Laparoscopic liver resection for hepatocellular carcinoma

Ibrahim Dagher Æ Panagiotis Lainas Æ Alessio Carloni ÆCecile Caillard Æ Axele Champault Æ Claude Smadja ÆDominique Franco

Received: 20 February 2007 / Accepted: 19 June 2007 / Published online: 18 August 2007

� Springer Science+Business Media, LLC 2007

Abstract

Background Single, small hepatocarcinomas (HCC) are

still an indication for partial liver resection in patients

ineligible for transplantation. Anatomical resections are

recommended for oncological reasons. The mini-invasive

approach of laparoscopy should minimize hepatic and

parietal injury, thereby decreasing the risk of liver failure

and ascites. However, the oncological results of this ap-

proach and its presumed benefits remain undemonstrated.

We evaluated the short- and midterm results of laparo-

scopic liver resections for HCC.

Methods Between 1999 and 2006, we performed 32

laparoscopic liver resections for HCC. Mean tumor size

was 3.8 ± 2 cm and the mean age of the patients was

65 ± 11 years. Twenty-two patients had cirrhosis (21 Child

A and one Child C). Operative and postoperative results

were analyzed, together with recurrence and survival rates.

Results We carried out 13 unisegmentectomies, nine bi-

segmentectomies, one trisegmentectomy, two right hepa-

tectomies, one left hepatectomy, and six atypical

resections. The duration of the operation was 231 ± 101

minutes. Conversion to laparotomy was required in three

patients (9%), none in emergency situations. Mean blood

loss was 461 ml, with five patients (15.6%) requiring blood

transfusion. The mean surgical margin was 10.4 mm. One

cirrhotic patient (Child C) underwent surgery for a partially

ruptured tumor and died of liver failure. Two patients had

ascites and no transient liver failure occurred in the other

19 cirrhotic patients. Mean hospital stay was 7.1 days.

During a mean follow-up of 26 months, 10 patients (31%)

presented recurrence within the liver. None of the patients

had peritoneal carcinomatosis or trocar site recurrence.

Three-year overall and disease-free survival rates were

71.9% and 54.5%, respectively.

Conclusions Laparoscopic liver resection for HCC is

feasible and well tolerated. Midterm survival and recur-

rence rates are similar to those after laparotomy.

Keywords Laparoscopy � Liver resection �Hepatocarcinoma

Laparoscopy was slow to develop in liver surgery and was

initially used for small wedge resections or the fenestration

of hepatic cysts [1–3]. Several limited series of minor

laparoscopic hepatectomies were initially reported, mainly

for benign lesions [4–7]. Most surgeons were skeptical

about the use of laparoscopy for cancers, due to the risk of

dissemination [8, 9]. Advances in laparoscopic cancer care

and increasing experience of liver surgeons with laparos-

copy have carved out a new role for laparoscopic surgery in

the management of hepatic tumors.

Hepatocellular carcinomas (HCC), particularly in cir-

rhotic patients, are generally small and discovered during

screening examinations [10]. Cirrhotic patients have lim-

ited access to liver transplantation because of their age,

persistent alcohol abuse, associated diseases, and espe-

cially donor shortage. In addition, tumor progression in

patients awaiting transplantation may necessitate an inter-

mediary bridging treatment [11, 12]. Radiofrequency

ablation techniques have their limitations, such as sub-

I. Dagher � P. Lainas � A. Carloni � C. Caillard �A. Champault � C. Smadja � D. Franco

Department of General Surgery, Antoine Beclere Hospital,

157 Avenue de la Porte de Trivaux, Clamart,

France

I. Dagher (&) � A. Carloni � C. Smadja � D. Franco

Paris-Sud University, Kremlin-Bicetre, France

e-mail: ibrahim.dagher@abc.aphp.fr

123

Surg Endosc (2008) 22:372–378

DOI 10.1007/s00464-007-9487-2

capsular tumors or malignant tumors in the vicinity of

blood vessels [13, 14]. On the other hand, surgical resec-

tion of HCC provides good oncological results. Laparos-

copy, a minimally invasive approach, should reduce

parietal and hepatic injury, preserving the collateral venous

circulation and thereby decreasing the incidence of post-

operative liver failure and ascites. However, laparoscopic

liver resection for HCC is limited to centers with experi-

ence in both laparoscopic surgery and the management of

cirrhotic patients. Few laparoscopic liver resections for

HCC were therefore reported before 2005 [4, 15–20], with

only two surgical teams reporting more than 20 patients in

the last two years [21, 22]. These studies demonstrated the

feasibility and safety of the procedure without increasing

tumor dissemination. However, the oncological results of

this approach and its presumed benefits remain uncertain.

