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Surgical EndoscopyAnd Other Interventional TechniquesOfficial Journal of the Society ofAmerican Gastrointestinal andEndoscopic Surgeons (SAGES) andEuropean Association for EndoscopicSurgery (EAES) ISSN 0930-2794Volume 27Number 6 Surg Endosc (2013) 27:1881-1886DOI 10.1007/s00464-012-2687-4
Totally laparoscopic liver resections forprimary and metastatic cancer in theelderly: safety, feasibility and short-termoutcomes
Marcello Giuseppe Spampinato,Marianna Arvanitakis, Francesco Puleo,Lucio Mandala, Giuseppe Quarta,Donatella Traisci, et al.
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Totally laparoscopic liver resections for primary and metastaticcancer in the elderly: safety, feasibility and short-term outcomes
Marcello Giuseppe Spampinato • Marianna Arvanitakis • Francesco Puleo •
Lucio Mandala • Giuseppe Quarta • Donatella Traisci • Antonella Plaia •
Nicola Di Bartolomeo • Gianandrea Baldazzi • Umberto Cillo
Received: 23 July 2012 / Accepted: 20 October 2012 / Published online: 18 December 2012
� Springer Science+Business Media New York 2012
Abstract
Background Standard oncologic liver resections per-
formed on elderly patients (C70 years old) have been
shown to be safe and effective. The aim of this study was to
analyze operative and oncologic short-term outcomes of
totally laparoscopic liver resections (TLLR) performed on
elderly patients for malignancies.
Methods We performed a retrospective statistical analysis
of prospectively recorded data of TLLR performed from
October 2008 to February 2012 by a single hepato-pan-
creato-biliary (HPB) surgeon. Patients were divided into
two groups according to age (\70 vs. C70 years old) and
perioperative outcomes were compared.
Result A total of 60 TLLR for malignancies were identified
of which 25 patients (42 %) were aged C70 years (Group A)
and 35 (58 %) were aged\70 years (Group B). There was no
difference in operative time (170 vs. 180 min, p = 0.267),
median blood loss (200 vs. 250 ml, p = 0.183), number and
time of Pringle maneuver (p = 0.563 and p = 0.180), blood
transfusion rate (4 vs. 17 %, p = 0.222), conversion rate (4
vs. 9 %, p = 0.443), morbidity rate (12 vs. 20 %,
p = 0.797), and perioperative mortality rate (0 vs. 3 %,
p = 0.688). An R0 resection was achieved in 92 (Group A)
versus 83 % (Group B) (p = 0.265). At a median follow-up
of 18 months, 12 % of patients in Group A experienced a
disease recurrence with a related mortality rate similar to that
of Group B (8 vs. 12 %, p = 0.375).
Conclusion This retrospective comparative study shows
that TLLR performed on elderly for liver neoplasm are
feasible and safe and lead to short-term outcomes similar to
those of younger patients.
Keywords Laparoscopic liver resection �Elderly patients �Liver neoplasm � Hepatectomy � Hepatocellular carcinoma
and liver metastases
In the past few decades, mean life expectancy has steadily
increased resulting in an aging population [1]. As a conse-
quence, the number of elderly patients requiring treatment
for primary and metastatic liver neoplasm is constantly rising
and, despite a limited life expectancy, the use of liver surgery
Presented at the 20th EAES Congress, June 20–23, 2012, Brussels,
Belgium.
M. G. Spampinato (&) � N. D. Bartolomeo � G. Baldazzi �U. Cillo
HPB and Advanced Laparoscopic Surgical Unit, Department of
General and Minimally Invasive Surgery, Policlinic of Abano
Terme, Piazza C. Colombo 1, 35031 Abano Terme, PD, Italy
e-mail: marcello.spampinato@gmail.com
M. Arvanitakis � F. Puleo
Department of Gastroenterology, Erasmus University Hospital,
Brussels, Belgium
L. Mandala
HPB Unit, La Maddalena Cancer Center, Palermo, Italy
G. Quarta
Unit of Medical Oncology, Gallipoli General Hospital, Gallipoli,
Italy
D. Traisci
Unit of Medical Oncology, Policlinic of Abano Terme,
Abano Terme, Italy
A. Plaia
Department of Statistical and Mathematical Sciences,
University of Palermo, Palermo, Italy
U. Cillo
Hepatobiliary and Liver Transplantation Unit,
University of Padua, Padua, Italy
123
Surg Endosc (2013) 27:1881–1886
DOI 10.1007/s00464-012-2687-4
and Other Interventional Techniques
Author's personal copy
has been found by many authors to be a safe and effective
treatment for these patients [2–8]. Meanwhile, the laparo-
scopic approach to liver resection for oncologic purpose, for
either primary or secondary liver neoplasm, has been used
increasingly with outcomes comparable to those of standard
hepatectomies [9, 10]. Moreover, recent studies have shown
the benefits of laparoscopic liver resection in terms of
reduced use of blood transfusions, shorter hospital stay,
fewer readmissions, and rapid return to oncologic medical
treatment [11, 12]. To the best of our knowledge, there are no
specific data in the literature about the use of a totally lapa-
roscopic approach to liver resections for oncologic purposes
in the elderly.
