ORIGINAL ARTICLES

A Multicenter Study on Oncologic Outcome of

Laparoscopic Gastrectomy for Early Cancer in Japan
Seigo Kitano, MD, PhD,* Norio Shiraishi, MD, PhD,* Ichiro Uyama, MD, PhD,†
Kenichi Sugihara, MD, PhD,‡ Nobuhiko Tanigawa, MD, PhD,§ and the
Japanese Laparoscopic Surgery Study Group

increased use of mass and individual screenings.1,2 For the

Background: Laparoscopic surgery for gastric cancer is technically
feasible, but it is not widely accepted because it has not been
management of patients with early gastric cancer (EGC),
evaluated from the standpoint of oncologic outcome. We conducted
minimally invasive therapies, such as endoscopic and lapa-
a retrospective, multicenter study of a large series of patients in
roscopic procedures, have been available since the 1980s.3,4
Japan to evaluate the short- and long-term outcomes of laparoscopic
Since the first report of laparoscopy-assisted distal gastrec-
gastrectomy for early gastric cancer (EGC). tomy (LADG) in 1994, LADG has been widely adopted for
Methods: The study group comprised 1294 patients who underwent EGC and the number of patients undergoing LADG has been
laparoscopic gastrectomy during the period April 1994 through increasing in Japan.5 Laparoscopy-assisted gastrectomy (LAG)
December 2003 in 16 participating surgical units (Japanese Lapa- is now performed not only as distal gastrectomy but also as
roscopic Surgery Study Group). The short- and long-term outcomes proximal gastrectomy and total gastrectomy.6 – 8
of these patients were examined. Several small retrospective studies analyzing the short-
Results: Distal gastrectomy was performed in 1185 patients (91.5%), term outcome of LAG showed that patients who underwent
proximal gastrectomy in 54 (4.2%), and total gastrectomy in 55 (4.3%); LAG had less pain, earlier recovery to active daily life, a
all were performed laparoscopically. The morbidity and mortality rates shorter hospital stay, and better quality of life than patients
associated with these operations were 14.8% and 0%, respectively. who underwent conventional open surgery.9 –11 However,
Histologically, 1212 patients (93.7%) had stage IA disease, 75 (5.8%) LAG for the treatment of malignancies remains controversial
had stage IB disease, and 7 (0.5%) had stage II disease (the UICC because of the lack of large-scale study data on the short-term
staging). Cancer recurred in only 6 (0.6%) of 1294 patients treated and long-term outcomes.
curatively (median follow-up, 36 months; range, 13–113 months). The To clarify the short- and long-term outcomes of LAG
5-year disease-free survival rate was 99.8% for stage IA disease, 98.7% for EGC, we examined the clinical data obtained by 16
for stage IB disease, and 85.7% for stage II disease. surgical departments that are members of the Japanese Lapa-
Conclusions: Although our findings may be considered preliminary, roscopic Surgery Study Group.
our data indicate that laparoscopic surgery for EGC yields good
short- and long-term oncologic outcomes.
MATERIALS AND METHODS
(Ann Surg 2007;245: 68 –72) The study included 1294 patients with EGC who under-
went LAG in one of the 16 participating departments during the
period 1994 through 2003. The patients who underwent LAG in
each institution for that period were all registered for the present
In Japan, the incidence of early gastric cancer has increased
to more than 50% of the overall incidence of gastric cancer
because of the development of diagnostic instruments and
study. All tumors were adenocarcinomas that were shown by
preoperative gastric endoscopy and barium meal study to be
present only in the mucosal or submucosal layer of the stomach
and were not candidates for endoscopic mucosal resection.
From the *Department of Surgery I, Oita University Faculty of Medicine, Patients with cancer in another organ or with previous upper
Oita, Japan; †Department of Surgery, Fujita Health University Hospital, abdominal laparotomy or with cardiac, pulmonary, or hepatic
Nagoya, Japan; ‡Department of Surgical Oncology, Tokyo Medical and insufficiency were not included. The exclusion criteria in insuf-
Dental University, Tokyo, Japan; and §Department of Surgery, Osaka ficiency of the organs were 1) operative cardiovascular risk
Medical College, Osaka, Japan.
Supported in part by a Grant-in-Aid for Cancer Research from the Japanese greater than New York Heart Association II, 2) operative pul-
Ministry of Health, Labor, and Welfare (No. 13-17). monary risk greater than Hugh-Jones II, and 3) severe liver
Reprints: Seigo Kitano, MD, Department of Surgery I, Oita University disease (Child classes B and C). All participating surgeons were
Faculty of Medicine, 1-1 Idaigaoka, Yufu, Oita 879-5593, Japan. E-mail: personally responsible for obtaining the written informed con-
[email protected].
Copyright © 2006 by Lippincott Williams & Wilkins
sent of their patients. According to the location of the tumor,
ISSN: 0003-4932/07/24501-0068 LADG, laparoscopy-assisted proximal gastrectomy (LAPG), or
DOI: 10.1097/01.sla.0000225364.03133.f8 laparoscopy-assisted total gastrectomy (LATG) was performed.

