Surgical Science, 2013, 4, 393-400 Published Online September 2013 (
Surgical Treatment of Liver Metastases
from Gastric Cancer
Daniel Vasilev Kostov1, Georgi Leonidov Kobakov2, Daniel Veselov Yankov1
1Department of Surgery, Naval Hospital of Varna, Varna, Bulgaria
2Clinic of Surgery, Specialized Hospital for Oncologic Diseases of Varna, Varna, Bulgaria
Received June 28, 2013; revised July 30, 2013; accepted August 7, 2013
Copyright © 2013 Daniel Vasilev Kostov et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background: Hepatectomy for gastric metastases remains controversial. We aimed at assessing the surgical results,
clinicopathological features of gastric cancer liver metastases (GCLM) and prognostic factors. Methods: The outcome
of 28 consecutive patients with synchronous (n = 24) or metachronous (n = 4) GCLM was retrospectively analyzed.
Curatively, initial hepatectomies such as segmentectomy and hemihepatectomy or non-anatomical limited liver resec-
tion less extensive than segmentectomy followed complete primary gastric cancer (GC) resections. Results: Median
survival time was 16 months (range, 5 - 66 months). The actuarial overall 12-, 36-, and 60-month survival rates after
hepatectomy were 67.8% (n = 19), 39.2% (n = 11), and 28.5% (n = 8), respectively. In multivariate analysis, absent GC
serosal invasion-hazard ratio (HR) 1; 95% confidence interval (CI) 1.2 - 9.9; P = 0.020; solitary LM-HR 1; 95% CI 1.6
- 16.0; P = 0.005, and curative liver resection with negative resection margin (R0)-HR 1, 95% CI 2.2 - 18.0; P = 0.001
were independent prognostic factors. Conclusions: Surgery of GCLM is a good indication in well-selected patients
with an absent serosal invasion of primary tumour, single GCLM and attainment of R0 liver resection. For most GCLM
patients, however, there are no other therapeutic modalities. Thus systemic chemotherapy remains the best hope for a
longer patient’s survival and an improved individual quality of life.
Keywords: Gastric Cancer; Liver Metastases; Hepatectomy; Survival; Prognostic Factors; Univariate Analysis;
Multivariate Analysis
1. Introduction
Liver is a common site of metastases of GC. However,
their treatment has not been well-defined yet. Gastric
adenocarcinoma is the fourth most common cancer
worldwide and accounts for 1.5% of all new diagnoses
and 5.2% of all cancer deaths [1,2]. Early tumour detec-
tion, standardized surgical treatment including lymph
node dissection and appropriate adjuvant therapy im-
prove the survival of primary GC patients. At the time of
diagnosis, 35% of the cases present with evidence of
distant metastases and 4% - 14% do with metastatic liver
disease [3,4]. Patients with isolated metastases are un-
usual and account for 0.5% of the cases in a comprehen-
sive series [5]. The benefits of surgical approach to me-
tastatic GC remain debatable and have been rarely stud-
ied [6]. GCLM convey a very poor prognosis. Most me-
tastases will be diffused, and chemotherapy is then the
optimal treatment modality. Therefore, proper determi-
nation of selection criteria for hepatic resection and pre-
conditions for long-term survival after hepatectomy is
crucial. Several authors report limited experiences of sur-
gical resection of GCLM in selected patients, with five-
year survival rates of 0% - 38% [7,8]. Complete removal
of the primary GC and the LM appears to be the only
option for possibly curing the disease, although the bene-
fits of metastasectomy are poorly defined.
Accordingly, we herewith review retrospectively 28
patients who have undergone liver resection for GCLM
in order to clarify the surgical outcome and clinico-
pathological features of favourable prognosis in such
2. Methods
Between 1992 and 2006, 756 GC patients were surgically
treated in the Department of Surgery, Naval Hospital of
Varna, Bulgaria. Of these, 88 patients (11.6%) presented
with synchronous LM and 52 ones (6.8%) developed
metachronous LM after resection of the primary GC.
opyright © 2013 SciRes. SS
Synchronous LM was defined by detection before and
during surgery or within 3 months of primary tumour
resection. GCLM were diagnosed through endoscopy and
biopsy, echography, computer axial tomography (CAT)
and intraoperative echography. The following criteria
were actually accepted for GCLM resection: 1) good
control and complete resection of the primary tumour
and lymph nodes involvement in synchronous disease; 2)
no signs at preoperative workup of disseminated diseases,
hilar lymph nodes metastases, peritoneal dissemination,
or extrahepatic metastases; 3) complete LM resection (no
residual tumour at macroscopical examination) [9]. Ac-
cording to these criteria, twenty-eight out of a total of
140 patients having undergone initial hepatectomy were
selected for this study.
