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Review Clinical and Molecular Hepatology 2016;22:212-218

Current status of laparoscopic liver resection for hepa-

tocellular carcinoma
Hanisah Guro1,2, Jai Young Cho2, Ho-Seong Han2, Yoo-Seok Yoon2, YoungRok Choi2, Mohan Periyasamy2,3
1
Department of Surgery, Amai Pakpak Medical Center, Marawi City, Philippines; 2Department of Surgery, Seoul National University
Bundang Hospital, Seoul National University College of Medicine, Seongnam, Korea; 3Department of Surgery, Tamil Nadu Dr. MGR
Medical University, Chennai, India

Laparoscopic liver resection (LLR) is becoming widely accepted for the treatment of hepatocellular carcinoma (HCC).
Laparoscopic left lateral sectionectomy and minor laparoscopic liver resection are now considered standard approaches,
especially for tumors located in the anterolateral segments of the liver. Laparoscopic left lateral sectionectomy in adult
donors is also gaining acceptance for child liver transplantation in many centers. Major LLRs, including left hepatectomy
and right hepatectomy, have been recently attempted. Laparoscopic donor hepatectomy is becoming more popular
owing to increasing demand from young living donors who appreciate its minimal invasiveness and excellent cosmetic
outcomes. Several centers have performed total laparoscopic donor right hepatectomy in adult-to-adult living donor
liver transplantation. Many meta-analyses have shown that LLR is better than open liver resection in terms of short-term
outcomes, principally cosmetic outcomes. Although no randomized control trials have compared LLR with open liver
resection, the long-term oncologic outcomes were similar for both procedures in recent case-matched studies.
(Clin Mol Hepatol 2016;22:212-218)
Keywords: Laparoscopy; Hepatectomy; Outcome; Prognosis; Recurrence

INTRODUCTION liver cirrhosis. However, the scarcity of donors precludes trans-

plantation in all patients with early HCC.2 Liver resection for
Hepatocellular carcinoma (HCC) is the fifth most common HCC is now considered to be a safer procedure than was previ-
malignant tumor worldwide, accounting for 5.6% of all human ously believed owing to technical advances and improvements
cancers, and is the most common primary liver cancer.1 It is in postoperative patient management.3-6 Accordingly, in many
also the third most common cause of cancer-related deaths centers, liver resection is still the first-line treatment for HCC in
worldwide.2 The number of new cases is estimated to range patients with compensated cirrhosis.7 Since the first laparo-
from 500,000 to 1 million per year.1 Up to 80–90% of HCCs scopic liver wedge resection was reported in 1992, an increas-
develop in a cirrhotic liver.2 ing number of reports have described the feasibility, safety,
Liver transplantation appears to be effective treatment ap- and adequacy of laparoscopic hepatic procedures.8-11 Now,
proach because it treats both the cancer and the underlying laparoscopic liver resection (LLR) is commonly performed in

Abbreviations: Corresponding author : Jai Young Cho

HCC, hepatocellular carcinoma; LLR, laparoscopic liver resection; OLR, open liver Department of Surgery, Seoul National University Bundang Hospital,
resection; RCT, randomized controlled trial 82 Gumi-ro 173beon-gil, Bundang-gu, Seongnam 13620, Korea
Tel: +82-31-787-7098, Fax: +82-31-787-4078
E-mail: [email protected]

Received : Apr. 30, 2016 / Accepted : May 3, 2016

Copyright © 2016 by The Korean Association for the Study of the Liver
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/)
which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
 Hanisah Guro, et al.
Laparoscopic hepatectomy for HCC