The aim of this study was to analyze perioperative and
oncologic short-term outcomes of totally laparoscopic liver
resections (TLLR) performed for malignancies in the
elderly.
Patients and methods
This was a retrospective comparative study that analyzed
prospectively recorded data of consecutive elective TLLR
for primary and metastatic liver neoplasms performed by a
single hepatobiliary surgeon (MGS) with advanced lapa-
roscopic skills between October 2008 and February 2012.
A cutoff point of 70 years was chosen to define elderly
patients for comparison with younger patients. Exclusion
criteria for TLLR were congestive heart failure, high-risk
coronary artery disease, and chronic obstructive pulmonary
disease that significantly limited moderate exertion as
indicated by a full preoperative workup. With respect to the
tumor, patients with large ([5 cm) lesions for which it was
considered difficult to obtain an R0 liver resection due to
the central location and intimate contact with major hepatic
veins or that required a locoregional lymph node dissection
were excluded. Previous abdominal surgery was not con-
sidered a contraindication for a laparoscopic approach.
The extent of hepatic resection was recorded according to
the Brisbane 2000 terminology of liver anatomy and resec-
tions [13]. A major hepatic resection was defined as the
removal of three or more liver segments, while the term
complex was used to define the removal of the right
superoposterior segments of the liver (segments VII and
VIII). Perioperative mortality was defined as death during
the same hospital admission or within 90 days of hepatic
resection. Postoperative complications were classified as per
Dindo–Clavien [14] classification. Margin status was
defined as R0 for microscopically negative for tumor or R1
for microscopically positive for tumor. Data collected
included patient demographics, liver parenchyma and tumor
characteristics, operative factors, postoperative morbidity
and mortality, length of stay, and short-term survival.
Surgical technique
The operation was performed with the patient in a lithotomy
position and with four to five operative ports. In the event of
a complex hepatectomy, a semisupine position was used to
facilitate access to the right posterior segments. Liver
resectability was always confirmed by an intraoperative
staging ultrasound. A 90-cm cotton sling and an 8-cm silicon
intracorporeal tourniquet were always placed around the
hepatoduodenal ligament and brought extracorporeal
through the paraumbilical port to be used if an intermittent
Pringle maneuver (IPM) was required. In the event of a right/
left hemihepatectomy, an extrahepatic intra-Glissonian
approach was used to control hepatic inflow with division of
the arterial and portal branches with the aid of Hem-o-lock
clips (Weck Closure Systems, Research Triangle Park, NC,
USA), while an attempt to control the outflow extraparen-
chymal was never done. A combination of a cavitation-
aspiration system, harmonic scalpel, and bipolar forceps was
used to divide the parenchyma; vascular staplers were used
to divide the hepatic veins as well as the bile duct within the
Glissonian pedicles intraparenchymally. The specimen was
retrieved in an Endobag through a Pfannenstiel incision.
Statistical analysis
Descriptive statistics were expressed as median and range for
continuous variables. Differences between groups were cal-
culated by using the Mann–Whitney test for continuous
variables. Pearson’s v2 test or Fisher’s exact test, if appro-
priate, was used for categorical variables. All p values
\0.05 were deemed significant. Statistical analyses were
performed with SPSS software ver. 20.0 (SPSS Inc., Chicago,
IL, USA).
Results
From October 2008 to February 2012, a total of 70 TLLR were
performed at our institution, of which 60 (86 %) were for
malignancies with curative intent. Among the latter, 25
patients (42 %) were C70 years old (Group A) and 35 (58 %)
were\70 years old (Group B). The two groups were compared
with respect to baseline characteristics, intraoperative factors,
and short-term outcomes, including postoperative complica-
tions, perioperative mortality, length of stay, and recurrence.
