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Journal of Surgical Oncology 2008;98:515–519
Laparoscopy-Assisted Distal Gastrectomy With D2 lymphadenectomy for T2b
Advanced Gastric Cancers: Three Years’ Experience
HOON HUR, MD,1,2 HAE MYUNG JEON, MD, PhD,2 AND WOOK KIM, MD, PhD1*
1Department of Surgery, Holy Family Hospital, College of Medicine, The Catholic University of Korea, Gyeonggi-do, Republic of Korea2Department of Surgery, St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
Background: The application of laparoscopy-assisted distal gastrectomy (LADG) with advanced gastric cancer (AGC) is a controversial. The
purpose of this study was to assess the possibility of using LADG application to AGC.
Methods: Of 160 patients who underwent LADG with D2 lymphadenectomy between April 2004 and March 2007, 26 patients with stage pT2b
were selected and compared to 25 patients of the same stage who underwent open distal gastrectomy (ODG) within same period. The comparison
was based on the clinicopathologic characteristics, surgical outcome, and follow-up results.
Results: There was no significant difference between LADG and ODG groups in most operation results including complication rates (15.4% vs.
16.0%, P¼ 1.000) except for less average loss of blood (160.0 ml vs. 215.0 ml, P¼ 0.012) and longer average operating time (255.0 min vs.
190.0 min, P< 0.001) in LADG. Three-year overall survival rates (88.2% vs. 77.2%; P¼ 0.246) and disease-free survival rates (71.4% vs. 53.4%;
P¼ 0.757) were not significantly different in LADG and ODG groups.
Conclusions: The early results of current study suggest that LADG for AGC is technically safe and oncologically feasible. Therefore, LADG
should be considered as a curative treatment for AGC not exposed to serosa.
J. Surg. Oncol. 2008;98:515–519. � 2008 Wiley-Liss, Inc.
KEY WORDS: gastric cancer; laparoscopic surgery; survival
INTRODUCTION
Since laparoscopy-assisted distal gastrectomy (LADG) for early
gastric cancer (EGC) was first performed in 1991 by Kitano et al. [1],
the use of this procedure has been rapidly increasing in EGC high-
prevalence countries like Korea and Japan. In spite of the potential
benefits of LADG compared to the conventional open procedure, such
as less post-operative pain, faster recovery, and shortened hospital
stays [2,3], here remain some controversies in terms of its oncologic
benefits.
Most notably, LADG application in locally advanced gastric
cancers (AGC) must overcome some problems associated with
incomplete D2 lymph node dissection as the difficult anatomical
approach by laparoscopic view increases the chances of incomplete
removal of nodes and incomplete en bloc dissection. Despite recent
innovative progression in laparoscopic tools and improvement in
surgical experience, most surgeons have hesitated to extend their
indications of laparoscopic surgery into advanced diseases and few
reports have addressed the application of a laparoscopic procedure to
advanced cancer in terms of oncologic benefits or risks. However, our
institution has tried to improve laparoscopic techniques, as we already
reported our results of laparoscopic surgery for upper advanced gastric
cancer [4], and is consequently able to perform LADG with complete
D2 lymph node dissection unless locally AGC is exposed to serosa in
the preoperative imaging or laparoscopic staging. In the present study,
in order to evaluate the technical safety and the oncologic feasibility of
laparoscopic surgery for AGC with the results of our institution’s
operations, we enrolled patients who were pathologically diagnosed
with a tumor that had invaded the subserosa (pT2b) after LADG or
open distal gastrectomy (ODG) with D2 lymphadenectomy, and then
we compared the surgical outcomes and prospective early follow-up
results of these two groups.
The aim of this study is to suggest the possibility of applying LADG
with D2 lymph node dissection to AGC not exposed to serosa.