We initiated a program of laparoscopic liver surgery for

HCC resections, based on our proficiency in the manage-

ment of cirrhotic patients and over 10 years of experience

in laparoscopic liver surgery. This work covers the largest

number of laparoscopic resections for HCC reported to

date. The aim of this study was to evaluate our results for

laparoscopic liver resection for HCC in terms of feasibility,

safety, outcome, recurrence and survival.

Patients and methods

From 1999 to 2006, we performed 89 liver resections by

laparoscopy, 32 of which (36%) were for HCC. Liver

transplantation was considered in all cases and non-eligible

patients were evaluated for resection. The criteria for pa-

tients’ selection were not modified by the use of laparos-

copy and included the following: noncirrhotic livers or

Child A cirrhosis, oesophageal varices £ 1 and platelet

count ‡ 80 · 109/L. Only one Child C patient underwent

surgery for a partially ruptured tumor of the left lobe, in our

early experience. Tumors smaller than 4 cm in diameter,

located in the inferior or anterior segments of the liver

(segments III, IV, V, and VI), were treated by segmental or

atypical resection. Larger tumors and those invading more

than three segments were treated by major hepatectomy,

provided hepatic function allowed such resection. Tumors

invading or adjacent to the portal pedicle or hepatic veins

were not considered suitable for laparoscopy. Patients were

informed about the innovative nature of the procedure and

prior consent was obtained. Liver resections were defined

according to Couinaud’s classification. Anatomical resec-

tions were preferred to atypical resections for removal of

the corresponding portal territory. However, nonanatomical

wedge resections were performed for small peripheral le-

sions. Vascular control of the portal vessels and the con-

cerned hepatic vein, and ligation of the portal pedicle were

carried out before parenchymal transection, whenever

possible. This procedure was typically sought for right

hepatectomy (segments V, VI, VII, and VIII), left hepa-

tectomy (segments II, III, and IV), and left lateral lobec-

tomy (segments II and III), but not for segmentectomies or

atypical resections. The Pringle maneuver was not used.

Surgical procedure

The technique used for laparoscopic liver resection has

been described elsewhere [23, 24]. In summary, patients

were maintained in a supine position regardless of tumor

location. Pneumoperitoneum was maintained below 11

mmHg. A 0o laparoscope was used in all cases and intra-

operative ultrasound was routinely carried out. The

parenchymal transection was performed using an ultrasonic

dissector (Dissectron; Satelec, Merignac, France) in the

first three patients, a harmonic scalpel (Ultracision; Ethi-

con, Issy les Moulineaux, France) in the following 10 pa-

tients and a thermofusion device (Ligasure; Tyco

Healthcare, Elancourt, France) in the last 19 patients.

Bipolar coagulation was used to prevent bleeding from

minor vessels in all patients. Large intraparenchymal

structures and portal pedicles were secured with absorbable

clips. In major resections, hepatic veins were divided using

a linear roticulating stapler (Endo GIA roticulator; Tyco

Healthcare, Elancourt, France). At the end of resection, the

hepatic stump was scrutinized for bleeding while the

pneumoperitoneum was lowered to 5–6 mmHg. The re-

sected liver was placed in a plastic bag and extracted,

without fragmentation, through a suprapubic horizontal

incision. None of the patients had any abdominal drainage.

The hand-assisted technique was not used.

Intraoperative complications and postoperative course

were assessed, together with data for outpatient follow-up,

including oncological check-ups every four months. The

data collected included duration of surgery, blood loss,

perioperative transfusions, conversions to laparotomy, liver

test results, tumor characteristics, surgical margins, post-

operative complications, hospital stay, and disease-free and

overall survival rates.

Statistical analysis was performed with JMP 6.0 soft-

ware (SAS Institute Inc. Cary, NC, USA), using the Mann-

Whitney test and the Kaplan-Meier method (for survival

rates). All p values less than 0.05 were considered statis-

tically significant.

Results

Between February 1999 and June 2006, 32 (28%) of 114

liver resections for HCC were performed by laparoscopy.

These 32 resections were carried out on 10 women and 22

Surg Endosc (2008) 22:372–378 373

123

men with a mean age of 65 ± 11 years (range: 44–79

years). The characteristics of the patients are summarized

in Table 1. The liver parenchyma was cirrhotic in 22 pa-

tients (69%), fibrotic in six patients (19%) and normal in

four patients (12%). The etiology of liver disease was

alcohol abuse in 14 cases, hepatitis C in nine cases, hep-

atitis B in two cases, and hemochromatosis in three cases.