Patients and neoplasm characteristics
The two groups were similarly matched for clinical and
oncologic characteristics (Table 1). ASA scores was
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significantly higher in Group A (p = 0.039), while there
was no difference in preoperative liver function between
the groups (p = 0.139). Cirrhotic patients were equally
distributed (Group A, 36 %; Group B, 20 %) and all of
them were in Child-Pugh class A with a MELD score\12.
Type, number, and size of liver tumors were similar
(p = 0.347, p = 0.076, and p = 0.307, respectively;
Table 1). In patients with metastatic disease, the use of
neoadjuvant prehepatectomy chemotherapy was similar in
the two groups (52 vs. 60 %, p = 0.362). The most com-
monly used chemotherapy regimen was oxaliplatin and
5-fluorouracil-based regimens (FOLFOX) ± bevacizumab.
Operative outcomes
Operative details were comparable in both groups
(Table 2). Types of resection were not statistically signif-
icant (p = 0.154), with a similar percentage of major-
complex resections in Groups A and B (28 vs. 37 %). A
synchronous laparoscopic colorectal resection was per-
formed in 12 % (Group A) and 26 % (Group B), respec-
tively. Median operative time was similar for both groups
(170 vs. 180 min, p = 0.267). Median blood loss was
200 ml I Group A and 250 ml in Group B (p = 0.183).
There was no difference in the use and the time of IPM
between groups A and B (p = 0.563 and p = 0.180), and
the conversion rate was not statistically significant for
either group as well (4 vs. 9 %, p = 0.443).
Perioperative outcomes
The short-term outcomes are given in Table 3. The trans-
fusion rate was similar between the two groups (4 vs. 17 %,
p = 0.222). There was no difference in terms of median time
to first flatus, first liquid diet, and intensive care unit (ICU)
stay (p = 0.887, p = 0.582, and p = 0.065). Although the
median total hospital stays were similar (5 vs. 6 days), a
statistically significant difference was found for that
parameter between the two groups (p = 0.041). This result
was due to one patient in Group A who had a prolonged ICU
and hospital stay because of a Dindo–Clavien type IV
complication requiring a reoperation, as shown in Fig. 1.
There was no difference in terms of perioperative mor-
tality (0 vs. 3 %, p = 0.688) and overall morbidity rate (12
vs. 20 %, p = 0.797), although the nonelderly group expe-
rienced a significant higher rate of type II complications
according to the Dindo–Clavien scale (17 vs. 0 % of elderly
group, p = 0.046); the higher rate of synchronous resections
in Group B may have affected the complication rate.
Oncologic short-term outcomes
Final histopathology data are given in Table 4. The pre-
operative neoplasm type was confirmed in 100 % of the
cases (data not shown). There was no difference in terms of
number of lesions, size, grade, and vascular invasion
(p = 0.076, p = 0.307, p = 0.862, p = 0.693), although
the elderly group had a higher percentage of poorly dif-
ferentiated neoplasm compared to the younger group (64
vs. 14 %). The two groups were comparable with respect to
achieving an R0 resection (92 vs. 83 %, p = 0.265) and the
median distance of the tumor from the resection margin (10
vs. 10.5 mm, p = 0.434).
Table 1 Patients and preoperative oncologic characteristics
Variable Group A
(C70 years)
(n = 25)
Group B
(\70 years)
(n = 35)
p value
Age (years) [median
(range)]
73 (70–83) 62 (33–69) \0.001
Sex [M:F (%)] 16:9 (64, 36) 22:13 (62.9, 37.1) 0.573
BMI [median (range)] 24.8 (20–28) 25 (21–30) 0.471
ASA [n (%)] 0.039
1 0 (0) 6 (17)
2 18 (72) 25 (71)
3 7 (28) 4 (11)
Liver function [n (%)] 0.139
Normal 16 (64) 28 (80)
Cirrhosis 9 (36) 7 (20)
Child-Pugh class (%) A (100) A (100)
MELD score (%) \12 (100) \12 (100)
Type of neoplasm
[n (%)]
0.347
HCC 9 (36) 7 (20)
CRLM 14 (56) 23 (66)
Others 2 (8) 5 (14)
No. of lesions [median
(range)]
1 (1–5) 1 (1–6) 0.076
Size of largest lesions
(mm) [median
(range)]
30 (10–83) 25 (10–80) 0.307
Preop. Chtx [n (%)] 0.362
Yes 13 (52) 21 (60)
No 12 (48) 14 (40)
Abdominal surgery
[n (%)]
0.347
Yes 15 (60) 18 (51)
No 10 (40) 17 (49)
BMI body mass index, ASA American Society of Anesthesiologists
grade, HCC hepatocellular carcinoma, CLRM colorectal liver metas-
tasis, Preop. ChTx preoperative chemotherapy
Surg Endosc (2013) 27:1881–1886 1883
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Short-term oncologic outcomes are given in Table 5.
