AJ Koffron

B Descottes

C Simillis

D Cherqui

David A. Geller

H Kaneko

H Nelson

HY Chen

JF Buell

JF Gigot

Kevin Tri Nguyen

KT Nguyen

N O’Rourke

English

PubMed

Springer - Publisher Connector

EDITORIAL
Is Laparoscopic Liver Resection Safe and Comparable
to Open Liver Resection for Hepatocellular Carcinoma?
Kevin Tri Nguyen, MD, PhD and David A. Geller, MD
UPMC Liver Cancer Center, Starzl Transplant Institute, Department of Surgery, University of Pittsburgh, Pittsburgh, PA
The field of surgery has evolved to increasingly incor-
porate minimally invasive approaches. Although the use of
laparoscopy gained rapid and widespread acceptance for
the treatment of benign diseases such as biliary and gas-
troesophageal reflux diseases, its utility in the treatment of
cancer has been more cautious due to initial concerns of
compromising oncologic principles and fears of port-site
recurrence. For colon cancer, a 10-year randomized clinical
trial was conducted to compare laparoscopically assisted
versus open colectomy, showing that the rates of recur-
rence were similar between the two groups and suggesting
that the laparoscopic approach was an acceptable alterna-
tive to open resection for colon cancer.1 Liver surgery itself
has evolved significantly with a better understanding of
liver anatomical segments, enhanced imaging, improve-
ments in anesthesia techniques including maintenance of
low central pressures during liver mobilization and resec-
tion to prevent bleeding, and improved postoperative care
and nursing. Minimally invasive liver resection is the next
challenge; however, it has been slower to gain widespread
acceptance, especially for cancer, due to concerns of
compromising oncologic principles, uncontrollable hem-
orrhage, bile leakage, and air embolism.2 In addition, there
has been lack of adequate training of liver surgeons in both
open liver surgery and minimally invasive techniques.
No randomized controlled trial has compared laparo-
scopic liver resection with the traditional open liver
resection; however, numerous case series have shown that
it is safe and feasible in experienced hands.3–13 Initially
performed with nonanatomical wedge resections of
peripheral liver lesions, laparoscopic liver resections are
being performed with anatomical liver resections (left
lateral sectionectomy, left hepatectomy, right hepatectomy,
extended left hepatectomy, extended right hepatectomy,
and central hepatectomy). Almost 3,000 laparoscopic liver
resections have been reported in the world literature, 50%
of which were for malignancies, with a cumulative mor-
bidity and mortality of 10.5% and 0.3%, respectively.14
In the absence of a randomized controlled clinical trial,
a case-controlled analysis provides another option to
compare laparoscopic liver resection with open liver
resection. The article by Sarpel et al., entitled ‘‘Outcome
for patients treated with laparoscopic versus open resec-
tion of hepatocellular carcinoma: a case-matched
analysis’’ sought to compare the outcomes of laparoscopic
versus open liver resection for hepatocellular carcinoma
(HCC), with specific emphasis on surgical margin status
and survival.15 To this end, the authors performed a case-
matched analysis between 20 laparoscopic cases and 56
matched open controls based on cirrhosis and tumor size
within 10%. The laparoscopic procedure employed four or
five trocars, with a hand port as needed. Vascular inflow
control with the Pringle maneuver was not performed and
parenchymal transection utilized a combination of har-
monic scalpel and vascular staplers. Open hepatectomies
were performed with a curved subcostal or chevron inci-
sion with superior extension. The Pringle maneuver was
routinely performed and parenchymal transection was by a
modified crush-clamp technique using a closed Metzen-
baum scissors to divide the liver tissue and clips to ligate
the exposed structures. Outcome measures that were ana-
lyzed included operative time, intraoperative transfusion
rate, margin status (positive if B3 mm), length of hospital
stay, 30-day readmission rate, tumor recurrence, and
survival.
The study period for the laparoscopic group was 2004–
2007 and for the open hepatectomy group was 1997–2007.
There were no significant differences reported between the
two groups based on age, gender, baseline cirrhosis, and
 Society of Surgical Oncology 2009
Published Online: 2 May 2009
D. A. Geller, MD
e-mail: gellerda@upmc.edu
Ann Surg Oncol (2009) 16:1765–1767
DOI 10.1245/s10434-009-0496-3
tumor size; however, there was a trend towards older
patients undergoing laparoscopic surgery compared with
the open group (64 years versus 58 years, p = 0.054).
Results of univariate and multivariate analyses showed that
there was no significant difference in the operative time,
rates of intraoperative transfusion, rates of positive margins
or 30-day readmission rates between the laparoscopic and
open resection groups. However, the percentage of patients
with length of stay C6 days was significantly higher in
patients undergoing open hepatectomy [odds ratio 0.09,
95% confidence interval (CI) 0.03–0.32]. After median
follow-up of 24 months for the laparoscopic group and
18 months for the open group, the authors found no sig-
nificant difference in overall survival (hazard ratio 0.11,
95% CI 0.01–1.01) and disease-free survival (hazard ratio
0.76, 95% CI = 0.30–1.96) between the two groups. For
the laparoscopic group, the projected 5-year overall sur-
vival was [ 95% and recurrence at 5 years was 50%;
however, this may be a generous projection, given that the
