fig 1. Schematic overview of Associating Liver Partition with Portal Vein Ligation for Staged Hepatectomy (right trisectionectomy). (A)
e liver was occupied with multiple tumors on both sides. e potential procedure is right trisectionectomy with the lateral section as the
future remnant liver. (B) In the rst stage, complete parenchymal transection was carried out along the falciform ligament, the tumors in
the remnant liver were removed, and the right portal vein was ligated. (C) e future liver remnant shows signicant hypertrophy, and then
the deportalized lobe was removed.
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Preservation of the middle hepatic vein
e rst ALPPS series mentions ligation of the
middle hepatic vein during the rst stage of the procedure
5
however, a recent study
13
discovered its relation with
congestion of liver segments IV, V, VIII. is may result
in decreased outow, followed by a higher risk of ischemia
and hepatic necrosis as well as subsequent bile leakage.
e middle hepatic vein is now preserved as the venous
outow of segment IV, rather than being removed as
previously reported, without compromising parenchymal
hypertrophy. Most hepatobiliary surgeons currently use
this method.
6
Hybrid ALPPS (Non touch technique)
is modication aims to avoid manipulating the
right lobe of the liver in order to improve tumor tissue
handling and prevent hematologic malignancy spread.
13,15,16
e parenchymal transection is performed using an anterior
approach, without mobilization, and the hepatoduodenal
ligament is le intact. In the days following the operation,
interventional radiology performs right PVE. At the
second stage, there is less inammation around the liver;
according to reports. Nevertheless, some of the authors
are against this idea, due to the inability to achieve
optimal vascular control during a technically complex
procedure; especially via an anterior approach.
14,15
Partial ALPPS
is modied technique solely diers in the degree of
liver partition. In contrast to conventional ALPPS, where
parenchymal transection was complete, partial ALPPS
transected only 50% to 80% of the parenchyma in stage
I.
14
Anatomic outow structures (hepatic veins), and/
or tumor(s) lying inside or near the future transection
line, determine the degree of partial transection. e
main advantage of this modication in technique is
that it limits the deleterious congestion of the excluded
segments and segment IV necrosis, by preserving their
outow via the middle hepatic vein.
17,18
Partial ALPPS
generates equivalent FLR hypertrophy to complete ALPPS,
but with decreased morbidity and near-zero mortality.
16
However, Chan et al. demonstrated that complete ALPPS
can cause rapid FLR hypertrophy more so than partial
ALPPS, while having no impact on perioperative risks in
chronic liver disease.
19
In the meta-analysis by Wu et al,
they compared partial and complete ALPPS and showed
that FLR hypertrophy and time intervals between stages
were not substantially dierent for both techniques.
20
Although, the post-operative complication rate was
signicantly lower in partial ALPPS.
Mini-ALPPS
Mini-ALPPS simplies rst stage hepatectomy, by
using a partial parenchymal transection technique and
intraoperative portal vein embolization, without hilar
dissection or liver mobilization. is approach allows
for an accelerated FLR hypertrophy to be obtained at
a mean of 63% within 11 days.
19
is is similar to that
reported for classic ALPPS; but without the high rate of
mortality and morbidity.
5,6
Associating Liver Tourniquet and Portal Ligation for
Staged Hepatectomy
With this method, a tourniquet is used to replace the
completion of the parenchymal transection, this reduces
the complexity and time required in the rst stage of the
operation.
21
A thick suture material is applied around the
liver in the deep sulcus of the parenchymal transection
(an extra-glissonian approach). en the tourniquet
is subsequently tightened to completely obstruct all
interlobar collateral circulation.
Radiofrequency assisted liver partition
is is an application of radiofrequency ablation to
the parenchyma, aer right PVL at the site of demarcation.
e hypertrophic rate is increased by up to 62% over a
mean interval of 22 days, according to the study, and
that it also avoids the complications of liver partition.
22
ALPPS outcome
Primary outcomes
e studies that investigated the ecacy of ALPPS
have consistently revealed that ALPPS causes hypertrophy
of 60-90%, with the average duration of the stage being
9-14 days (Table 1). Most of the cases (95-100%) that
complete the rst stage could be undergoing a later
stage.
5,6,15,23,24
e international ALPPS registry consists
of 141 (70%) colorectal liver metastasis (CRLM) patients
among 202 patients.