patients with HCC and chronic liver disease. ability to explore the deeper regions of the liver.16 Therefore,
The indications for LLR have been changed substantially LLR has been reserved for patients who require limited resec-
since its introduction. Initially, LLR was limited to the treatment tion of tumors located on the left side of the liver. The recent
of benign diseases. However, with increasing know-ledge of improvements in laparoscopic techniques and the introduction
this procedure, its indications have widened to include malig- of new technologies mean that LLR is technically feasible and
nant disease such as HCC and liver metastasis of colorectal safe for tumors on the right side of the liver.17 The first interna-
cancer. The extent of resection has also grown over time.12 tional position statement on LLR published in 2008 stated that
Major liver resection, such as right or left hemihepatectomy, the best indications for LLR were patients with solitary lesions,
has been performed more frequently in recent years.13,14 ≤ 5 cm in diameter, located in the peripheral liver segments
Laparoscopic left lateral sectionectomy is now regarded as a (i.e. segments 2–6; Fig. 1). Laparoscopic left lateral sectionec-
standard treatment option. By contrast, it will take many years tomy should be considered as the standard of care, but major
for LLR to become a standard procedure for treating all kinds hepatectomy, such as right hepatectomy, should be reserved
of HCC.15 Extending the indications, the introduction of ad- for experienced surgeons.15
vanced techniques, and outcomes similar to those of open liver Improved laparoscopic techniques, better visualization of the
resection (OLR) are required for LLR to become a standard pro- operative field using a flexible laparoscope, and routine use of
cedure in HCC.9 a laparoscopic cavitron ultrasonic surgical aspirator for tran-
The aim of this review is to assess the current indications, secting the deeper portion of the liver parenchyma have al-
advantages, and limitations of laparoscopic surgery for HCC lowed laparoscopic left lateral sectionectomy to be performed
resection. We will also discuss the feasibility of LLR and its on- more widely.18-20 LLR for HCC located in the posterosuperior
cologic outcomes compared to OLR. The information in this re- segments in selected patients was reported to be safe and fea-
view was extracted from a literature search of Medline. sible, and offered comparable oncologic outcomes to those of
OLR. Other benefits of LLR include reduced blood loss, fewer
complications, and shorter postoperative hospital stay com-
BEST INDICATIONS FOR LLR pared with open resection.21

Tumor location Presence of cirrhosis

Unlike laparoscopic cholecystectomy, laparoscopy is not Cirrhosis precedes HCC in approximately 80%–90% of cases
widely accepted for liver resection because of the technical dif- worldwide.22 Asian countries, especially, have a disproportion-
ficulty associated with parenchymal transection, hemostasis at ately high prevalence of HCC, mainly because hepatitis B and
the transection plane, the risk of air embolism, and limited C viruses are endemic in these countries,23 and chronic infec-
tion is associated with high risk of liver cirrhosis and HCC.24
When considering liver resection in patients with liver cirrhosis,
it is important to consider the degree of surgical stress placed
on the patient and the liver, as well as the oncological out-
comes.8 Decompensated cirrhosis is generally considered to be
a contraindication to liver resection and thereby LLR.25 Uncon-
trolled portal hypertension, including esophageal varices and
low platelet count, is also usually considered as an exclusion
criterion for LLR.26 Anatomical liver resection is preferred for
HCC because of its tendency to invade the portal veins and
spread along the intrasegmental branches.27
Figure 1. The peripheral area of anterolateral segments (segments 2, 5, 6, Major advantages of laparoscopy are the rapid recovery of
and lower part of 4) is considered to be a favorable location of tumors for
patients and the shorter hospital stay compared with open sur-
laparoscopic liver resection, whereas the posterosuperior segments (seg-
ments 1, 7, 8, and upper part of 4) of the liver are unfavorable locations. gery, as previously reported for LLR of HCC.28,29 These advan-

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 Clin Mol Hepatol
Volume_22 Number_2 June 2016