68 Annals of Surgery • Volume 245, Number 1, January 2007

Annals of Surgery • Volume 245, Number 1, January 2007 Laparoscopic Gastrectomy for Early Cancer in Japan

As described previously,5,6,8 LAG consisted of the lated by the Kaplan-Meier method. A P value of ⬍0.05 was
following procedures: 1) laparoscopic dissection of the lesser considered significant.
and greater omentum, ligation and division of the main
vessels to mobilize the stomach under pneumoperitoneum, 2)
laparoscopic D1⫹␣, D1⫹␤, or D2 lymph node dissection, RESULTS
based on the Guidelines of the Japan Gastric Cancer Associ- Laparoscopic procedures consisted of 1185 (91.5%)
ation, and 3) resection of the distal two thirds (LADG), LADGs, 54 (4.2%) LAPGs, and 55 (4.3%) LATGs, and the
proximal third (LAPG), or total stomach (LATG), depending total patient group comprised 872 men and 422 women. The
on the location of the tumor, followed by reconstruction by clinicopathologic characteristics of the study patients are shown
the Billroth-I, esophagogastrostomy, or Roux-en-Y method in Table 1. The percentages of female patients and of mildly
through a 5- to 7-cm-long minilaparotomy incision. To es- obese patients were greater in the LADG group than in the
tablish techniques of LAG as an oncologic surgery, the other groups. D1⫹␤ and D2 lymph node dissection were
laparoscopic procedures for lymph node dissection in each performed frequently in the LADG group because of the high
institution had been reviewed by video examination in the frequency of signet-ring cells carcinoma. The operation time
group conferences. of LATG was longer than that of LADG or LAPG. There
Data obtained for each patient included the following: were no other differences between groups in patient charac-
age, sex, body mass index, previous laparotomy, surgical teristics or pathologic characteristics of tumors. According to
procedure, operation time, conversion to open surgery, post- UICC staging, there were 1212 (93.7%) stage IA tumors, 75
operative complications, postoperative oncologic outcome, (5.8%) stage IB tumors, and 7 (0.5%) stage II tumors.
histologic type of tumor, depth of tumor invasion, lymph Intraoperative and postoperative complications oc-
node metastasis, and clinical stage according to the UICC curred in 25 (1.9%) of the 1294 patients and 167 patients
staging and the WHO classification of tumors.12,13 (12.9%), respectively (Table 2). Conversion to open surgery
All patients were monitored postoperatively by physi- was required in only 14 cases (1.1%) because of intraopera-
cal examination, and blood tests including a test for serum tive complications: bleeding in 9 cases, mechanical trouble in
carcinoembryonic antigen at least every 3 months for the first 3, and others in 2. Bleeding was the most frequent intraop-
year, every 6 months for the next 2 years, and every year for erative complication, and it resulted mainly from the injury to
5 years, and thereafter by abdominal ultrasonography, com- the branches of the left gastric artery, short gastric vein, or
puted tomography, chest radiography, and gastroscopy at spleen. Intraoperative complications occurred more fre-
least once each year. quently during LAPG than during other laparoscopic proce-
Data were compared between the three types of lapa- dures (P ⬍ 0.05). The most frequent postoperative compli-
roscopic surgeries (LADG, LAPG, and LATG). Differences cations were anastomotic stenosis, anastomotic leakage, and
in categorical variables such as postoperative complications, wound infection, and there was no significant difference in
tumor recurrences, and other clinicopathologic factors were the incidence of postoperative complications between lapa-
analyzed by ␹2 test, and differences in continuous variables roscopic procedures. Intraoperative and postoperative com-
were analyzed by Student t test. Survival rates were calcu- plications were not associated with any of the factors studied,