PATIENTS AND METHODS
Patients
From April 2004 when we firstly performed laparoscopy-assisted
gastrectomy (LAG) for gastric cancer to March 2007, 200 patients
underwent LAG (distal gastrectomy in 160 cases, total gastrectomy in
39 cases, and proximal gastrectomy in one case) performed by one
surgeon (Dr. W. Kim) who had an experience of open conventional
surgery for gastric cancer more than 100 cases per year over 10 years
at the Department of Surgery, Holy Family Hospital, The Catholic
University of Korea, and operative and follow-up data were
prospectively collected. In our institution, the indications for perform-
ing laparoscopic procedure for gastric cancer were: depth of invasion
confined to the subserosal layer (cT2), and either no evidence of lymph
node metastasis or metastasis confined to group 1 nodes (less than cN1)
without distant metastasis. Laparoscopic D2 lymphadenectomy was
performed when the tumor was preoperatively predicted to invade
muscle or metastasize to a lymph node. However, when laparoscopic
observation of serosal invasion was seen, conversion to an open
procedure was carried out and these patients were excluded from the
present study. For the current study, of 160 patients who underwent
LADG, 26 with pathologically confirmed T2b (invasion to the
subserosa) were compared to the 25 patients who also had patho-
logically confirmed T2b and underwent conventional ODG with D2
lymphadenectomy performed by the same surgeon within the given
*Correspondence to: Wook Kim, MD, PhD, Department of Surgery, HolyFamily Hospital, College of Medicine, The Catholic University of Korea.Sosa-dong, Wonmi-gu, Bucheon-si, Gyeonggi-do 420-171, Republic ofKorea. Fax: þ82-32-340-2036. E-mail: kimwook@catholic.ac.kr
Received 10 June 2008; Accepted 18 August 2008
DOI 10.1002/jso.21155
Published online 17 October 2008 in Wiley InterScience(www.interscience.wiley.com).
� 2008 Wiley-Liss, Inc.
time period because of various reasons including patients’ intention,
financial difficulties and so on. These enrollments were considered by
the already known clinical course of pathologic subserosal cancer
(pT2b) comparing with muscle proper cancer (pT2a) or serosa exposed
cancer (pT3) [5–9]. Two groups were compared in terms of their
clinicopathologic characteristics, morbidity and mortality, and were
prospectively followed up for survival analysis. All procedures were
performed after obtaining informed consent following the explanation
of the surgical and oncologic risks.
Operative Procedures
The D2 lymphadenectomy was always performed according to the
lymph node classification by the Japanese Gastric Cancer Association
[10].
Patients were placed in the supine position and subjected to a 208head-up tilt. After CO2 pneumoperitoneum was induced, using an open
technique, an initial 10-mm trocar for electrolaparoscope was inserted
through the infraumbilical port. The stomach and peritoneal cavity
were carefully examined to exclude patients who had serosal invasion
or 2nd-tier lymph node and distant metastasis. The gastrocolic
ligament was divided using ultrasonic-activated scissors (Laparoscopic
Coagulation Shears [LCS1]; Ethicon Endo-Surgery, Cincinnati, OH)
along the border of the transverse colon with omentum. After left
gastroepiploic vessels were exposed and divided with double clips and
lymph node no. 4sb was removed using the LCS. The dissection was
directed toward the inferior border of the pancreas neck portion with
preserving the middle colic artery. And then, the superior mesenteric
vein, gastrocolic trunk, and right gastroepiploic vein were exposed
to dissect lymph node no. 14v (Fig. 1A). The right gastroepiploic
vessels were divided with double clips at its origin, and lymph node
no. 6 was dissected.
After the anterior portion of the hepatoduodenal ligament was
carefully dissected, the right gastric artery was divided with double
clips at its origin from the proper hepatic artery and lymph nodes no. 5
were dissected. Then, the first part of the duodenum was adequately
dissected and transected 2 cm distal to the pylorus, using a 45-mm
endoscopic stapling device. The common hepatic artery was then
carefully identified and encircled with umbilical tape. With retraction,
the hepatic artery was skeletonized to dissect lymph node nos. 8a and
12 using LCS (Fig. 1B). The lymph node dissection was continued
leftward along the celiac axis (lymph node no. 9), left gastric artery
(lymph node no. 7) and proximal splenic artery (lymph node no. 11p),
and the left gastric vein and the root of the left gastric artery were
divided with double clips. Lymph nodes nos. 1 and 3 were approached
along the upper portion of lesser curvature and dissected. After
midline minilaparotomy in the upper abdomen, Billroth-II (B-II) or
Jejunal pouch interposition (JPI) reconstruction was performed using
the hand-sewn technique.
Statistical Analysis
Statistically significant differences were analyzed by the Pearson
chi-square test or Fisher’s exact test for categorical variables and the
Mann–Whitney U-test for continuous variables. The survival data for
both groups were analyzed by means of the Kaplan–Meier method,
and the log-rank test was used for the assessment of the difference
between two groups. P< 0.05 (two-sided) was considered to be
significant. All statistic analyses were performed using the Statistical
Package for the Social Science (SPSS1) version 12.0 for Windows
(SPSS, Inc., Chicago, IL).