Disease free was defined and determined in accor-
dance with clinical, laboratory, endoscopic and imaging
diagnostic methods as following-up ranged from 12 to
122 months (median of 26 months). Postoperatively, all
the patients were followed-up every six months clinically,
biochemically, echographically, endoscopically and by
means of CAT or positron emission tomography (PET) if
needed up to the end of the 60th postoperative month.
Follow-up ranged from 12 to 122 months (median of 26
months). The following preoperative demographic and
clinical information was obtained from the patient re-
cords: age, gender, histological differentiation, serosal
invasion, extent of lymph node metastases, lymphatic
and venous invasion of the primary GC, size and number
of LM, lobar distribution, vascular invasion within LM,
time of LM appearance (synchronous or metachronous),
fibrous pseudocapsule between LM and liver paren-
chyma, peritumoural lymphocytes surrounding LM, CEA
level before hepatectomy, type of hepatic resection, sur-
gical margin and completeness of the resection. In each
patient, intraoperative liver ultrasound was performed to
assess the extent and number of hepatic lesions and their
relationships to intrahepatic vascular and biliary struc-
tures. Surgical procedures were classified either as ana-
tomical liver resection (segmentectomy and hemihea-
tectomy), or as non-anatomical limited liver resection
(for all the resections less extensive than segmentectomy).
One-, two- and three-month mortality rates were ana-
The rest 112 patients with GC with concomitant LM
were excluded as candidates for potential R0 because of
the present multiple bilateral metastases. They underwent
systemic or hepatic artery infusion chemotherapy plus
local-regional radiation.
Actuarial overall survival rates since the date of the
liver resection onwards were calculated using the Kap-
lan-Meier method. Differences were compared between
subgroups according to univariate analysis in the result-
ing distributions using the log-rank test. Based on these
results, a multivariate stepwise Cox regression analysis
was performed to identify factors that were independ-
ently associated with prognosis. Statistical significance
was defined as a P-value below 0.05. Any statistical
analyses were accomplished using SPSS 9.0 package
(SPSS Inc., Chicago, IL, USA).
3. Results
Of these 28 patients, there were 19 males and 9 females
at a mean age of 68 years (range, 51 - 81 years). Curative
resection of the GC with lymph node dissection up to the
second echelon (D2) was performed in all the cases. Se-
rosal invasion was absent in 10 (35.7%) and present in 18
(64.3%) patients. Lymph node grouping was based on
Japanese classification on cancer typing. GC with lymph
node involvement was established in 21 (75%) patients.
A well-to poorly differentiated adenocarcinoma in the
primary gastric location was pathologically proven in all
the patients. The number of metastatic nodules was one
in 19 (67.8%) patients, two in three (10.7%) ones, three
in three (10.7%) ones, and four to seven in three (10.7%)
ones. GCLM median size was 37 mm (range, 6 - 105
mm). With regard to pathological features in GCLM
peritumoural lesion, fibrous pseudocapsule between the
tumour and hepatic parenchyma was seen in 16 (57.1%)
patients where lymphocytic infiltration was graded as
weak in 21 (75%) patients. Synchronous hepatic resec-
tion and gastrectomy was performed in 24 (85.7%) pa-
tients. The mean interval between gastric and hepatic
resection in the remaining 4 (14.2%) patients with meta-
chronous metastases was 19 months (range, 6 - 22
months). Anatomical resection was carried out in 19
(67.8%; major 11; minor 8) patients and limited non-
anatomical minor resection in 9 (32.1%) ones. In 25
(89.2%) patients the resection was classified as curative
(R0), whereas microscopically positive margins were
identified in three (10.7%) patients. Adjuvant systemic
chemotherapy was administered to all the patients.