TABLE 1. Clinicopathologic Characteristics of Patients With Early Gastric Cancer

No. of Patients
LADG (n ⴝ 1185) LAPG (n ⴝ 54) LATG (n ⴝ 55) P
Patients
Age (yr) 62.7 ⫾ 11 63.7 ⫾ 9 62.1 ⫾ 12 NS
Male/female 786/399 41/13 45/10 ⬍0.05*
BMI (⬍25/25–30/⬎30) 1002/176/7 40/13/1 52/2/1 ⬍0.05*
Post-EMR (yes/no) 49/1136 2/52 0/55 NS
Previous laparotomy (presence/absence) 120/1065 5/49 6/49 NS
Operation
Lymph node dissection (D1⫹␣/D1⫹␤/D2) 429/549/207 31/20/3 6/45/4 ⬍0.05*
Operation time (min) 253.1 ⫾ 19 229.4 ⫾ 31 271.4 ⫾ 26 ⬍0.05*
Tumor
Histologic type (tubular adenocarcinoma/ 933/223/29 50/3/1 46/5/4 ⬍0.05*
signet-ring cell carcinoma/others)
Tumor depth (mucosa/submucosa) 729/456 25/29 27/28 ⬍0.05*
Lymph node metastasis (N0/N1/N2) 1111/68/6 49/4/1 52/3/0 NS
Tumor staging† (stage IA/IB/II) 1111/68/6 49/4/1 52/3/0 NS
Data are mean ⫾ SD or number. NS, not significant; BMI, body mass index.
*Statistical significance.
†
Tumor staging is classified by UICC staging.