The median follow-up was 18 (range = 3–32) months for
Group A and 23 (range = 3–39) months for Group B
(p = 0.239). In this period, 12 % of the elderly patients
and 26 % of nonelderly patients experienced a disease
recurrence (p = 0.163). There was no difference in terms
of disease-related mortality rate between the two groups (8
vs. 12 %, p = 0.375).
Discussion
The ever-growing aging population will lead to an increased
number of elderly patients with primary or metastatic liver
neoplasm suitable for surgical treatment. Open hepatic
resection for hepatocellular carcinoma and colorectal liver
metastases has been shown to be as safe in the elderly as in
younger patients [7, 15, 16]. Our study sought to determine
the impact of the totally laparoscopic approach on short-term
perioperative outcomes in elderly patients who undergo a
liver resection for malignancies, thus justifying the inclusion
of heterogeneous types of neoplasm in the study. In our
population, despite an expected significant difference in
ASA class between elderly and younger patients, the mor-
bidity and mortality rates were not found to be statistically
significant. This finding contradicts that of Adam et al. [7]
and could be explained by the absence of a major abdominal
incision and the consequences related to it.
The majority of complications in our study were minor
(grade II or less) and these were statistically higher in
younger patients; this finding could be explained by double
the rate of synchronous resection performed in the younger
group requiring a longer operative time. In the elderly
group there was one patient who experienced postoperative
anastomotic failure following a synchronous liver and
colon resection that required a reoperation and subse-
quently had a prolonged ICU and hospital stay. This event
negatively affected the total length of hospital stay in the
elderly group and led to a significant difference compared
to the younger group, albeit the median length of hospital
stay was only 5 days with a fast recovery and a rapid return
to adjuvant chemotherapy when needed. Besides, both
groups were found to have a low percentage of blood loss
and perioperative blood transfusion, in agreement with
other studies and supporting the efficiency of the laparo-
scopic liver resection [11, 12].
Perhaps one of the most dreaded complications of major
liver resection is postoperative liver failure. Despite con-
cerns over decreased hepatic function in the elderly [17]
and a higher risk of morbidity related to major hepatectomy
Table 2 Operative procedure
Variable Group A
(C70 years)
(n = 25)
Group B
(\70 years)
(n = 35)
p value
Type of resection [n (%)] 0.154
Minor 19 (76) 21 (60)
Major (C3 segments) 5 (20) 13 (37)
RH 5 (100) 6 (50)
LH 0 (0) 6 (50)
Other 0 (0) 1 (3)
Complex (RPS) 2(8%) 1(3%)
Associated procedure
[n (%)]
Synchronous colectomy 3(12) 9 (26)
Liver MW ablation 2(8) 4 (11)
Operative time (min)
[median (range)]
170 (60–500) 180 (40–600) 0.267
EBL (ml) [median
(range)]
200 (40–600) 250 (40–1,200) 0.183
IPM [n (%)] 0.563
No 19 (76) 26 (74)
Yes 6 (24) 9 (26)
Time (min) [median
(range)]
10 (10–40) 20 (10–40) 0.180
Conversion [n (%)] 0.443
No 24 (96) 32 (91)
Yes 1 (4) 3 (9)
RH right hemihepatectomy, LH left hemihepatectomy, RPS right
posterior sectionectomy, MW microwave, EBL estimated blood loss,
IPM intermittent Pringle maneuver
Table 3 Perioperative outcomes
Variable Group A
(C70 years)
(n = 25)
Group B
(\70 years)
(n = 35)
p value
Transfusion [n (%)] 0.222
No 24 (96) 29 (83)
Yes 1 (4) 6 (17)
Postoperative recovery (day)
[median (range)]
First flatus 1 (1–3) 1 (0–3) 0.887
First liquid diet 1 (0–2) 1 (0–2) 0.582
ICU stay 0 (0–1) 1 (0–4) 0.065
LOS 5 (3–42) 6 (3–10) 0.041
Complications type [n (%)] 0.797
I 2 (8) 0 (0)
II 0 (0) 6 (17) 0.046
III–V 1 (4) 1 (3)
Mortality [n (%)] 0.688
No 25 (100) 34 (97)
Yes 0 (0) 1 (3)
ICU intensive care unit, LOS length of hospital stay