The characteristics of the tumors are presented in table 2.

The mean size of the resected tumor was 3.8 ± 2 cm

(range: 1.5–8.5 cm). The mean surgical margin was

10.4 ± 9 mm and exceeded 5 mm in 25 patients (78%)

(Table 4). The free margin was larger in non cirrhotic than

in cirrhotic patients (13.1 vs. 8.1 mm), although this dif-

ference was not statistically significant. Portal vein embo-

lization was performed in two patients before right

hepatectomy on a cirrhotic liver. The types of liver resec-

tion are detailed in Table 3. The resection was anatomical

in 26 patients (81%). Extraparenchymal portal control was

achieved before liver transection in 17 patients (53%).

Primary control of the hepatic vein was achieved in all

major liver resections and left lateral lobectomies.

Intraoperative results

Surgical results are summarized in Table 4. The mean

duration of the operation was 231 ± 101 min (range: 96–

540 min). Mean operative blood loss was 461 ± 498 ml

(range: 100–1800 ml). Bleeding resulted from parenchymal

transection in all cases. Five patients (15.6%) required

blood transfusion (2.8 ± 1.5 packed red cell units). Con-

version to laparotomy was required in three patients (9%).

It was due to continuous bleeding during parenchymal

transection in two patients (bisegmentectomy V–VI and

segmentectomy V) and problems achieving exposure to-

gether with unsatisfactory progress during parenchymal

transection in the third case (trisegmentectomy V–VI–VII).

The decision to convert to laparotomy was not once taken

in emergency conditions or due to life-threatening bleeding

or major vessel injury. No conversions were required in the

last 17 patients. Laparoscopic radiofrequency was used in

addition to surgery in three patients. Radiofrequency was

used to treat a second tumor located away from the resected

tumor in two cases and to treat an insufficient free margin

in the third patient. In this patient, the tumor was close to

the hepatic stump, which was subsequently treated by ra-

diofrequency. The conversion rate was similar in cirrhotic

and non cirrhotic patients (9% and 10%, respectively).

Blood loss was greater in cirrhotic than in noncirrhotic

patients (570 vs. 381 ml), although this difference was not

statistically significant (p = 0.36).

Postoperative results

Specific postoperative complications occurred in five pa-

tients (15.6%, Table 5). These complications included

ascites in two patients, bleeding from the liver stump in the

third patient requiring reoperation by laparoscopy on the

Table 1 Patients characteristics

Age, years (mean ± SD) 65.0 ± 11.0

Gender ratio (male:female) 22:10

ASA classification

ASA I, n (%) 2 (6.2)

ASA II, n (%) 19 (59.4)

ASA III, n (%) 11 (34.4)

Child classification for the 22 cirrhotic patients

A / B / C 21 / 0 / 1

Preoperative laboratory results, mean ± SD (range)

Total bilirubin (lmol/L) 12.1 ± 6.8 (4–30)

AST (IU/L) 38 ± 25.4 (14–116)

ALT (IU/L) 34.7 ± 18.8 (12–89)

Prothrombin rate (%) 86.3 ± 18 (61–100)

ASA: American Society of Anesthesiologists physical status score

Total bilirubin, normal value: 2–17lmol/L. AST: aspartate amino-

transferase (normal value, 14–50 IU/L); ALT: alanine aminotrans-

ferase (normal value, 11–60 IU/L)

Table 2 Liver and tumor characteristics

II

III

VIII

V

IV

VII 11

6

64

2

3

II

III

VIII

V

IV

VII 11

6

64

2

3

3.8 ± 2 Tumor size, cm (mean ± SD)

Tumor localisation

left lateral lobe: 11

segment IV: 6

right lobe : 15

Cirrhosis

Fibrosis (F1: F2 : F3)

Normal liver

22

6 (1:2:3)

4

Table 3 Types of liver resection

n (%)

Right hepatectomy 2 (6.2)

Left hepatectomy (segments II, III, IV) 1 (3.1)

Left lateral lobectomy (segments II, III) 7 (21.8)

Trisegmentectomy (segments V, VI, VII) 1 (3.1)

Bisegmentectomy (segments V, VI) 2 (6.2)

Segmentectomy 13 (40.6)

Segment III 4

Segment IV 3

Segment V 6

Atypical resection 6 (18.7)

374 Surg Endosc (2008) 22:372–378

123

day after a segmentectomy IV, biliary collection drained

percutaneously in the fourth patient and trocar site bleeding

in the fifth patient. The Child C patient who underwent

surgery for a partially ruptured tumor of the left lobe died

of liver failure. Three patients (9.3%) developed nonspe-

cific complications, including cardiac failure (n = 1) and

respiratory complications (n = 2). Mean hospital stay was

7.1 ± 7 days (range: 2–33 days).