No patient died within three months of surgery. The
overall morbidity rate was 25% (seven patients). Com-
plications comprised transient liver failure, bile leakage,
biloma, intaabdominal abscessus, pleural effusion, and
wound infection.
The results of the statistical analysis of prognostic
factors are presented in Table 1. The absent serosal inva-
sion of primary tumour (P = 0.031) and of lymph node
involvement (P = 0.042), the present solitary LM (P =
0.032) and peritumoural brous pseudocapsule (P =
0.021) as well as the R0 liver resection (P = 0.003) were
significant determinants for a favourable prognosis after
hepatic resection at univariate analysis while remaining
factors associated with the primary lesion, LM and sur-
gery were not. Median survival time was 16 months
(range, 5 - 66 months). Five patients remain alive and
Copyright © 2013 SciRes. SS
Copyright © 2013 SciRes. SS
Table 1. Clinicopathological characteristics and prognostic signicance by univariate analysis.
Surviving patients n/(%)
Variable Patients (n)
1 year 3 years 5 years
(P value)
Histological differentiation
Well 11 8 (72.7) 5 (45.4) 3 (27.2) 0.122
Moderately, poor 17 11 (64.7) 6 (35.2) 5 (29.4)
Absent serosal invasion 10 8 (80) 8 (80) 6 (60) 0.031
Present serosal invasion 18 11 (61.4) 3 (16.6) 2 (11.1)
Lymph node involvement
N0-N1 16 12 (75) 7 (43.7) 6 (37.5) 0.042
N2 12 7 (58.3) 3 (25) 2 (16.6)
Absent lymphatic and venous invasion of 13 9 (69.2) 5 (38.4) 4 (30.7)
primary GC 0.303
Present lymphatic and venous invasion of 15 10 (66.6) 6 (40) 4 (26.6)
primary GC
LM number
Tumour size <4 cm
Tumour size 4 cm
Unilobar lobar distribution
Bilobar lobar distribution
Absent vascular invasion
Present vascular invasion
Absent fibrous pseudocapsule
Present fibrous pseudocapsule
Absent peritumoural lymphocytes
Present peritumoural lymphocytes
CEA level before hepatectomy
<5 ng/ml
>5 ng/ml
13 (68.4)
5 (55.4)
7 (77.7)
12 (63.1)
16 (69.5)
3 (60)
12 (66.6)
7 (70)
10 (83.3)
9 (56.2)
5 (71.4)
14 (66.6)
12 (70.5)
7 (63.6)
11 (57.8)
4 (44.4)
7 (36.8)
9 (39.1)
2 (40)
7 (38.8)
4 (40)
2 (16.6)
9 (56.2)
3 (42.8)
8 (38)
7 (41.1)
4 (36.3)
8 (42.1)
2 (22.2)
6 (31.5)
7 (30.4)
1 (20)
5 (27.7)
3 (30)
1 (8.3)
7 (43.7)
2 (28.5)
6 (28.5)
4 (23.5)
3 (27.2)
Synchronous LM appearance
Metachronous LM appearance
Anatomical hepatic resection
Non-anatomical hepatic resection
R0 (curative resection)
R1 (non-curative resection)
16 (66.6)
3 (75)
13 (68.4)
6 (66.6)
19 (76)
9 (37.5)
2 (50)
8 (42.1)
4 (44.4)
11 (44)
7 (29.1)
1 (25)
6 (31.5d)
3 (33.3)
8 (32)
disease-free at >5 years after the hepatic resection. In all
of them, there was neither serosal GC invasion, nor
lymph node involvement. However, they presented with
a solitary LM and a peritumoural brous pseudocapsule
and underwent a R0 liver resection.
GCLM recurred in 23 (82.2%) of the patients between
6 and 31 months after hepatic resection. The recurrence
was located in the liver in 12 patients, the lung in eight,
lymph nodes in two, and brain in one patient. Hepatic
relapse was combined with peritoneal dissemination in
five patients and limited to the remnant liver only in six
ones. No patient underwent a second hepatic resection
for recurrent intrahepatic metastasis. The actuarial over-
all 12-, 36-, and 60-month survival rates after hepatic
resection were 67.8% (n = 19), 39.2% (n = 11), and
28.5% (n = 8), respectively (Figure 1). Rates of 12-, 36-
and 60-month disease-free survival were 53.5% (n = 15),
25% (n = 7), and 17.8% (n = 5), respectively.