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[18], in our study 20 % of the elderly patients underwent a
formal right hemihepatectomy for colorectal metastases
and none of them experienced this complication. In addi-
tion, none of the cirrhotic subgroups experienced worsen-
ing of their preoperative liver function status. This result
may be explained by a strong selection bias with cirrhotic
patients who undergo surgery and the absence of a detri-
mental large surgical incision in the abdominal wall,
allowing preservation of important collaterals of the portal
vein system. With regard to the oncologic results, we did
not attempt to calculate the disease-free survival and
overall survival curves due to the low number of deaths,
short median follow-up, and the presence of a heteroge-
neous type of neoplasm with different biological behavior
in both groups. Despite this limitation, in our series the
laparoscopic approach to liver resections in the elderly was
shown to be oncologically efficient in terms of percentage
of R0 resection achieved and a short-term overall survival
in agreement with that in the current literature [9, 19].
Others limitations of this study are its retrospective
nature and the potential for selection bias and confounding
variables. Furthermore, this study represents the experience
of a single specialized hepatobiliary surgeon, highly trained
in both open liver surgery and advanced laparoscopic
procedures.
Conclusions
With the caveat of being a retrospective study analyzing a
small sample of patients, this work showed that TLLR for
treatment of elderly patients with primary hepatocellular
carcinoma or secondary metastases requiring a liver
resection is feasible and safe and leads to short-term out-
comes similar to those of younger patients. In the event of a
major hepatectomy, the laparoscopic approach should not
be denied to elderly patients who are without severe
comorbidities and have normal preoperative liver function,
provided that the operation is performed by a highly spe-
cialized hepatobiliary surgeon with skills in advanced
laparoscopic techniques. These results need to be validated
by larger prospective and randomized studies.
Acknowledgments We thank Prof. G. Mudo’ from the Department
Experimental Medicine and Clinical Neurosciences, Division of
Human Physiology, University of Palermo (Italy) for her kindly
assistance in the editing of the manuscript. Dr. Francesco Puleo is
currently granted by Fonds Erasme, Brussels, Belgium.
Disclosures Marcello G. Spampinato, Marianna Arvanitakis, Lucio
Mandala’, Giuseppe Quarta, Donatella Traisci, Antonella Plaia,
Fig. 1 Distribution of total hospital stays in the two groups of
patients; boxplot reports the medians (bold lines) and interquartile
ranges (boxes), together with possible outliers (circle)
Table 4 Histopathology data
Variable Group A
(C70 years)
(n = 25)
Group B
(\70 years)
(n = 35)
p value
No. lesions [median (range)] 1 (1–5) 1 (1–9) 0.076
Size largest lesion (mm)
[median (range)]
30 (10–80) 20 (10–80) 0.307
Grade [n (%)] 0.862
G1 5 (20) 7 (20)
G2 4 (16) 23 (66)
G3 16 (64) 5 (14)
Margin status [n (%)] 0.265
Positive 2 (8) 6 (17)
Negative 23 (92) 29 (83)
Margin distance (mm)
[median (range)]
10 (1–25) 10.5 (2–20) 0.434
Vascular invasion [n (%)] 0.693
Yes 6 (24) 8 (23)
No 19 (76) 27 (77)
Table 5 Oncologic outcomes
Variable Group A
(C70 years)
(n = 25)
Group B
(\70 years)
(n = 35)
p value
Follow-up (months)
[median (range)]
18 (3–32) 23 (3–39) 0.239
Recurrence [n (%)] 3 (12) 9 (26) 0.163
Death [n (%)] 2/25 (8) 5/35 (14) 0.375
Recurrence location 0.764
Liver [n (%)] 2 (67) 6 (67)
Systemic [n (%)] 1 (33) 3 (33)
Surg Endosc (2013) 27:1881–1886 1885
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Nicola Di Bartolomeo, Gianandrea Baldazzi, and Umberto Cillo have
no conflicts of interest or financial ties to disclose.
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