Survival and recurrence

Over a mean follow-up period of 26 months (range: 6–78

months), 10 patients presented recurrence (31%). All

recurrences were within the liver, adjacent to the stump in

two patients and in another liver segment in the remaining

eight patients. The free parenchymal margin in the two

patients with recurrence near the stump was 6 and 9 mm.

During the study period, none of the patients displayed

peritoneal carcinomatosis or port-site recurrence. Recur-

rence was treated by a second resection in three patients,

intraoperative radiofrequency in two patients, percutaneous

radiofrequency in two patients, and transarterial chemo-

embolization in one patient. The recurrence was not treated

in two patients, due to contraindications for repeated sur-

gery, radiofrequency ablation or chemoembolization. In

addition to the patient who died during the postoperative

period, six patients (18.7%) died during the study period.

Death resulted from recurrence in three patients, cardiac

failure in two patients and peritonitis in one patient. Three-

year overall and disease-free survival rates were 71.9% and

54.5%, respectively (Fig. 1).

Discussion

Hepatocellular carcinomas can frequently be diagnosed at

an early stage in the surveillance of patients with chronic

liver diseases. Orthotopic liver transplantation seems to

offer the highest rate of recurrence-free survival in patients

with HCC. However, only selected patients can be referred

for transplantation. In addition, the indication of liver

transplantation for small solitary HCC is still under dis-

cussion and partial resection may be proposed as a treat-

ment with curative intent [25] or as a bridge to

transplantation [22].

The most frequently required type of liver resection for

small single HCC is limited anatomical resection. Such

resections are particularly suitable for laparoscopy. How-

ever liver resections in cirrhotic patients are technically

more difficult than in patients with a normal liver, pre-

senting added complications, such as profuse bleeding

during liver mobilization and parenchymal transection. A

few reports have already suggested that laparoscopic

resections may be successfully performed in patients with

HCC and cirrhosis [16, 21, 22, 26].

In this study, laparoscopic liver resections were suc-

cessfully performed in 91% of the patients. Only three

patients required conversion to open surgery, each during

segmental resection in the right liver. Laparoscopic resec-

tions of segment V or segments V and VI are often con-

sidered to be easy technical procedures. However, this type

of liver resection combines a large liver stump with two

transection planes crossing at right angles. Furthermore,

Table 4 Intraoperative results

Operative time, mean ± SD (min) 231 ± 101

Blood loss, mean ± SD (ml) 461 ± 498

Transfusion, n (%) 5 (15.6)

Packed red cell units 2.8 ± 1.5

Conversion, n (%)

Surgical margin

Mean ± SD (mm) 10.4 ± 9

> 10 mm, n (%) 15 (47)

5–10 mm, n (%) 10 (31)

< 5 mm, n (%) 7 (22)

Table 5 Postoperative results

Mortality, n (%) 1 (3.1)

Specific morbidity, n (%) 5 (15.6)

Reoperation for hemorrhage 1

Ascites 2

Biliary collection 1

Trocar site bleeding 1

General morbidity, n (%) 3 (9.3)

Cardiac failure 1

Respiratory complication 2

Hospital stay (days)

Mean ± SD 7.1 ± 7

Fig. 1 Overall (continuous line) and disease free (dotted line)

survival curves

Surg Endosc (2008) 22:372–378 375

123

the anatomical limits of these segments are difficult to

define, particularly in cirrhotic livers. The problems expe-

rienced with these resections generally arose deep in the

liver, at the junction between the two transection planes,

where bleeding often occurred. We therefore modified our

technique for segmentectomy V, approaching the portal

pedicle early during parenchymal transection, following

ultrasound localization. In other anatomical resections,

such as left lateral lobectomies, right and left hepatecto-

mies and segmentectomies III and IV, extraparenchymal

control of the feeding vessels was achieved without tech-

nical difficulties. No conversions were required in the last

17 patients.