Multivariate analysis revealed that absent serosal GC
invasion (HR 1; 95% CI 1.2 - 9.9; P = 0.020), solitary
LM (HR 1; 95% CI 1.6 - 16.0; P = 0.005), and R0 liver
resection (HR 1; 95% CI 2.2 - 18.0; P = 0.001) were in-
dependent prognostic factors (Table 2).
None of 112 GC patients with concomitant LM having
undergone some non-surgical treatment survived longer
than 60 months.
Figure 1. Overall survival and disease-free survival curves
of 28 patients following hepatic resection for GCLM.
Table 2. Significant prognostic factors on multivariate anal-
Variable Hazard
95% Confidence
Interval (P value)
Absent serosal invasion of
primary tumour
1 1.2 - 9.9 0.020
Present serosal invasion
of primary tumour 3.5
LM number
Solitary 1 1.6 - 16.0 0.005
Multiple 5.1
R0 (curative resection) 1 2.2 - 18.0 0.001
R1 (non-curative resection) 7.0
4. Discussion
According to the concept that GCLM are synonymous
with generalized neoplastic disease, they are considered
for a long time as a contraindication to a curative treat-
ment and thus only a palliative chemotherapy was given
with a median survival of approximately 7 months [10].
Even intensive systemic chemotherapy does not achieve
a satisfactory survival benefit. The incidence of syn-
chronous GCLM is about 2.0% - 9.6% that is lower than
that from colorectal cancer [11]. However, the results
from non-surgical treatments such as systemic or hepatic-
artery infusion chemotherapy are not satisfactory yet.
Most GCLM are diffuse and the local-regional radiation
along with the novel chemotherapy regimens such as
FOLFOXIRI (5-uorouracil, leucovorin, oxaliplatin and
irinotecan) are encouraging [12]. Trials using this regi-
men achieve for the rst time a median overall survival
of 15 months. The benefit of metastasectomy in GC has
not been well-defined yet, and it is not considered as a
standard treatment. This is because LMs are, usually,
multiple lesions scattered to both hepatic lobes and ac-
companied by widespread peritoneal dissemination, too.
The lymphatic dissemination results from the phe-
nomenon of lymphatico-venous communication and
lymph flow reflux by lymphatic obstruction. This path-
way is at the origin of hepatic and peritoneal metastasis
[13]. The multiplicity of these broad mechanisms ex-
plains that at time of diagnosis, GCLM are rarely isolated
and, most often, associated with other visceral sites.
However, little is known about the factors influencing on
the prognosis after GCLM resection because of the small
number of cases. A consensus has not been reached yet,
and there is a definite need for further research.
GCLM resectability rate is low and only 10% to 20%
of patients undergo resection of the primary cancer and
of LM as well [8,14-17]. Indeed, there were 247 cases of
LM among 5520 cases of gastrectomy for gastric adeno-
carcinoma. Among them, only 42 liver resections were
performed which corresponded to a resectability rate of
17% [15].
In the present study, 20% of GCLM patients have been
considered suitable for liver resection according to the
inclusion criteria of ours. We prove that the absent se-
rosal GC invasion, the solitary LM and attainment of R0
liver resection are independent favourable prognostic
factors in both univariate and multivariate analyses. The
serosal invasion of primary GC is the rst step in the
advancement to peritoneal dissemination and thus con-
sidered as a signicant poor prognostic factor after
GCLM resection [18]. Peritoneal lavage cytology may be
of use when considering liver resection [19]. In our series,
serosal invasion is absent in six of eight five-year survi-
vors. Hepatectomy should be attempted in absent serosal
or microscopic lymphovascular invasive primary GC
Copyright © 2013 SciRes. SS
involvement [18,20]. There is an insignificant difference
in terms of serosal invasion or lymph node GCLM be-
tween surviving and non-surviving patients [14,21,22]. A
marginal significance of primary tumour serosal invasion
is proved [15]. Nobody of our patients presenting with
multiple GCLM has survived longer than three years,
whereas 42.1% of those with a solitary GCLM have done
at least five years.