tages are related to less postoperative pain, early ambulation, pared 17 questions in 2 categories—benefits and risks, and
early return of oral feeding, and lower incidence of postopera- techniques of LLR. Each question was assigned to a working
tive complications after LLR. Another important advantage of group of 3–7 members of the expert panel who were selected
LLR in cirrhotic patients is the lower incidence of postoperative based on their scientific and clinical activities. The jury con-
liver failure and ascites. This may be due to the reduced inva- cluded that minor LLRs had become standard practice (IDEAL
siveness of laparoscopy, which helps to preserve the abdomi- 3) and that major liver resections were innovative procedures
nal musculature by avoiding large abdominal incisions, pre- in the exploratory phase (IDEAL 2b). Continued cautious intro-
serve the parietal circulation, and minimize liver manipulation.8 duction of major LLRs was recommended. All of the evidence
available for scrutiny was considered to be of low quality by
GRADE, which prompted the recommendation for higher qual-
RECOMMENDATIONS OF THE FIRST AND ity evaluative studies. The expert panel developed recommen-
SECOND CONSENSUS MEETINGS FOR LLR dations regarding preoperative evaluation, bleeding control,
transection methods, anatomical approaches, and equipment.
Because the potential applications for LLR have expanded Both the expert panel and jury recognized the need for a for-
considerably in the last 15 years,28,30,31 an first International mal structure of education for surgeons interested in perform-
Consensus Conference on LLR was convened in Louisville, Ken- ing major LLR because of the steep learning curve.34
tucky, in 2008.15 The experts discussed achievements and rec-
ommendations for this approach.15 This consensus statement
defined the current international position on laparoscopic liver RETROSPECTIVE COMPARISON OF
surgery as “a safe and effective approach for the management OUTCOMES BETWEEN LAPAROSCOPIC AND
of surgical liver disease in the hands of trained surgeons with OPEN LIVER RESECTION
experience in hepatobiliary and laparoscopic surgery.” It also
stated that the best indications for LLR were patients with soli- Over the past decade, LLR has progressed internationally fol-
tary lesions, ≤ 5 cm in diameter, located in the peripheral liver lowing advances in technology and the increasing experience
segments (i.e. segments 2–6) and that laparoscopic left lateral of liver surgeons. Indeed, more than 9,000 procedures were
sectionectomy should be considered as the standard of care. If reported in the English literature.35 With the proper selection
local resection of HCC is performed, it should involve anatomi- of patients, LLR is considered as a safe technique, with mor-
cal segmental resection, if possible, considering the overall tality and morbidity rates of 0% and 15%, respectively.36 Since
function of the liver. This is because this procedure is associat- the first case was reported, an increasing number of case-se-
ed with lower local recurrence rates and should be used in- ries have been published especially from the beginning of new
stead of tumorectomy. Since then, LLR has been introduced to millenium.37 LLR was initially performed for low-risk opera-
middle-tier centers as well as high-volume and/or specialized tions, including the excision of benign hepatic lesions. The
centers.32 Moreover, the number of HCC cases treated by LLR techniques have gradually become incorporated into the prac-
has increased over the last 5 years, especially in Asia and Eu- tices of most liver centers, and LLR is now widely accepted for
rope.33 the management of benign and malignant liver tumors.38 In a
Six years later, the second International Consensus Confer- global survey of the current practices of liver surgery, Yoshihiro
ence on LLR was held to evaluate the current status of LLR and et al. reported that 88% of the participating centers had incor-
to develop recommendations and guidelines. This goal was porated laparoscopic approaches into liver surgery.33
achieved through analysis of the available literature and expert To our knowledge, no randomized controlled trials (RCT)
presentations, which including videos presented to an inde- have compared the outcomes between LLR and OLR. However,
pendent jury. The organizing committee invited 43 respected several retrospective case–cohort matched studies have com-
surgeons from 18 countries. The expert panel comprised 34 pared these two procedures. The majority of studies showed
members, with demonstrated experience in LLR, and the jury that LLR has major benefits compared with OLR. LLR was as-
contained 9 members. The expert panel provided evidence and sociated with less intraoperative blood loss, less postoperative
developed recommendations. The organizing committee pre- pain medication requirement, earlier return of oral feeding,

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 Hanisah Guro, et al.
Laparoscopic hepatectomy for HCC

Table 1. Previous studies comparing the outcomes of laparoscopic liver resection versus open resection.
Operative Hospital Resection
Author Type Blood loss Transfusion Complications
time stay margin
Zhou et al. [40] Meta-analysis LLR < OLR LLR < OLR NSD LLR < OLR LLR < OLR NSD
(2011) 21 studies
Rao et al. [41] Systematic review LLR < OLR LLR < OLR NSD LLR < OLR LLR < OLR NSD
(2011) 10 studies
Fancellu et al. [42] Meta-analysis LLR < OLR LLR < OLR NSD LLR < OLR LLR < OLR NSD
(2011) 9 studies
Li et al. [43] Meta-analysis LLR < OLR LLR < OLR NSD LLR < OLR LLR < OLR NSD
(2012) 10 studies
Xiong et al. [44] Meta-analysis LLR < OLR LLR < OLR NSD LLR < OLR LLR < OLR NSD
(2012) 16 studies
Yin et al. [45] Meta-analysis LLR < OLR LLR < OLR NSD LLR < OLR LLR < OLR NSD
(2013) 15 studies
LLR, laparoscopic liver resection; OLR, open liver resection; NSD, no significant difference.