25
Within 7 days, the median initial
standardized future liver remnant of 21% grew by 80%,
and ninety-day mortality was 9%. Severe complications
occurred in 27% of patients. Red blood cell transfusion,
an operative time of more than 300 minutes, patient ages
being greater than 60 years, and non-CRLM were all
independent risks for severe complications. Additionally,
the registry shows that many factors directly aect the
rate of liver hypertrophy; such as, age, intermittent
Pringle maneuver, and abnormal parenchyma.
25
According to meta-analysis,
26
ALPPS seems to be
more eective than the two-stage approach in causing
remnant hypertrophy, with signicantly higher resection
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TABLE 1. Success rate and outcome of Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy
compare with two-staged hepatectomy.
Author Year Primary tumor FLR volume Drop-out rate Morbidity*/
(reference) (N) increment(%)afterrststage(%) mortality
CRLM HCC CCA ALPPS TSH ALPPS TSH (%)
Schnitzbauer
5
2012 14 3 4 74 n/a n/a n/a 64/12
ShindohJ
8
2013 14 3 4 70 62 n/a 28 40/12
SchaddeE
25
2014 141 17 19 80 n/a 2 n/a 27/9
SchaddeE
6
2015 228 32 27 90 n/a 2 n/a 14/9
Sandstrom
31
2018 97 - - 68 36 8 43 43/8
WangZ
36
2020 - 45 - 57 n/a 9 n/a 12/11
ChanA
37
2021 - 46 - 49 38 2 32 21/6.5
Abbreviations: CRLM; Colorectal Liver Metastasis, HCC; Hepatocellular carcinoma, CCA; Cholangiocarcinoma, FLR; Future liver remnant,
ALPPS; Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy, TSH; two-stage hepatectomy
* Clavien-Dindo grade ≥ IIIB
n/a: non-available
rates of approximately 92-100%.
25–28
Additionally, there
is a shorter time interval of 1-2 weeks vs. 20-45% in
2-8 weeks following PVE. Furthermore, prolonged
periods between stages in TSH has caused up to 30%
of patients to be ineligible for a nal hepatectomy, due
to disease progression.
10,29,30
At the same time, ALPPS
faces the problem of most candidates having a higher
risk for micrometastasis in FLR aer a second stage
operation. Additionally, there is an argument concerning
the hypertrophic liver, in regards to cellular swelling
or complete functioning regeneration, and that liver
hypertrophy in such a short period of time may not
ensure its functional capacity.
9
In conclusion, despite
ALPPS having a greater resectability rate, there is no
signicant dierence in disease free survival between
ALPPS and TSH.
Morbidity and mortality
e major obstacle of the procedure is the signicant
rate of morbidity and mortality. e largest study, 202
patients, cited major morbidity of 28% and mortality of
9%.
6,15,25
Although, the reported mortality rate is variable,
the high complication rate is may have occurred from
the small sample size of the study. A German study
revealed a 12 percent 90-day death rate, triggering a
erce debate among international experts;
5
surgical
exploration, right portal vein ligation (PVL additionally,
other small studies found signicantly higher rates;
ranging from 22-29%. Conversely, there have been no
90-day mortalities recorded across multiple centers.
13,15,25
Comparison between ALPPS and Two-stage hepatectomy.
e retrospective comparative analysis of 140 patients
undergoing PVE to the 25 patients undergoing ALPPS
showed that the rates of hypertrophy were similar in both
groups: 70% in the ALPPS group and 60% in the PVE
group.
8
Overall, there was no signicant dierence in
major morbidity between the two groups (40% ALPPS
versus 30% PVE). However, for other complications
ALPPS had signicantly higher rates than PVE in all
causes; bile leak (24% versus 6%), re-laparotomy (30%
versus 3%) and sepsis (20% versus 0%); but was no
signicantly higher in liver-related mortality (12% versus
6%).
Data from the retrospective multicenter study
showed a trend towards higher morbidity and mortality
associated with ALPPS compared with PVE. e 90-day
mortality was 15% versus 6%, and post-hepatectomy
liver failure was 13% versus 9% for the ALPPS versus
the PVE group, respectively. Moreover, patients in the
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270
ALPPS group achieved more completion of resection
(83% versus 66%); however, the recurrence at one year
was comparable (54% versus 52%).
