Yonago Acta medica 2008;51:25–30

Laparoscopy-Assisted Pylorus-Preserving Gastrectomy
for Treating Early Gastric Cancer
Hiroaki Saito, Yoji Fukumoto, Tomohiro Osaki, Yoshinori Yamada, Kenji Fukuda,
Shigeru Tatebe, Shunichi Tsujitani and Masahide Ikeguchi
Division of Surgical Oncology, Department of Surgery, School of Medicine, Tottori University
Faculty of Medicine, Yonago 683-8504 Japan

Laparoscopy-assisted pylorus-preserving gastrectomy (LAPPG) with lymphadenectomy
has been used for treating early gastric cancer located in the middle-third of the stomach. However, firm evidence supporting its safety and usefulness is scant. This study
examined 24 and 10 gastric adenocarcinoma patients who had undergone conventional
pylorus-preserving gastrectomy (CPPG) and LAPPG, respectively, at our institution.
Operation time for LAPPG (362.8 ± 49.6 min) was significantly longer than that for
CPPG (221.9 ± 50.0 min; P = 0.04). Estimated blood loss with LAPPG (127.5 ± 91.2 mL)
was not significantly different from that with CPPG (167.9 ± 149.9 mL; P = 0.44). Total
number of resected lymph nodes was 26.3 ± 9.5 and 21.3 ± 10.8 with LAPPG and CPPG,
respectively, with no statistically significant difference. C-reactive protein in serum on
postoperative day 1 was significantly lower in the LAPPG than in the CPPG group (5.3 ±1.7 mg/dL versus 7.8 ± 3.6 mg/dL; P = 0.049). The requirement for analgesia after surgery was more frequent in the CPPG than in the LAPPG group (3.7 ± 2.0 versus 2.2 ± 1.7;
P = 0.04). Time to first flatus was shorter in the LAPPG than in the CPPG group (1.9 ±0.9 days versus 3.1 ± 0.9 days; P = 0.0006). Postoperative hospital stay was significantly
shorter in the LAPPG than in the CPPG group (12.0 ± 4.0 days versus 23.0 ± 10.7days;
P = 0.0036). With regard to postoperative complications, stasis was observed more frequently in the CPPG (33.3%) than in the LAPPG (10%) group. In conclusion, patientstreated by LAPPG showed a comparable quality of surgical operation compared withthose treated by CPPG.
Key words: early gastric cancer; laparoscopy-assisted pylorus-preserving gastrectomy; pylorus
preservation

Gastric cancer is one of the most common cancers
in Asia and its mortality still ranks second among
all cancer deaths worldwide (Ries et al., 2003).
Recent progress in endoscopic devices and diagnostic techniques has improved the early detection
rate. Since the prognosis of patients with earlygastric cancer is extremely good in Japan, minimally invasive treatment or function-preserving

techniques, such as endoscopic mucosal resection,
endoscopic submucosal dissection and laparoscopic surgery, are used increasingly to maintainquality of life after treatment. Endoscopic resection enables resection of primary tumor and isindicated for nearly all mucosal cancers without
lymph node metastasis (Gotoda et al., 2000).
However, about 10% of early gastric cancers have

Abbreviations: CPPG, conventional PPG; LADG, laparoscopy-assisted distal gastrectomy; LAPPG, laparoscopy-assisted PPG; LCS, laparosonic coagulation shears; PPG, pylorus-preserving gastrectomy25

H. Saito et al.

tion between September 1997 and May 2007, and10 patients who had undergone LAPPG between
September 2006 and May 2007. The clinicopathological findings were determined according
to the Japanese Classification of Gastric Cancer(Japanese Gastric Cancer Association, 1998). Patient background is shown in Table 1. There were
no differences in background except the distanceof preserved pylorus between LAPPG and CPPG.
All tumors were classified histologically as adenocarcinomas that had invaded only the mucosa
or submucosa of the stomach without lymph nodemetastasis (cT1, cN0). Clinical classification oftumor depth (cT) and nodal involvement (cN) was
determined by preoperative and intraoperativeevaluation, including barium radiography, uppergastrointestinal tract endoscopy, abdominal ultrasonography, computed tomography and endoscopic ultrasonography. Intramucosal or submucosal
carcinoma without lymph node metastasis (cT1,cN0) located in the middle-third of the stomach
is indicated for either CPPG or LAPPG. The exclusion criteria affected patients who had cardiac(greater than New York Heart Association II),
pulmonary (greater than Hugh-Jones II), hepatic(Child classes B and C) or renal insufficiency.