RESULTS
The clinicopathologic characteristics of the study groups are
summarized in Table I. Gender, age, histological type, lymph-node
metastasis, proximal resected margin, the number of retrieved nodes
and metastatic nodes did not differ between groups. The median tumor
size of LADG was smaller than the ODG group (5 (range, 1.7–10) cm
vs. 6 (range, 2–10) cm; P¼ 0.005) and the tumor location was
frequently located in the middle third of the stomach in the LADG
group. As for adjuvant chemotherapy, patient’s general condition or
refusal hindered six patients (23.1%) and eight patients (32.0%) in
LADG and ODG group, respectively, from 5-FU and platinum-based
chemotherapy, which results in no difference in terms of percentage of
patients subjected to adjuvant chemotherapy (P¼ 0.475).
The perioperative data are presented in Table II. There was no
conversion to an open surgery from these laparoscopic procedures.
Postoperative hospital stays, median time to first flatus and start of soft
diet did not differ between the LADG and ODG groups, but the
median time to operate LADG was longer than ODG (255 (range,
155–325) min vs. 190 (range, 115–240) min; P< 0.001) and median
blood loss in LADG was less than ODG (160 (range, 35–385) ml vs.
215 (range, 85–450) ml; P¼ 0.012). Complications in the LADG
group occurred in four patients (15.4%): intraoperative leakage of the
left bile duct in one patient who had a T-tube inserted through
minilaparotomy, two patients with wound seroma and one patient
showing duodenal stump leakage, postoperatively. Postoperative
complications in the ODG group also occurred in four patients
(16.0%): one patient with a wound abscess, one with intra-abdominal
bleeding and two with atelectasis and pleural effusion. However, there
was no difference in morbidity rate for either group and no patients
required re-operation in either group.
Table III summarizes the patients whose cancer recurred in both
groups. During the follow-up period of 26.5 months on average
(median 29.0 months, range, 6–47 months), the recurrence rate in the
LADG group was 30.8% (8/26 cases) and in the ODG group was
24.0% (6/25 cases). The sites of recurrence in the ODG group were
all intra-peritoneal lymph nodes except for one patient who had
Journal of Surgical Oncology
Fig. 1. Laparoscopic view of D2 lymphadenectomy. A: Lymph node no. 14v around the superior mesenteric vein. B: Lymph node no. 12 aroundthe hepatoduodenal ligament (SMV: superior mesenteric vein). [Color figure can be viewed in the online issue, available at www.interscience.wiley.com.]
516 Hur et al.
recurrence in the liver; five out of the six patients that had recurrence
died. However, the recurrent sites of the gastric cancer in the LADG
group were rather variable compared with those in the ODG group,
revealing recurred cancers in the liver, bone, remnant stomach,
peritoneum and intra-peritoneal lymph nodes. The curative resections
of recurrent tumor were possible in four patients who had recurrence in
the remnant stomach and lymph node, and they are following up
without recurrence during 1–34 months.
The cumulative 3-year overall survival rates in LADG and ODG
groups were 88.2% and 77.2% (P¼ 0.246), and the cumulative 3-year
disease-free survival rates were 71.4% and 53.4% (P¼ 0.757),
respectively, with no significant difference between groups (Figs. 2
and 3).
DISCUSSION
Curative resection for gastric cancer essentially requires enough
lymphadenectomy as well as gastric resection plus omentectomy to
improve the therapeutic outcome [11]. The general surgical commu-
nity has concerns about limited lymphadenectomy for laparoscopic
procedures, although several prospective clinical trials have demon-
strated LADG to be superior to the open procedure because it results in
less postoperative pain, faster recovery, and better cosmetic results
[2,3]. As a result, most surgeons perform LADG for EGC in which the
rate of lymph node metastasis is not as high as AGC. Hyung et al. [12]
recently reported that patients with some EGCs, such as submucosal
cancer, which invade the vessels should be performed with D2
lymphadenectomy. Therefore, several surgeons who have experience
with laparoscopic procedures have attempted laparoscopic-extended
D2 lymphadenectomy for oncologic suitability in LAG [13,14]. For
stomach cancer located in the lower-third, lymph nodes around the
hepatoduodenal ligament (no. 12a) and the superior mesenteric vein
(no. 14v) should be included in group 2 by the 13th edition of the
Japanese classification of gastric carcinoma published in 1998 [10]. In
addition, the Japanese Gastric Cancer Association has presented
complete D2 lymph node dissection as the standard therapy for local
AGC [15]. Consequently, a small series of studies have recently
reported the possibility of applying LADG with D2 lymphadenectomy
for AGC [16,17]. However, the fact that there is no study showing the
availability of LADG for AGC in terms of survival rate raises doubts
about its radicality for AGC. In this study, we presented that LADG
with D2 lymphadenectomy was a sufficient procedure for AGC, and
for the first time showed that the follow-up results for patients with
advanced pT2b gastric cancer were acceptable compared with ODG.