Table 2. Recent studies on long-term outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma
1 year 3 year 5 year Overall and
Study Type 1 year DFS 3 year DFS 5 year DFS
survival survival survival DFS
Lee et al. [50] Case matched L - 86.9% L – 81.8% L – 76% L – 78.8% L – 51% L – 45.3% NSD
(2011) O - 98% O – 80.6% O – 76.1% O – 69.2% O – 55.9% O – 55.9%
Parks et al. [51] Meta-analysis L – 92% L – 77.7% L – 61.9% NA NA NA NA
(2014) O – 91.3% O – 76.5% O – 56.5%
Cheung et al. Retrospective L – 96.6% L – 87.5% L – 76.6% L – 87.3% L – 72.6% L – 54.5% NA
[52] (2013) O – 95.2% O – 72.9% O – 57% O – 63.5% O – 50% O – 44.3%
Kim et al. [53] Case matched L – 100% L – 100% L – 92.2% L – 81.7% L – 61.7% L – 54% NSD
(2014) with PSM O – 96.5% O – 92.2% O – 87.7% O – 78.6% O – 60.9% O – 40.1%
Han et al. [54] Case matched L – 91.6% L – 87.5% L – 76.4% L – 69.7% L – 52% L – 44.2% NSD
(2015) with PSM O – 93.1% O – 87.8% O – 73.2% O – 74.7% O – 49.5% O – 41.2%
Takahara et al. Case matched L – 95.8% L – 86.2% L – 76.8% L – 83.7% L – 58.3% L – 40.7% NSD
[46] (2015) with PSM O – 95.8% O – 84% O – 70.9% O – 79.6% O – 50.4% O – 39.3%
DFS, disease free survival; PSM, propensity score matching; L, laparoscopic liver resection; O, open liver resection; NSD, no significant difference; NA, not
analyzed.

and shorter hospital stay compared with OLR. In addition, from time was shorter with OLR than with LLR. LLR was also associ-
a financial standpoint, although the minimally invasive LLR ap- ated with shorter hospital stay and earlier return of oral feed-
proach was associated with higher operating room costs in ing. However, all of these significant results were associated
some studies, the total hospital costs were either offset or im- with significant heterogeneity in the evaluated studies. There
proved by LLR because of the shorter hospital stay. In addition, were no differences between the two groups in terms of ad-
LLR did not compromise oncological measures such as margin verse outcomes in the early postoperative period. Neverthe-
status, disease-free survival, or overall survival, but did im- less, a significant finding was the lower number of positive re-
prove short-term perioperative outcomes.39 section margins in the LLR group than in the OLR group. This
A systematic review published in 2012 compared LLR with finding was not associated with significant heterogeneity. The
OLR.41 The data analysis suggested that LLR was associated other variables associated with oncological clearance were not
with improvements in most of the perioperative factors, includ- significantly different between LLR and OLR. Another impor-
ing blood loss, the number of patients requiring transfusion, tant result was that LLR was associated with a significant re-
and the use of portal triad clamping. By contrast, the operation duction in overall morbidity compared with OLR.

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 Clin Mol Hepatol
Volume_22 Number_2 June 2016

In the last 5 years, several meta-analyses of studies compar- CONCLUSION

ing LLR and OLR for malignant lesions have been published
(Table 1). All of these meta-analyses concluded that LLR is su- LLR is now considered as a standard procedure in the man-
perior to OLR in terms of perioperative outcomes. The opera- agement of HCC in some settings, and it is increasingly being
tion time was not significantly different between LLR and OLR, performed worldwide. The short- and long-term outcomes of
even though operation time was shorter for OLR in prior stud- LLR were comparable to those of OLR.
ies. The absence of a difference in the meta-analyses could be
explained by recent advances in surgical instruments, accumu- Acknowledgements
lated experience, and overcoming the learning curve. Further- This work was supported by grant no 13-2015-024 from the
more, no technique compromised the oncological out- SNUBH Research Fund.
comes.40-45 Unfortunately, it is impossible to reach a convincing
conclusion regarding the bene-fits and risks of LLR over OLR in Conflicts of Interest
the absence of RCTs.46 However, Abraham et al. recently re- The authors have no conflicts to disclose.
ported that a meta-analysis of well-designed non-randomized
controlled trials of surgical procedures is probably as reliable as
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