lymph node metastasis, and gastrectomy withlymph node dissection remains the treatment ofchoice for mucosal cancers with high possibility
of lymph node metastasis and submucosal cancers(Kikuchi et al., 2004). Laparoscopy-assisted distal gastrectomy (LADG) was first performed inJapan in 1991 and has recently been used increasingly in gastric cancer operations because it has
been associated with less postoperative pain, an
early return of bowel function, shorter periods of
hospitalization and disability and better cosmetic
results (Kitano et al., 1994; Mochiki et al., 2002).
LADG with perigastric lymph node dissection isreadily applicable to T1 stage gastric cancer.
Pylorus-preserving gastrectomy (PPG),
which retains pyloric ring and gastric function,
was first performed in 1967 (Maki et al., 1967).
It was used as an alternative treatment for gastriculcer, in order to prevent postoperative dumping
syndrome and bile-juice reflux. Recently, PPG
with radical lymph node dissection has beenused for patients with early gastric cancer. Like
LADG, laparoscopy-assisted PPG (LAPPG) withlymphadenectomy has been applied for treating
early gastric cancer located in the middle-third of
the stomach instead of conventional PPG (CPPG).
Hiki et al. (2006) recently demonstrated thatclinical outcomes of surgical treatment were comparable for gastric cancer patients who underwent
LAPPG and those treated with CPPG in termsof station-dependent lymph node dissection, andestimated blood loss. However, firm evidence
supporting its safety and usefulness is scant compared to LADG. Therefore, this study was undertaken to compare LAPPG and CPPG with respect
to quality of lymph node dissection and otherclinical outcomes.

Surgical procedure
For CPPG, the peritoneal cavity is accessed
through an upper medican incision. For LAPPG,
the pneumoperitoneum is created by injection ofcarbon dioxide to 8 to10 mmHg and the laparoscopy is inserted through the umbilical port. Under the view of the laparoscopic image, a total of
4 ports including two 5-mm ports and two 12-mm
ports are inserted into the left upper, left lower,right upper and right lower quadrants. For CPPG
and LAPPG, the gastrocolic ligament is divided 4
cm distal to the epiploic arcade to reach the lesser
peritoneal cavity. During LAPPG, laparosoniccoagulation shears (LCS; Ethicon Endo-Surgery,Cincinnati, OH) is used. Toward the lower pole ofthe spleen-dividing gastrocolic ligament, the left
gastroepiploic vein and artery are exposed andMaterials and Methods
Patients
This study examined 24 gastric adenocarcinoma
patients who had undergone CPPG at our institu26

LAPPG in early gastric cancer
Table 1. Background of patients included in the present study
					
Variable
LAPPG

CPPG

P valueAge(year)
57.5 ± 11.3
62.0 ± 10.3
0.27
GenderMale		
612
0.59
Female		412Tumor size(cm)
2.2 ± 0.8
2.0 ± 0.9
0.41
Macroscopic appearance*
Protruded		03
0.61
Depressed type		
10
21
Histology†					Differentiated		
5
14
0.95
Undifferentiated		510Depth of invasion‡
M; tumor has invaded the lamina propria
49
0.81
SM; tumor has invaded the submucosa
614SS; tumor has invaded the subserosa		
01
Lymph node metastasis
Absent		10
23
0.99
Present		
0
1
Stage
1a		
10
22
0.99
1b		
0
2
Distance of preserved pylorus(cm)
3.9 ± 0.57
2.9 ± 1.2
0.018
* When the elevated lesion had a depressed area, we classified it as the depressed type.
† Differentiated, papillary or tubular adenocarcinoma; undifferentiated, poorly differentiated or mucinous adenocarcinoma, or signet-ring cell carcinoma.
CPPG, conventional pylorus-preserving gastrectomy; LAPPG, laparoscopy-assisted pylorus-preserving gastrectomy.