median follow-up for the laparoscopic group was 2 years
and at least 70% of patients in the sample should be
deceased to make sure the analysis, using censored data, is
correct.
This case-matched analysis by Sarpel et al. provides
evidence that laparoscopic liver resection for HCC is on-
cologically comparable to open liver resection for HCC, in
regards to surgical margin, overall survival, and disease-
free survival. The improved length of hospital stay in
patients undergoing laparoscopic liver resection suggest
that the benchmark criteria for discharge (ambulation,
tolerating oral intake, pain controlled with oral pain med-
ication) was reached in the laparoscopic group sooner than
in the open group. These results are comparable to those
reported in the literature on laparoscopic liver resection for
HCC. Cherqui et al. in 2006 provided midterm results
showing the safety, feasibility, and oncologic efficiency of
laparoscopic liver resection of 27 patients with HCC in a
background of chronic liver disease.12 Surgical margins
averaged 11 mm and overall 3-year overall and disease-
free survivals were 93% and 64%, respectively. Simillis
et al. in 2007 conducted a meta-analysis of eight studies,
totaling 409 resections, comparing 165 laparoscopic liver
resections (LLR) versus 244 open liver resections (OLR)
for benign and malignant lesions.16 From an oncological
standpoint, there was no differences in tumor-free margin
status, overall survival (5 year, 61% LLR versus 62%
OLR), and disease-free survival (5 year, 31% LLR versus
29% OLR) between laparoscopic and open liver resection
for cancer.16,17 In addition, the laparoscopic resection
group sustained less blood loss, achieved earlier oral
intake, and were discharged to home sooner than the open
resection group.
In summary, this study by Drs. Schwartz and Labow’s
group offers further support to the premise that laparo-
scopic hepatectomy for HCC provides short-term benefits
to patients without compromising long-term oncologic
outcomes, thus providing a safe and comparable alternative
to open liver resections for HCC in experienced hands.
Surgeons should be trained in performing both open liver
resections and advanced minimally invasive techniques.
Until a large randomized, controlled clinical trial compar-
ing laparoscopic with open liver resection for cancer is
initiated, similar to that performed for colon cancer, critics
of the minimally invasive approach will remain. However,
such a trial comparing laparoscopic with open hepatic
resection is likely to be challenging, as patients may resist
being randomized to a more invasive procedure. In addi-
tion, such a trial would require a large sample size to detect
small differences in complication rates. Alternatively, as
minimally invasive surgery is increasingly adopted by liver
surgeons, a registry to track all laparoscopic liver resec-
tions should be considered to track all perioperative
outcomes and help detect infrequent, but significant,
occurrences of complications that may be too small to be
detected by a clinical trial.
REFERENCES
1. Nelson H. A comparison of laparoscopically assisted and open
colectomy for colon cancer. The Clinical Outcomes of Surgical
Therapy Study Group. N Engl J Med. 2004;350(20):2050–9.
2. Nguyen KT, Gamblin TC, Geller DA. Laparoscopic liver resec-
tion for cancer. Future Oncol. 2008;4(5):661–70.
3. Buell JF, Thomas MT, Rudich S, et al. Experience with more
than 500 minimally invasive hepatic procedures. Ann Surg.
2008;248(3):475–86.
4. Koffron AJ, Auffenberg G, Kung R, Abecassis M. Evaluation of
300 minimally invasive liver resections at a single institution: less
is more. Ann Surg. 2007;246(3):385–92; (discussion 392–4).
5. Koffron AJ, Geller DA, Gamblin TC, Abecassis M. Laparoscopic
liver surgery: Shifting the management of liver tumors. Hepa-
tology. 2006;44(6):1694–700.
6. Cho JY, Han HS, Yoon YS, Shin SH. Experiences of laparo-
scopic liver resection including lesions in the posterosuperior
segments of the liver. Surg Endosc. 2008.
7. Chen HY, Juan CC, Ker CG. Laparoscopic liver surgery for
patients with hepatocellular carcinoma. Ann Surg Oncol.
2008;15(3):800–6.
8. Topal B, Fieuws S, Aerts R, et al. Laparoscopic versus open liver
resection of hepatic neoplasms: comparative analysis of short-
term results. Surg Endosc. 2008.
9. Descottes B, Glineur D, Lachachi F, et al. Laparoscopic liver
resection of benign liver tumors. Surg Endosc. 2003;17(1):23-30.
10. O’Rourke N, Shaw I, Nathanson L, et al. Laparoscopic resection
of hepatic colorectal metastases. HPB (Oxford). 2004;6(4):230-5.
11. Kaneko H, Otsuka Y, Tsuchiya M, et al. Application of devices
for safe laparoscopic hepatectomy. HPB (Oxford). 2008;
10(4):219–24.
12. Cherqui D, Laurent A, Tayar C, et al. Laparoscopic liver resec-
tion for peripheral hepatocellular carcinoma in patients with
1766 K. T. Nguyen, D. A. Geller
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2006;243(4):499–506.
13. Gigot JF, Glineur D, Santiago Azagra J, et al. Laparoscopic liver
resection for malignant liver tumors: preliminary results of a
multicenter European study. Ann Surg. 2002;236(1):90–7.
14. Nguyen KT, Gamblin TC, Geller DA. World review of laparo-
scopic liver resection – 2,804 patients. Ann Surg, (in press).
15. Sarpel U, Hefti M, Wisnievsky J, et al. Outcome for patients
treated with laparoscopic versus open resection of hepatocellular
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17. Kaneko H, Takagi S, Otsuka Y, et al. Laparoscopic liver
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Is Laparoscopic Liver Resection Safe and Comparable? 1767