© 2006 Lippincott Williams & Wilkins 69

Kitano et al Annals of Surgery • Volume 245, Number 1, January 2007

TABLE 2. Intraoperative and Postoperative Complications

No. (%) of Patients
LADG LAPG LATG
Complications (n ⴝ 1185) (n ⴝ 54) (n ⴝ 55) P
Intraoperative 20 (1.7%) 4 (7.4%) 1 (1.8%) ⬍0.05*
Bleeding 11 1 0
Perforation 0 1 0
Organ injury 5 0 0
Machine trouble 1 2 1
Others 3 0 0
Postoperative 151 (12.7%) 10 (18.5%) 6 (10.9%) NS
Bleeding 13 0 1
Anastomotic 35 3 0 FIGURE 1. The disease-free survival rate in 1294 treated pa-
stenosis tients with early gastric cancer. The 5-year disease-free sur-
Anastomotic 25 3 0 vival rate was 99.8% for stage IA, 98.7% for stage IB, and
leakage 85.7% for stage II. Tumor staging system is used with classi-
Intraabdominal 17 0 0 fication by the UICC staging.
abscess
Pancreas injury 12 0 2
Ileus 3 0 0 Since LADG for EGC was first reported in 1994,5
Respiratory 9 0 0 several laparoscopic procedures for EGC have been devel-
complication oped and have been performed by a limited number of
Wound infection 16 2 2 surgeons.6 – 8 Over the last decade, the number of LAGs for
Port-metastasis 0 0 0 early cancer has rapidly increased, and the indication for
Others 21 2 1 LAG has extended to advanced cancer.17 Several studies of
NS, not significant.
the short-term outcome of LAG in comparison to open
*Statistical significance. gastrectomy showed the several advantages of LAG, includ-
ing less invasiveness, less pain, earlier recovery of bowel
movement, and shorter hospital stay.9 –11 We have reported
additional advantages of LADG, including less impaired
including sex, age, body mass index, history of laparotomy respiratory function, better preservation of postoperative TH1
and tumor stage. cell-mediated immune function, and better postoperative
There were only 6 cancer recurrences, 1 local recur- quality of life.18 Some studies, however, indicated technical
rence, 1 lymph node recurrence, 2 peritoneal disseminations, difficulties and limitations in lymph node dissection per-
1 liver metastasis, and 1 skin metastasis at the abdominal wall formed during LAG.19 Therefore, we performed a retrospec-
different from the port-site, during the median follow-up tive multicenter study to clarify the technical feasibility and
period of 36 months (range, 13–113 months). The cancer in oncologic outcome of LAG for EGC in Japan.
all 6 recurrent cases invaded to the deeper submucosal layer. The prognosis of patients with EGC is known to be
In 3 of 6 cases, lymph node metastasis (N2) was detected excellent, with 5-year survival rates of 90% or more.15,16
histologically, and the tumors were classified as stage II Multivariate analysis has shown that lymph node metastasis
tumors. Recurrence was not associated with any surgical is the only significant predictive factor for recurrence of
procedure, complications, or conversion to open gastrectomy.
The 5-year disease-free survival rate was 99.8% for stage IA
disease, 98.7% for stage IB disease, and 85.7% for stage II
(Fig. 1). The 5-year disease-free survival rate was 99.4% for
patients who underwent LADG, 98.7% for those who under-
went LAPG, and 93.7% for those who underwent LATG
(Fig. 2).

DISCUSSION
This retrospective multicenter study is the first investi-
gation of short- and long-term outcomes of LAG for EGC in
a large series of patients in Japan. Both the mortality rate and
the morbidity rate associated with LAG were shown to be as
low as those of conventional open gastrectomy,14 and the 5-year
survival rate of patients who underwent LAG for EGC was as FIGURE 2. The disease-free survival rate according to opera-
good as that of patients who underwent conventional open tion. The 5-year disease-free survival rate was 99.4% for
surgery for EGC.15,16 LADG, 98.7% for LAPG, and 93.2% for LATG.

70 © 2006 Lippincott Williams & Wilkins

Annals of Surgery • Volume 245, Number 1, January 2007 Laparoscopic Gastrectomy for Early Cancer in Japan