In our experience, as in other laparoscopic studies [21,

27], blood loss was no greater than that in open surgery,

despite the longer operation. This was probably due to the

use of new coagulation and transection devices. In addi-

tion, pneumoperitoneum can also reduce the bleeding from

hepatic vein branches. The blood loss in this study was

similar to that reported in other laparoscopic studies in

which hepatic pedicle clamping was used [22, 26, 27],

despite more major resections being performed. This may

be due to prior control of the portal pedicle, which was

achieved whenever possible (53%). As expected, blood

loss was greater with cirrhotic than with noncirrhotic livers,

although this difference was not statistically significant.

Postoperative morbidity and mortality rates were low

after laparoscopic liver resections for HCC. One patient

with poor preoperative liver function and a partially rup-

tured tumor died from progressive liver failure. Laparos-

copy does not prevent severe liver failure, and does not

facilitate resection any more than open surgery in patients

with poor liver function, in contrast to what has been

suggested in other studies [28]. However, the risk of ascites

after laparoscopy appeared to be lower than after open

resections [27], in which the large abdominal incision re-

duces abdominal counterpressure. Ascites occurred in two

of our patients, with leakage through a trocar site in one

case. The measures used to prevent ascites after open liver

resections in cirrhotic patients should also be used in lap-

aroscopy. In addition, great care should be taken in the

closure of each trocar incision, to prevent ascites leakage

and possible postoperative infection. Most other postoper-

ative complications could be treated by further laparoscopy

or by percutaneous drainage.

Neither peritoneal carcinomatosis nor port-site recur-

rence were observed following HCC resection by lapa-

roscopy. Studies of other digestive cancers have confirmed

that initial fears of cancer growth and dissemination after

laparoscopy are unfounded [29, 30]. The parenchymal

margin in our study was free of tumor cells in all patients,

with a margin of less than 5 mm in only seven cases.

However, two patients presented recurrence near the he-

patic stump, although the margin exceeded 5 mm in both.

This frequency is slightly higher than that obtained in our

study of open liver resection for HCC [31]. The exact

location of the tumor and transection planes must be pre-

cisely defined to ensure that an adequate surgical margin is

obtained. The use of intraoperative ultrasound is thus even

more important in laparoscopy than in open surgery, be-

cause the tumor cannot be identified by palpation. The

limits of the resection should be carefully marked on the

liver surface using ultrasound, particularly for segmental or

atypical resections.

The recurrence rate was similar to those reported for

other laparoscopic studies [16, 22] and for open resection

of HCC [32–34]. Laparoscopy did not increase the fre-

quency of tumor recurrence in the liver or elsewhere. As

often observed following HCC resections, most recur-

rences occurred away from the hepatic stump. Disease-free

survival in our study was within the range of reported

disease-free survival after HCC resection [16, 26, 27].

Prospective comparative studies are required to determine

whether laparoscopy improves the results of HCC resec-

tion, as previously suggested [27].

Which HCC can be resected by laparoscopy? Almost all

types of liver resection have already been performed by

laparoscopy [22, 23, 35–37]. However, it is currently ac-

cepted that resections of anterior and inferior liver seg-

ments are much easier to perform than those of posterior

and superior segments. In our experience, major anatomi-

cal hepatectomies and left lateral lobectomies are easy to

perform, as extraparenchymal dissection of the portal

pedicles and hepatic veins is possible before transection.

This prior control of the feeding vessels facilitates tran-

section and minimizes blood loss. We consider the lapa-

roscopic approach to be the treatment of choice for left

lateral lobectomies and would recommend it in all other

anatomical resections, even major ones. We resected tu-

mors up to 8.5 cm in size, but large tumors remain difficult

to handle and are associated with a higher risk of tumor

injury during liver mobilization. This is particularly true if

the tumor is subcapsular, close to the parenchymal tran-

section plane or located in the posterior segments of the

right liver. Tumors arising in the vicinity of major blood

vessels have also been considered unsuitable for laparos-

copy. However, the image magnification achieved in lap-

aroscopy may result in the dissection being safer than for

laparotomy, indicating that this view should be reconsid-

ered. HCC resection may occasionally require the removal

of a neoplastic thrombus from a large portal branch. Even

this procedure could be performed by laparoscopy, al-

though it has not yet been reported.

Our study shows that laparoscopic liver resection for

HCC in patients with preserved liver function is a safe

procedure with good operative and oncological results.

376 Surg Endosc (2008) 22:372–378

123

Acknowledgements We thank Anthony Kazan for his suggestions

and reading of the manuscript; and Helene Agostini, Clinical Re-

search Unit, Paris-Sud University, for assistance with statistical

analysis.

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