Is Laparoscopic Liver Resection Safe and Comparable to Open Liver Resection for Hepatocellular Carcinoma?

Crossref

A comparison of laparoscopically assisted and open colectomy for colon cancer. The Clinical Outcomes of Surgical Therapy Study Group.

Application of devices for safe laparoscopic hepatectomy. HPB

Evaluation of 300 minimally invasive liver resections at a single institution: less is more.

Experience with more than 500 minimally invasive hepatic procedures. Ann Surg.

Experiences of laparoscopic liver resection including lesions in the posterosuperior segments of the liver. Surg Endosc.

Laparoscopic liver resection for cancer. Future Oncol.

Laparoscopic liver resection for malignant liver tumors: preliminary results of a multicenter European study. Ann Surg.

Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with 1766

Laparoscopic liver resection of benign liver tumors. Surg Endosc.

Laparoscopic liver resection of hepatocellular carcinoma.

Laparoscopic liver surgery for patients with hepatocellular carcinoma. Ann Surg Oncol.

Laparoscopic liver surgery: Shifting the management of liver tumors.

Laparoscopic resection of hepatic colorectal metastases. HPB

Laparoscopic versus open hepatic resections for benign and malignant neoplasms–a meta-analysis.

Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of shortterm results. Surg Endosc.

Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: a case-matched analysis. Ann Surg Oncol.

World review of laparoscopic liver resection – 2,804 patients. Ann Surg,

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Is Laparoscopic Liver Resection Safe and Comparable to Open Liver Resection for Hepatocellular Carcinoma?

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