Since Uyama et al. [18] reported laparoscopy-assisted total
gastrectomy with D2 lymph node dissection and distal pancreaticos-
plenectomy for advanced upper-third gastric cancer in 1999, there have
been several studies to determine the technical feasibility of D2 lymph
node dissection in AGC [16,17,19]. In our institution, the laparoscopy
procedure for AGC also includes D2 lymphadenectomy, according to
the currently acceptable standard. In particular, special attention is
required to remove lymph nodes around the superior mesenteric vein
(no. 14v) and hepatoduodenal ligament (no. 12a), though we safely
accomplished this. The gastrocolic vein and mid-colic vessels became
the landmark for handling lymph node no. 14v dissection. For lymph
node no. 12a, meticulous dissection and traction of the major
hepatic vessels and bile ducts are also mandatory and this was
accomplished using umbilical tape with protection of the portal vein.
These complicated laparoscopic procedures, especially performed
during early-experienced periods for laparoscopic D2 lymphadenect-
omy, might contribute to a longer operation time and yield non-
superior results of a recovery from the operation when compared to
ODG. Two cases of major complications occurred in our laparoscopic
series, in which left bile-duct injury was related to D2 lymphade-
nectomy. The authors assumed that the bile duct injury occurred
unconsciously through LCS, because lymphadenectomy around porta
hepatis was mainly performed by LCS. Therefore, iatrogenic heat
injury by LCS should be avoided, especially in the interest of
preventing the delayed rupture of a pseudoaneurysm or bile leakage
after dissecting lymph nodes around major vessels and the hepato-
duodenal ligament. Nevertheless, the results of our complication
rate were comparable with other case-controlled studies for EGC
[20,21].
To date, several investigations have reported no differences in
recurrence or survival following LADG and ODG for EGC [2,21,22].
In particular, a randomized controlled trial of EGC showed a similar
curability rate for open and laparoscopic procedures after a mean
follow-up of 52.2 months [2]. In the present study for AGC, though a
short follow-up period was used, patients who had tumor invading into
Journal of Surgical Oncology
TABLE I. Clinicopathological Characteristics
Variable LADG (n¼ 26) ODG (n¼ 25) P
Sex
Male 19 19 0.811
Female 7 6
Age
<60 years 15 10 0.206
�60 years 11 15
Reconstruction
B-I 0 2 0.171
B-II 25 20
JPI 1 3
Tumor location
Body 6 1 0.048
Antrum 20 24
Histological type
Differentiated 13 15 0.795
Undifferentiated 13 10
LN metastasis
N0 11 6 0.324
N1 9 9
N2 4 8
N3 2 2
Tumor sizea (cm) 5 (1.7–10) 6 (2–10) 0.005
PRMa (cm) 4.25 (1.5–10) 5 (0.5–11) 0.205
No. of retrieved nodea 30.5 (12–78) 35 (12–83) 0.129
No. of metastatic nodea 2 (0–44) 5 (0–22) 0.166
Adjuvant treatment
Yes 20 17 0.475
None 6 8
LN, lymph node; PRM, proximal resection margin.aMedian (range).
TABLE II. Surgical Outcomes and Postoperative Courses
Variable LADG (n¼ 26) ODG (n¼ 25) P value
Operative timea (min) 255 (155–325) 190 (115–240) <0.001
Blood lossa (ml) 160 (35–385) 215 (85–450) 0.012
Hospital staya (days) 7 (6–22) 9 (5–18) 0.137
Time to first flatusa (days) 2 (1–4) 2 (1–4) 0.527
Time to soft dieta (days) 4 (4–6) 4 (2–8) 0.906
Postoperative complicationsb 4 (15.4) 4 (16.0) 1.000
Wound problems 2 1
Intra-abdominal bleeding 0 1
Leakage 1 0
Bile duct injury 1 0
Lung complication 0 2
B-I, Billroth-I; B-II, Billroth-II; JPI, jejunal pouch interposition.aMedian (range).bNumber(percentages).
LADG With D2 Lymphadenectomy for AGCa 517
the subserosa did not show different survival or recurrent rates between
the procedures.