dissected (station 4sb). Then, the right side of thegreater omentum is dissected from the transverse
colon and the anterior sheet of the transverse mesocolon. The origin of the right gastroepiploicvein is then divided, and the right gastroepiploicartery is dissected (station 6). The infrapyloric
artery is preserved in this step to maintain the
blood supply to the remaining pyloric cuff. The
right gastric artery and vein are also preserved
up to the first branch of the stomach wall for thepreservation of the pyloric branch of the vagal
nerve without station 5 lymph node dissection.
The pedicle of gastropancreatic ligament is thencarefully lifted up, and the pancreatic capsule
is dissected with the LCS for LAPPG at the suprapancreatic border toward the pancreatic tail.
These steps expose the splenic artery and its root
as a starting point of the station 9 lymph nodedissection. The common hepatic artery is thenexposed toward the root of the left gastric artery.
During these procedures, the left gastric vein is
confirmed and divided. Lymph node dissectionof station 8a is continued on to lymph node dissection of station 9 around the celiac axis. The
left gastric artery is resected by clip, accompanied
by lymph node dissection of station 7. The cardiac lymph node (station 1) and the lymph nodes
along the lesser curvature of the stomach (station
3) are then removed. The celiac branch of the vagus nerve is not preserved in this operation. The
lymph node dissection is classified D0 becauseof the absence of station 5 lymph node dissection according to the Japanese Classification of
Gastric Cancer. For LAPPG, a 5-cm middleline
incision is made and the location of the tumor is
comfirmed by the palpation of the preopearive
clipping. The diatal and proximal portion of thestomach is then resected and gastrogastrostomy
27

H. Saito et al.

Table 2. Operative data
Variable			

Operation time(min)
Bleeding volume(mL)
Number of dissected lymph nodes
Lymph nodes retrieved for each station
Station 1		
Station 3		
Station 4sb		
Station 4d		
Station 6		
Station 7		
Station 8a		
Station 9		

LAPPG		

362.8 ± 49.6
127.5 ± 91.2
26.3 ± 9.5
4.3 ± 2.3
3.2 ± 3.1
1.0 ± 0.94
7.2 ± 5.6
3.7 ± 4.3
2.9 ± 1.7
3.1 ± 2.2
1.1 ± 1.2

CPPG			 P value
221.9 ± 50.0
167.9 ±149.9
21.3 ± 10.8

0.04
0.44
0.21

2.0 ±
6.7 ±
1.6 ±
6.7 ±
3.3 ±
2.3 ±
3.0 ±
2.0 ±

0.076
0.069
0.34
0.78
0.76
0.49
0.92
0.45

0.82
5.5
1.7
4.8
3.4
2.3
1.4
1.5

CPPG, conventional pylorus-preserving gastrectomy; LAPPG, laparoscopy-assisted pylorus-preserving gastrectomy.

LAPPG (127.5 ± 91.2 mL) was not significantly
different from that with CPPG (167.9 ± 149.9 mL;
P = 0.44) (Table 2). Total number of resected
lymph nodes was 26.3 ± 9.5 and 21.3 ± 10.8 with
LAPPG and CPPG, respectively, and there wasno statistically significant difference (Table 2).
Furthermore, number of dissected lymph nodes ineach lymph node station was similar between the
2 groups, with no significant differences (Table2). These results demonstrated that the quality oflymph node dissection with LAPPG was satisfactory compared with that with CPPG.
With regard to postoperative outcomes (Table3), C-reactive protein in serum on postoperative
day 1 was significantly lower in the LAPPG thanin the CPPG group (5.3 ± 1.7 mg/dL versus 7.8 ±3.6 mg/dL; P = 0.049). The requirement for analgesia (diclofenac sodium or pentazocine) in hospital after surgery was more frequent in the CPPG
than in the LAPPG group (3.7 ± 2.0 versus 2.2

was performed extracorporeally using Gambee’s
handsewn methods through a small incision, withthe wound protected.
Statistical analysis
Association among factors was evaluated by thechi-squared test and the significance of differences among means was determined by the MannWhitney U test. The accepted level of significance was P < 0.05. Stat View software (Abacus
Concepts, Berkeley, CA) was used for all statistical analyses.

Results
Operation time for LAPPG (362.8 ± 49.6 min)was significantly longer than that for CPPG (221.9± 50.0 min; P = 0.04). Estimated blood loss with

Table 3. Postoperative data					Variable

LAPPG

CPPG

P value

C-reactive protein(mg/dL)
Total frequency of analgesic drug administration in hospital (times)
Time until start of flatus(day)
Postoperative hospital stay(day)

5.3 ± 1.7
2.2 ± 1.7
1.9 ± 0.9
12.0 ± 4.0

7.8 ± 3.6
3.7 ± 2.0
3.1 ± 0.9
23.0 ± 10.7

0.049
0.04
0.00060.0036

CPPG, conventional pylorus-preserving gastrectomy; LAPPG, laparoscopy-assisted pylorus-preserving gastrectomy.