We also demonstrate a limited effect of surgical resec-
tion in the patients with multiple GCLM. Survival rates
of 56% for single GCLM but no ones for multiple ones
after hepatectomy have been reported [14]. The impor-
tance of GCLM number as a prognostic factor is sug-
gested elsewhere, too [17,23,24].
A single GCLM and absent peritoneal dissemination
are significantly independent prognostic factors for such
patients with synchronous GCLM [11]. The attainment
of R0 liver resection is the third independent prognostic
factor to consider for the indications of hepatic resection
of GCLM. There is a significant survival difference ac-
cording to the tumour-free hepatic resection margin [22].
Long-term survivors with more than three GCLM have
been reported [25] enabling the conclusion that if R0 can
be achieved, hepatic resection should not be abandoned
even in patients with multiple GCLM. A positive resec-
tion margin should be considered a powerful determinant
of poor outcome [7].
The results concerning the surgical margin of GCLM
are conflicting as some authors accept that anatomical
hepatic resection with a surgical margin of at least 10
mm is an important factor influencing survival [7,22,26],
while other investigators report that both the resection
margin and the type of liver surgery do not affect sur-
vival rates [14,16,24]. No relationship between the extent
of hepatic resection and prognosis has been established
yet [5,27]. Micrometastases around the macroscopic tu-
mour are more frequent in GCLM than in LM from co-
lorectal cancer thus suggesting the need for wider surgi-
cal resection margins. Approximately two thirds to three
quarters of patients develop liver recurrence [15,16].
Such a high recurrence rate within two years after hepatic
resection suggests the presence of intrahepatic microme-
tastases around LM at the time of surgery [27]. These
poor results motivate the search for the best candidates
for liver resection.
A generous surgical margin may not be essential for
R0 of LM, although positive surgical margins should be
avoided. Recurrent tumours are more frequently distri-
buted in both lobes than in the resected lobe suggesting
that liver recurrence is more probably derived from mul-
tiple metastatic foci from the primary disease than from
intrahepatic remetastases of the liver lesion. There is no
apparent value of surgery if residual disease remains,
whether it is involvement of resection margins, other
distant LM, or peritoneal carcinosis [28].
The time of GCLM resection represents another con-
troversial issue. Synchronous disease is a known prog-
nostic factor representative of aggressive biology. Some
authors report poor results in terms of survival after sur-
gery for synchronous metastases [14,26,29]. The syn-
chronous character of GCLM is considered the only in-
dependent factor of poor prognosis [25]. Recently, a five-
year survival rate of 60% after surgical resection of syn-
chronous GCLM is reported [30]. The extent of hepatic
involvement and macroscopic peritoneal dissemination
detected at surgical exploration represent the factors in-
fluencing upon survival in patients with synchronous
GCLM [30]. According to other authors, the size of me-
tastases smaller than 5 cm relates to better survival [8,
In the present study, a fibrous pseudocapsule around
GCLM and the status of lymph node involvement are
closely associated with patient’s survival at univariate
analysis only. In 16 patients, there is a thick brous
pseudocapsule with more than 8 layers of collagen bun-
dles between the tumour and hepatic parenchyma. Pseu-
docapsule formation should be considered as a protective
immunoinflammatory reaction against the metastastic
nodule reflecting the host defence reaction that creates a
wall to stop tumour diffusion [14]. The presence of a
brous pseudocapsule may be a valuable prognostic fac-
tor reecting the aforementioned reaction in GCLM pa-
tients [29]. Faithful lymph node dissection up to the
second echelon contributes to a better chance of cure for
the patients with lymph node metastases and GCLM.
There is an insignificant difference concerning the depth
of invasion or lymph node GCLM between the surviving
and non-surviving patients [14,22]. D2 or greater exten-
ded lymphadenectomy is conventionally performed for
advanced GC with good outcomes and relatively low-
frequent lymph node recurrences [32,33]. Patients with
positive paraaortic GCLM present with poor survival
rates following liver resection [15]. Long-term survival
in patients with both paraaortic lymph nodes and LM is a
seldom finding [32]. Therefore, we consider that liver
resection for GCLM is not indicated in patients with
paraaortic lymph node metastasis.
