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.

REFERENCES

1. Kitano S, Iso Y, Moriyama M, et al.: Laparoscopy-assistedBillroth I gastrectomy. Surg Laparosc Endosc 1994;4:146–148.

2. Huscher CG, Mingoli A, Sgarzini G, et al.: Laparoscopic versusopen subtotal gastrectomy for distal gastric cancer: Five-yearresults of a randomized prospective trial. Ann Surg 2005;241:232–237.

3. Kitano S, Shiraishi N, Fujii K, et al.: A randomized controlledtrial comparing open vs laparoscopy-assisted distal gastrectomyfor the treatment of early gastric cancer: An interim report.Surgery 2002;131:S306–S311.

4. Hur H, Jeon HM, Kim W: Laparoscopic pancreas- and spleen-preserving D2 lymph node dissection in advanced (cT2) upper-third gastric cancer. J Surg Oncol 2008;97:169–172.

5. Harrison JC, Dean PJ, Vander Zwaag R, et al.: Adenocarcinomaof the stomach with invasion limited to the muscularis propria.Hum Pathol 1991;22:111–117.

6. Kwee RM, Kwee TC: Imaging in local staging of gastric cancer:A systematic review. J Clin Oncol 2007;25:2107–2116.

7. Park do J, Kong SH, Lee HJ, et al.: Subclassification of pT2gastric adenocarcinoma according to depth of invasion (pT2a vspT2b) and lymph node status (pN). Surgery 2007;141:757–763.

8. Sarela AI, Turnbull AD, Coit DG, et al.: Accurate lymph nodestaging is of greater prognostic importance than subclassificationof the T2 category for gastric adenocarcinoma. Ann Surg Oncol2003;10:783–791.

9. Roukos DH, Lorenz M, Karakostas K, et al.: Pathological serosaand node-based classification accurately predicts gastric cancerrecurrence risk and outcome, and determines potential andlimitation of a Japanese-style extensive surgery for Westernpatients: A prospective with quality control 10-year follow-upstudy. Br J Cancer 2001;84:1602–1609.

10. Japanese Gastric Cancer Association: Japanese Classification ofGastric Carcinoma—2nd English Edition. Gastric Cancer 1998;1:10–24.

11. Kim JP: Current status of surgical treatment of gastric cancer.J Surg Oncol 2002;79:79–80.

12. Hyung WJ, Cheong JH, Kim J, et al.: Application of minimallyinvasive treatment for early gastric cancer. J Surg Oncol 2004;85:181–185.

13. Noshiro H, Nagai E, Shimizu S, et al.: Laparoscopicallyassisted distal gastrectomy with standard radical lymph nodedissection for gastric cancer. Surg Endosc 2005;19:1592–1596.

14. Song KY, Kim SN, Park CH: Laparoscopy-assisted distalgastrectomy with D2 lymph node dissection for gastric cancer:Technical and oncologic aspects. Surg Endosc 2007;22:655–659.

15. Nakajima T: Gastric cancer treatment guidelines in Japan. GastricCancer 2002;5:1–5.

16. Goh PM, Khan AZ, So JB, et al.: Early experience with laparo-scopic radical gastrectomy for advanced gastric cancer. SurgLaparosc Endosc Percutan Technol 2001;11:83–87.

17. Ziqiang W, Feng Q, Zhimin C, et al.: Comparison of laparoscopi-cally assisted and open radical distal gastrectomy with extendedlymphadenectomy for gastric cancer management. Surg Endosc2006;20:1738–1743.

18. Uyama I, Sugioka A, Fujita J, et al.: Laparoscopic totalgastrectomy with distal pancreatosplenectomy and D2 lympha-denectomy for advanced gastric cancer. Gastric Cancer 1999;2:230–234.

19. Uyama I, Sugioka A, Matsui H, et al.: Laparoscopic D2 lymphnode dissection for advanced gastric cancer located in the middleor lower third portion of the stomach. Gastric Cancer 2000;3:50–55.

20. Huscher CG, Mingoli A, Sgarzini G, et al.: Videolaparoscopictotal and subtotal gastrectomy with extended lymph nodedissection for gastric cancer. Am J Surg 2004;188:728–735.

21. Mochiki E, Kamiyama Y, Aihara R, et al.: Laparoscopic assisteddistal gastrectomy for early gastric cancer: Five years’ experience.Surgery 2005;137:317–322.

22. Kitano S, Shiraishi N, Uyama I, et al.: A multicenter study ononcologic outcome of laparoscopic gastrectomy for early cancerin Japan. Ann Surg 2007;245:68–72.

23. Lee YJ, Ha WS, Park ST, et al.: Port-site recurrence afterlaparoscopy-assisted gastrectomy: Report of the first case. JLaparoendosc Adv Surg Technol A 2007;17:455–457.

24. Gutt CN, Riemer V, Kim ZG, et al.: Impact of laparoscopicsurgery on experimental hepatic metastases. Br J Surg 2001;88:371–375.

25. Kim ZG, Mehl C, Lorenz M, et al.: Impact of laparoscopicCO2-insufflation on tumor-associated molecules in culturedcolorectal cancer cells. Surg Endosc 2002;16:1182–1186.

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