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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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