EGC.20 Several recent studies showed that the extent of present study, the mortality and morbidity rates were 0% and
lymph node metastasis in patient with EGC was associated 14.8%, respectively, and the rate of conversion to open
with tumor size and depth of invasion.21 However, the extent surgery was 1.1%. The conversion to open surgery in LAG
of lymph node dissection for EGC remains controversial.22 In for EGC was not associated with worse short- and long-term
the patients included in the present study, the lymph node outcome in the present study. As laparoscopic surgeries for
dissection was performed laparoscopically according to the gastrointestinal disease have been considered as technically
Guidelines of the Japanese Gastric Cancer Association. Sev- complex procedures with longer operation time, the signifi-
eral studies have evaluated laparoscopic lymph node dissec- cance of learning curve has been emphasized to perform them
tion. Adachi et al, in a retrospective study of 96 patients with safely.29,30 Although, in the present study, it seemed to take
EGC, showed that the number of lymph nodes dissected more 30 to 60 minutes to perform LAG than open gastrec-
laparoscopically was no different from that of lymph node tomy, the incidence of operative complications was as low for
dissected during open surgery.9 Yano et al also conducted a LAG as it was for open surgery. These findings suggest that
retrospective study of patients with EGC and reported that the LAG with longer operation time is safe for EGC.
number of resected lymph nodes in D1⫹␣ lymph node
dissection did not differ between LAG and open gastrecto- CONCLUSION
my.23 On the contrary, Miura et al showed less number of Our multicenter study of a large patient series showed
dissected lymph nodes along major curvature and the celiac that LAG is safe for EGC, with an oncologic outcome as
and splenic arteries in LAG than open gastrectomy.24 In the good as that of conventional open surgery. Results of this
present retrospective study, which covered a quite long time retrospective nonrandomized clinical analysis should be con-
period, the number of resected lymph nodes could not be firmed by large-scale prospective randomized trials.
evaluated because data of the number of resected lymph
nodes in several institutions were incomplete. To establish ACKNOWLEDGMENTS
techniques of LAG as an oncologic surgery, the laparoscopic The following centers and surgeons participated in the
procedures for lymph node dissection in each institution multicenter study initiated by the Japanese Laparoscopic
had been reviewed by video examination in the group Surgery Study Group (JLSSG): Seigo Kitano, Norio Shi-
conferences. raishi, Masafumi Inomata, Kazuhiro Yasuda, Oita University
There are few studies on the long-term outcome of Faculty of Medicine (Oita); Ichiro Uyama, Masahiro Ochiai,
LAG for EGC. Huscher et al25 recently showed, on the basis Fujita Health University Hospital (Aichi); Kenichi Sugihara,
of the first prospective randomized trial in small series of 59 Kazuyuki Kojima, Masayuki Enomoto, Masamichi Yasuno,
patients with EGC or advanced gastric cancer comparing the Tokyo Medical and Dental University (Tokyo); Nobuhiko Tani-
5-year results of subtotal gastrectomy against those of with gawa, Osaka Medical University (Osaka); Hitoshi Katai, Na-
laparoscopic and open approaches, that LAG is a safe onco- tional Cancer Center Hospital (Tokyo); Shinei Kudo, Showa
logic procedure; ie, the oncologic outcome matches that of University Northern Yokohama Hospital (Yokohama); Shinichi
conventional open surgery.25 Our preliminary prospective Sakuramoto, Kitasato University, School of Medicine (Kana-
randomized trial with a mean follow-up period of 21.5 gawa); Shuji Takiguchi, Morito Monden, Osaka University
months showed no difference in curability between laparo- (Osaka); Shinya Tanimura, Masayuki Higashino, Yosuke Fuku-
scopic and open procedures for EGC.26 Weber et al also did naga, Osaka City General Hospital (Osaka); Yugo Nagai, Izumi
not observe a difference in the 18-month survival rate between Otsu Municipal Hospital (Osaka), Hirokazu Noshiro, Kyusyu
patients with gastric cancer who underwent LAG and those who University Graduate School of Medicine (Fukuoka), Ken Ha-
underwent open gastrectomy.27 Although the present multi- yashi, Showa Inan General Hospital, Center on Endoscopic
center study of a large patient series was an uncontrolled study Surgery (Nagano); Hideki Hayashi, Takenori Ochiai, Graduate
and the follow-up period was short, the survival rate of patients School of Medicine, Chiba University (Chiba); Tetsu Fukunaga,
with EGC who underwent LAG was shown to be good. These The Cancer Institute Hospital of Japanese Foundation for Can-
data suggest that LAG is feasible for EGC from the standpoint cer Research (JFCR) (Tokyo); Masaki Fukunaga, Juntendo
of oncologic outcome. Urayasu Hospital, Juntendo University School of Medicine
Several studies have investigated mortality and mor- (Chiba); Minoru Matsuda, Tomokazu Hoshi, Shinichi Kasai,
bidity associated with LAG. Huscher et al reported LAG- Surugadai Nihon University Hospital (Tokyo); Tatsuo Ya-
associated mortality and morbidity rates of 3.3% and 26.7%, makawa, Nobuo Murata, Teikyo University, Mizonokuchi Hos-
respectively, in a randomized trial, and these rates were the pital (Kanagawa); Katsuhiko Yanaga, Jikei University School of
same as those of open gastrectomy.25 Adachi et al reported, Medicine (Tokyo).
on the basis of a retrospective study comparing 49 LAGs and
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