28

LAPPG in early gastric cancer± 1.7; P = 0.04). Time to first flatus was shorterin the LAPPG than in the CPPG group (1.9 ± 0.9
days versus 3.1 ± 0.9 days; P = 0.0006). Postoperative hospital stay was significantly shorter inthe LAPPG than in the CPPG group (12.0 ± 4.0
days versus 23.0 ± 10.7 days; P = 0.0036).
With regard to postoperative complications,no patient had anastomotic or pancreatic-juice
leakage. On the other hand, stasis was observed
more frequently in the CPPG (8 patients, 33.3%)
than in the LAPPG (1 patient, 10%) group. No
patients died of recurrent gastric cancer, and all
patients remain disease-free.

dissected lymph nodes was similar between the 2groups, with no significant differences. Moreover,number of dissected lymph nodes in each lymph
node station was similar between the 2 groups,
with no significant differences. This result demonstrated that the quality of lymph node dissection in LAPPG was satisfactory compared withthat in CPPG.
Recovery of bowel movements after operation occurred at an earlier stage in the LAPPG
group, as measured by first flatus and oral intake.
This was an important feature, as reduction in the
period of postoperative intestinal paralysis is oneof the most valuable features of laparoscopic surgery, and early recovery of bowel function can result in early resumption of food intake and earlier
discharge from hospital (Mochiki et al., 2002).
Less administration of analgesic drugs was required for LAPPG patients, and this might havecontributed to the greater activity of these patients
postoperatively. As in the previous studies (Adachi
et al., 2000; Mochiki et al., 2002; Migoh et al.,2003), the hospital stay was shorter in the LAPPG
than in the CPPG group in the present study.
With regard to the postoperative complications, there was no difference, except for stasis,
between the 2 groups. Postoperative gastric stasis due to aberrant pylorus function is the mostcommon complication, occurring in 23 to 40% of
patients after PPG (Kodama et al., 1995; Tomita
et al., 2003). In this regard, Nunobe et al. (2007)
have demonstrated that preservation of the vagus
nerve and infrapyloric artery induces less stasis.
The length of the antral segment and the volumeof the remnant stomach are also important factors
for gastric stasis after PPG. Nakane et al. (2002)
have shown that longer length of the retained
antrum is associated with less postprandial symptoms, improved food intake, earlier recovery ofbody weight and gastric emptying. In the present
study, infrapyloric artery and the pyloric branchof the vagal nerve were preserved in the LAPPG
group. Moreover, preserved length of the antral
segment was longer in the LAPPG than in the
CPPG group. With regard to length of the antral

Discussion
Many studies have compared the surgical featuresof LADG and conventional distal gastrectomy.
Some have reported longer operation times for
LADG than for conventional distal gastrectomy(Kitano et al., 2002; Mochiki et al., 2002). We
also found that operation times for LAPPG weresignificantly longer than those for CPPG in thepresent study. In this regard, however, Adachi etal. (2000) have reported that LADG performed byskilled and experienced surgeons takes no moretime than conventional distal gastrectomy. Therefore, it might be possible to shorten the operation
time through experience. On the other hand,
intraoperative blood loss tended to be less in
LAPPG patients than in CPPG patients, as reported by others, probably due to the effect of magnification by laparoscopy (Adachi et al., 2000; Yanoet al., 2001; Kitano et al., 2002; Mochiki et al.,
2002; Migoh et al., 2003).
It has been demonstrated that lymph nodemetastasis and lymph node dissection weredeemed as the most important prognostic factors
in patients with resected gastric cancer (Siewert
et al., 1998). Therefore, lymph node dissectionis the most important procedure in surgery for
gastric cancer. We determined the number oflymph nodes to be resected to evaluate the qualityof lymph node dissection. The total number of29

H. Saito et al.

segment, we have recently preserved the antral
segment as long as possible in both CPPG and
LAPPG patients. The difference in the preserved
length of the antral segment we observed in thepresent study was simply due to the difference inperiod of operation. Longer length of the pyloric
cuff and preservation of the infrapyloric artery andthe pyloric branch of the vagal nerve might haveresulted in the low frequency of gastric stasis.
In conclusion, our results demonstrated that
LAPPG was a safe and useful operation for earlygastric cancer located in the middle third of the stomach. Additional randomized control studies should
be undertaken to analyze long-term outcomes.

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Received March 26, 2008; accepted May 14, 2008
Correspondence: Hiroaki Saito, MD

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