Our study fails to establish any signicant association
between survival and the rest prognostic factors related
to primary GC, LM and surgery in the patients who have
undergone hepatectomy for GCLM. Literature data about
the clinicopathological features in GCLM patients are
contradictory and difficult to interpret. Tumour localiza-
tion in primary GC is a marginally predictive negative
factor for the overall patients’ survival [34]. GC tumour
size larger than 6 cm is associated with a poor prognosis
after GCLM resection [11,23]. A disease-free interval
between gastric and hepatic resection of >1 year is a
Copyright © 2013 SciRes. SS
signicant survival advantage as a result of the slow-
growing nature of this tumour [29]. The aggregation of
lymphocytes enclosing the metastatic tumour is a factor
of good prognosis [29]. The unilobular liver nodule dis-
tribution is a good predictor as most unilobular tumours
are solitary [26]. Unilobar LM distribution is also associ-
ated with a better survival after resection, especially, if
their size is less than 4 cm [16]. Primary tumour differ-
entiation grade is a negative predictor of outcome [6].
Bilobar tumours result in a worse patient’s outcome than
unilobar ones [34]. According to other authors, however,
these prognostic factors are not signifycant and there are
some controversies in this respect [14,15,22]. No primary
tumour-related or LM-related factor of prognostic value
has been identified [35,36]. Concerning the extrahepatic
disease associated to GCLM, this situation constitutes a
poor prognosis with significantly lower median survival
compared to cases in which resection of isolated GCLM
is performed (7 vs. 23 months, respectively) [7,37].
The comparison of the results from different studies
demonstrates that one-year survival rates range from
36% to 90%, three-year ones-from 22% to 57%, and
five-year ones from 0% to 43% [15,34,37]. The median
survival rate ranges from 8 to 25 months [12,14,18,29].
In individual studies, the overall one-, three-, and five-
year survival rates after hepatic resection are 80%, 60%,
and 60%, respectively, with median survival time rang-
ing from 31 to 34 months [15,16]. In our study, the me-
dian survival time is 16 months and the actuarial overall
one-, three-, and five-year survival rates after hepatic
resection are 67.8%, 39.2%, and 28.5%, respectively.
These parameters seem acceptable as they have been
achieved by means of a strict selection of the patients
suitable for hepatectomy.
Radio-frequency ablation is another important strategy
for GCLM treatment. This technique can be employed
either as alternative of, or in association to hepatectomy.
It could be the approach of choice in case of poor general
conditions contraindicating surgery. Currently, systemic
chemotherapy is considered the standard of care, how-
ever, long-term survival using chemotherapy alone is
rare. Although recent advancements with newer regimens
for this disease lead to modest improvements, long-term
survival beyond five years is seldom [38]. A five-year
survival rate of 75% in a subgroup of eight patients sub-
mitted to radical surgery followed by hepatic-artery infu-
sion chemotherapy has been reported [28]. Recurrent
disease develops, most commonly, in the liver after he-
patic resection in approximately 70% of the patients
[6,15]. Recurrence rates after liver resection in GCLM
could potentially decrease with the addition of these new
regimens such as adjuvant therapies [12]. Recently,
postoperative adjuvant chemotherapy advances in GCLM
as arterial chemotherapy statistically signicantly pre-
vents hepatic recurrence [12,15,39,40]. Liver surgery
rather than hepatic artery infusion could significantly
prolong the survival period for patients with synchronous
GCLM [28]. GCLM management is not consensual. If
systemic chemotherapy is an irrefutable indication for
GCLM associated with other extrahepatic metastases, the
attitude for isolated LM is still widely debated. Although
the level of evidence is low, the results of surgery in this
situation in terms of five-year survival and median sur-
vival are superior to those obtained with systemic che-
motherapy alone. This outcome is even more evident
when surgery is indicated for single LM of less than 5 cm
in size.
5. Conclusion
Nowadays the best treatment option for GCLM is inten-
sively discussed. Surgery is a good indication in properly
selected patients with an absent serosal invasion of pri-
mary tumour, single LM and attainment of R0 liver re-
section. However, this is not the most common condition.
For the remaining majority of GCLM, there is no suffi-
cient scientific evidence to indicate other therapeutic
modalities such as radio-frequency ablation, hepatic-ar-
tery infusion chemotherapy and palliative gastrectomy.
In this case, systemic chemotherapy remains the best
hope for a longer survival and an improved quality of
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