25
In contrast to Aloia et al, the PVE group had just a
34% increase in FLR compared to a 77% gain in the ALPPS
group.
28
e LIGRO was a landmark randomized controlled
trial that compared the resection rate between ALPPS and
TSH in CRLM patients. is study demonstrated that
ALPPS could oer a higher resection rate compared to
TSH, 92% to 57%, respectively, with comparable surgical
margins, complications, and short-term mortality.
31
A recent systematic review and meta-analysis of
ALPPS versus traditional staged hepatectomy, in 2019,
7
found that ALPPS increased FLR more than PVE and
TSH. However, the results of the study are limited due
to the high heterogeneity among the studies. As for
overall mortality and morbidity, the higher trend is
on the side of ALPPS over PVE/TSH; morbidity 30%
and 26%, respectively, without heterogeneity; mortality
10% and 4% consequently, without heterogeneity. e
feasible rate of stage 2 aer ALPPS and PVE were 94%
versus 63%, respectively, which is the same as between
ALPPS and TSH, 95% versus 72%, respectively.
ALPPS in CRLM
In the first international registry,
6
the 90-day
postoperative mortality among all patients who underwent
ALPPS was 9%. For patients with CRLM, the 2-year
overall survival (OS) and disease-free survival (DFS)
were 62% and 41%, respectively. Patients with CRLM
who were younger than 60 years of age had a better
chance of survival than patients with other malignancies.
A separate analysis of the international ALPPS registry
included 228 patients with CRLM, which comprised of
72% of the study population. In this report, the 90-day
mortality was 5%. e leading cause of mortality was liver-
related, for which it was recommended by the authors
to evaluate the patients underlying condition, using the
model of end-stage liver disease, and the international
study group for liver surgery criteria, so as to discriminate
against higher or lower risk.
27
Some of the suggested approaches to improve ALPPS
outcome include stratication of patients for developed
liver failure following rst stage hepatectomy, achieving
expertise in the learning curve, renement in patient
selection, modications to the original ALPPS procedure
to reduce liver traumatization, interval chemotherapy,
a shorter time o chemotherapy, and preservation of
segment IV.
9
e objective of oncologic liver surgery is
to achieve a tumor-free margin. In there meta-analysis,
Margonis et al,
29
found that a margin of >1 mm was
related with better overall survival, and a margin of >1
cm was even associated with better DFS. As a result, a
better oncologic outcome may even justify the removal
of signicant volumes of parenchyma. Furthermore,
regarding the numbers and sizes of metastases remaining
in the FLR, full tumor clearance of the FLR during the
rst stage is crucial for any two-stage strategy. ese
traditional markers; numbers and sizes of metastases
as well as intensity of oncologic pretreatment area are
important prognostic factors. KRAS mutation, which has
been linked to poor survival, and TP53 mutation have
both been linked to a higher chance of tumor relapse in
recent studies.
30
Hence, analysis by Schnitzbauer et al,
32
assumed
that there is a tendency for potential overuse of ALPPS.
Additionally, the role of major hepatectomy in CRLM has
become less, due to eective down-sizing of chemotherapy
being available. In this case, ALPPS must be viewed as
a last resort at the very end of the therapeutic spectrum
for CRLM.
ALPPS in Hepatocellular carcinoma (HCC)
e ALPPS registry’s initial report, which included
17 patients with HCC, and the second, which included
32 patients with HCC, reported 90-day mortality rates of
12% and 13%, respectively.
6,25
ese results appeared to
be the consequence of both an early learning curve and a
typically increased mortality of liver resection in altered
liver parenchyma. More devastating was when the rst
major analysis from the ALPPS registry, with 35 ALPPS
for intermediate-stage tumor, revealed a 90-day mortality
of 30%.
33
However, a thorough examination revealed
that ALPPS had been employed with broad inclusion
criteria and in an undierentiated manner. Fortunately,
aer careful selection, using the ALPPS technique in a
good patient candidate with HCC (Child A cirrhosis,
FLR volume > 30%, an indocyanine green clearance rate
at 15 minutes <20%, platelet count > 100,000/µL and no
complete right portal vein thrombosis), led to a decrease
in mortality of 7% and 0%.
23,34,35
A recent study, from
Wang et al, investigated their outcomes of conventional
ALPPS in 45 HCC patients.