The pT2b patients of our study were selected for the following three
reasons. First, several retrospective studies reported that patents with
T2b had worse prognoses than patients with T2a [5,7,8]. Park et al. [7]
reported that 5-year survival rates of patients with pT2a versus pT2b
cancer were 85.5% versus 55.7%. Second, laparoscopic curative
surgery for serosa-exposed (T3) AGC is not acceptable yet, because
there would be peritoneal seeding of malignant cells in dealing with
possible metastatic lymph nodes or a risk of port-site recurrence as
seen in a recent report [23]. In addition, a recent meta-analysis about
pre-operative accuracy of various imaging modalities showed that
sensitivity and specificity were higher in patients with gastric cancer
with serosa involvement than other patients [6]. Meanwhile, our results
have several limitations such as possible selection bias owing to non-
randomization, short periods of follow-up and small object numbers.
However, most clinicopathologic features except for tumor size were
well distributed over two groups, and this is the first comparison study
about the application of laparoscopic surgery on AGC which was
performed by one surgeon and institution. As such, our results in
following up with pT2b patients, in which surgeons were able to apply
a laparoscopic procedure on pre-operative serosa not exposed to gastric
cancer, would be more meaningful to address these points.
Interestingly, our results regarding recurrence pattern showed little
difference in the recurrence site despite the small number of cases.
While the major recurrent sites in the ODG group were intra-peritoneal
lymph nodes, the sites of recurrence in the LADG group were more
variable such as liver, bone, remnant stomach and so on, most
recurrences of patients in LADG group were able to be resects
curatively. These results suggest that our procedure for lymphade-
nectomy was sufficient for T2b cancer. On the other hand, regarding
the recurrence pattern, several in vivo studies have shown laparoscopy
with carbon dioxide insufflations seemed to stimulate the growth of
dormant tumor cells into overt liver metastases [24,25]. However,
further experimental studies and clinical data collection are necessary
to confirm the different recurrence pattern between the two groups.
Journal of Surgical Oncology
TABLE III. Summary of Recurrent Cases
No Sex Age pTNM Stage
Recurrence
Status
OS
(months)Site DFS (months) Tx
LADG
1 Male 45 T2bN1M0 II Liver 7 Resection Alive 41
2 Female 50 T2bN2M0 IIIa Bone 19 CTx Dead 20
3 Female 38 T2bN2M0 IIIa Bone 28 None Dead 29
4 Male 59 T2bN1M0 II Cp 12 CTx Alive 14
5 Male 65 T2bN3M0 IIIa Ln 36 Resection Alive 37
6 Male 58 T2bN2M0 IIIa Rs 31 Resection Alive 40
7 Male 69 T2bN3M0 IV Rs 12 CTx Alive 14
8 Female 38 T2bN0M0 Ib Rs 12 Resection Alive 23
ODG
1 Female 76 T2bN2M0 IIIa LN 6 None Dead 13
2 Male 79 T2bN2M0 IIIa LN 15 CTx Dead 21
3 Male 44 T2bN3M0 IV LN 9 CTx Dead 12
4 Male 74 T2bN2M0 IIIa LN 7 CTx Dead 17
5 Male 72 T2bN2M0 IIIa LN 11 None Dead 16
6 Male 34 T2bN2N0 IIIa liver 25 CTx Alive 32
pTNM, pathologic tumor node metastasis; DFS, disease-free survival; Tx, treatment; OS, overall survival; CTx, chemotherapy; Cp, Carcinomatosis Peritoni;
RS, remnant stomach; LN, lymph node.
Fig. 2. Comparison of cumulative overall survival rate accordingto operation methods during a 3-year interval by Log rank test(P¼ 0.246) (LADG: laparoscopy-assisted distal gastrectomy; ODG:open distal gastrectomy).
Fig. 3. Comparison of cumulative disease-free survival rate accord-ing to operation methods during a 3-year interval by Log rank test(P¼ 0.757) (LADG: laparoscopy-assisted distal gastrectomy; ODG:open distal gastrectomy).
518 Hur et al.
In conclusion, LADG with D2 lymphadenectomy was performed in
locally advanced T2b cancer, and early follow-up results demonstrated
that LADG had technically and oncologically satisfactory results.
This study showed that LADG for T2b advanced gastric cancer was
equivalent to ODG in terms of surgical morbidity, mortality and
survival. Consequently, LADG could be applied for locally advanced
cancer without serosal exposure and perigastric lymph node meta-
stasis. However, longer follow-up studies as well as additional
prospective clinical trials will be needed to confirm the oncologic
security of LADG for AGC.
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LADG With D2 Lymphadenectomy for AGCa 519
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