36
e results showed that
the patients who received ALPPS had similar eects to
those who underwent one-stage hepatectomy,; with 1-
and 3-year OS rates of 64% and 60% and 1- and 3-year
DFS rates of 48% and 44%. Furthermore, the results
were far superior to those who received transarterial
chemoembolization. Recently, Chan et al. investigated
the role of ALPPS for hepatitis-related HCC. e study
shows ALPPS induced FLR volume increment by 48.8%,
without dierence in morbidity and mortality compared
Teranasthiarphan et al.
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to PVE. Although, over 56.5% of patients that complete
stage 2 had cirrhosis.
37
ALPPS in cholangiocarcinoma
From the beginning, ALPPS was rstly used in a
case of hilar cholangiocarcinoma, even so, the latest
data reveals the highest perioperative complication risks
among all indicated diseases. e 90-day-mortality for
intrahepatic cholangiocarcinoma from the ALPPS registry
is about 13%.
6
e risk of perioperative complications
is higher in perihilar cholangiocarcinoma (PHC), most
likely from post rst stage parenchymal necrosis, possibly
infected bile, and biliary leakage. A matched case study
that compared data from the ALPPS registry to data
on PVE and right trisectionectomy for PHC found that
perioperative mortality was as high as 48% in the ALPPS
group versus 24% in the matched group.
38
ese results led
to unacceptable arguments over whether it is a homicidal
choice of treatment or not. However, from a closer
viewpoint, ALPPS in the research was performed with the
intention to improve resectability, by rapidly increasing
FLR; but at the same time some principles of surgery for
PHC were neglected. For example; performing the 1
st
stage
operation in the presence of infection and inammation
by conventional ALPPS; thereby causing a higher risk
of biliary leakage. Conversely, new techniques; such as:
“Mini-ALPPS” and “Hybrid ALPPS”, were introduced.
Both strategies aim to achieve appropriate FLR growth
in the shortest period possible, and both prevent hilar
dissection during the rst stage. As a result, in PHC
patients, ALPPS should not be deemed a categorical
contraindication.
Authors opinions
Aer the initial outcome of ALPPS demonstrated
the dramatic increment of FLR, this procedure became
famous among the hepatobiliary surgery community.
However, many patients have been through this procedure
without proper indication, which has lead to avoidable
complications. Even with the international ALPPS registry
results, the 90-day mortality was much higher than
conventional hepatectomy.
6
e authors suggest that the following issue should
be considered before selecting a patient for ALPPS.
1. For CRLM: the patient should receive episodes
of systemic chemotherapy, with or without
targeted therapy. Good response liver metastasis
could omit the need for this risky procedure.ALPPS
should only be used as a last measure in the
treatment of CRLM.
32
2. The CRLM patients who progress while on
systemic therapy are poor candidates for ALPPS.
3. Aer stage 1, preoperative liver evaluation is
crucial. Both quantitative and qualitative assessments
are essential. e second stage should be terminated,
or postponed for any patient that has good
FLR increase but impaired function. ere are
some discrepancies between the increased
volume and the remnant›s function because most
of the regenerated hepatocyte is still partly
immature.
10
4. In chronic viral hepatitis or cirrhosis there is
scant evidence of ALPPS; therefore, the surgeon
should select the most suitable patients for ALPPS.
5. Patients with cholangiocarcinoma should avoid
ALPPS. ALPPS in cholangiocarcinoma had the
highest risk of perioperative complication among
all indicated diseases. e 90-day-mortality for
intrahepatic cholangiocarcinoma is high as 13%,
and might be higher for perihilar cholangiocarcinoma.
6
CONCLUSION
ALPPS is one of the strategies to overcome inadequate
future liver remnants. Perioperative complications are
the main concern for ALPPS, because the tremendous
volume increment within 1-2 weeks is not well correlated
with the function of the remnant liver. As early results
from the ALPPS registry have shown, inappropriate
patient selection resulted in a high risk of PHLF and
postoperative mortality. Proper patient selection coupled
with a satisfactory pre-and interstage liver assessment
could improve outcomes; especially for CRLM, which
has comparable results to TSH.
ACKNOWLEDGEMENT
e authors would like to thank Woralux Phusoongnern,
M.D., FRCNST, for the illustrations.
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