ORIGINAL ARTICLE

Laparoscopic resection for gastrointestinalstromal tumors in the stomach

Yoshihiro Kakeji • Tomonori Nakanoko • Rintaro Yoshida • Kojiro Eto •

Ryuichi Kumashiro • Keisuke Ikeda • Akinori Egashira • Hiroshi Saeki •

Eiji Oki • Masaru Morita • Tetsuo Ikeda • Yoshihiko Maehara

Received: 28 April 2011 / Accepted: 16 May 2011 / Published online: 30 November 2011

� Springer 2011

Abstract

Purpose Gastrointestinal stromal tumors (GISTs) should

be surgically resected, even those smaller than 5 cm in

size, which is the threshold of clinical malignancy for

submucosal tumors (SMTs) in the gastrointestinal tract.

This study reviewed the use of laparoscopic surgery for

gastric partial resection of GISTs or SMTs that were sus-

pected to be GISTs.

Methods Eighteen patients underwent laparoscopic par-

tial resection of the stomach for GISTs or SMTs. The

tumor location was confirmed by intraluminal endoscopy.

One-half of the circumference around the tumor was dis-

sected, and the tumor was turned toward the abdominal

cavity. The nonresected part of the tumor and the edge of

the incision line was lifted up using forceps, and the inci-

sion line was closed using laparoscopic stapling devices.

Results Two cases were diagnosed as GIST by endo-

scopic biopsy. Six patients underwent endoscopic ultra-

sound-guided fine-needle aspiration biopsy (EUS-FNAB)

examinations, which diagnosed five GISTs. There were 18

tumors smaller than 5 cm, including 10 GISTs, 4 leio-

myomas, 3 schwannomas, and one heterotopic pancreas.

Conclusions Endoscopic ultrasound-guided FNAB is

recommended for definite preoperative diagnosis of hist-

opathologically unknown SMTs to determine the indica-

tions for surgery. The laparoscopic approach with the

assistance of endoscopy is useful for improving the

curability, with minimal invasiveness for the partial

resection of GISTs.

Keywords Gastrointestinal stromal tumor � Submucosal

tumor � Laparoscopic resection � Endoscopic ultrasound-

guided fine-needle aspiration biopsy

Introduction

Gastrointestinal stromal tumors (GISTs) represent a rela-

tively rare type of nonepithelial, mesenchymal neoplasms

originating in the gastrointestinal tract. Nevertheless,

GISTs are the most common mesenchymal tumors in the

gastrointestinal tract [1, 2], and can occur throughout this

tract. The most common location is the stomach,

accounting for 60–70% of all GISTs [3].

Surgery is the standard treatment for histologically veri-

fied primary GIST [4, 5]. The principles of surgical treatment

for primary resectable GIST are complete resection with

macroscopically negative margins [6]. A simple wedge

resection, when feasible, is the recommended surgical

approach, because GIST rarely metastasizes to lymph nodes

in adults. Gastric GIST resection is, therefore, particularly

amenable to minimally invasive techniques, and an

increasing number of laparoscopic resections have been

reported, demonstrating the feasibility and safety of this

approach [7–11]. The Japanese Clinical Practice Guideline

for GIST tailored for Japanese patients [12] indicated that

‘‘laparoscopic resection of gastric or intestinal GISTs

smaller than 5 cm in size appears to be safe when performed

by a skillful surgeon who is thoroughly familiar with the

neoplastic characteristics of GIST.’’

Laparoscopic surgery has been applied at our institution

for suspected GISTs measuring from 2 to 5 cm in diameter

Y. Kakeji (&) � T. Nakanoko � R. Yoshida � K. Eto �R. Kumashiro � K. Ikeda � A. Egashira � H. Saeki � E. Oki �M. Morita � T. Ikeda � Y. Maehara

Department of Surgery and Science, Graduate School of

Medical Sciences, Kyushu University, 3-1-1 Maidashi,

Higashi-ku, Fukuoka 812-8582, Japan

e-mail: kakeji@surg2.med.kyushu-u.ac.jp

123

Surg Today (2012) 42:554–558

DOI 10.1007/s00595-011-0072-x

and located almost anywhere in the stomach. This report

reviews the recent cases of GISTs or SMTs that were

suspected to be GISTs, and introduces a laparoscopic sur-

gery technique that secures minimal surgical margins.

Patients and methods

Patients

Eighteen patients who underwent laparoscopic gastric

resections of suspected GISTs or growing submucosal

malignancies in the Department of Surgery and Science,

Kyushu University Hospital, Fukuoka, Japan from 2005 to

2010 were prospectively investigated in the study. The

indications for laparoscopic management of gastric sub-

mucosal tumors were: a tumor between 2 and 5 cm, a rapid

increase in tumor size since any previous examination, or

the presence of symptoms. Surgical resection of the tumor

was recommended for patients with rapid growth of the

neoplasm, which strongly suggests malignant potential.

The diagnosis of GIST is an indication for surgical resec-

tion, regardless of the tumor size.

Preoperative evaluation

All patients underwent a preoperative upper gastrointesti-

nal series, endoscopy, endoscopic ultrasonography (EUS),

and computed tomography (CT). Six patients underwent an

EUS-guided fine-needle aspiration biopsy (EUS-FNAB)

examination. Lesions in which the immunohistochemical

staining was positive for the c-kit gene product/CD117

antigen were diagnosed to have a GIST [13, 14].

Laparoscopic surgical technique

Laparoscopic and intraluminal endoscopic assistance was

used for all cases, and the surgical procedures were tailored

according to tumor location. The patient was placed under

general anesthesia in the supine position. The first 12-mm

port was placed into the inferior umbilical lesion using an

open technique. Carbon dioxide was insufflated through

this port with a pressure setting of 10 mmHg. A 30� lap-

aroscope was introduced through the umbilical port and

diagnostic laparoscopy was performed. Four additional

ports (three 5-mm ports and one 12-mm port) were inserted

into the left upper, left lower, right upper, and right lower

quadrants, respectively, under the guidance of a

laparoscope.

The jejunum was clamped using clamp forceps 5 cm from

the anal side of the Treitz ligament, and the tumor location

was confirmed by intraluminal endoscopy. The endoscopist

visualized the lesion under direct diaphanoscopy for the

laparoscopic surgeon. The stomach wall was sometimes

maneuvered from the mucosal side using biopsy forceps.

Most lesions were removed by exogastric wedge

resection using an endoscopic linear stapler. Gastric vessels

or the omentum in the excision area around the tumor were

divided, if necessary, using ultrasonic coagulating shears.

The active blade of the ultrasonic coagulating shears was

inserted through the whole layer of the gastric wall,

maintaining a safe margin from the tumor. One-half of the

circumference of the tumor was dissected, and the tumor

was turned over toward the abdominal cavity (Fig. 1). The

nonresected part of the tumor and the edge of the incision

line were lifted up using supporting strings and/or forceps,

and the incision line was closed with a laparoscopic sta-

pling device. Ultrasonic coagulating shears were used to

minimize the resection area, except for the exoluminal type

resections.

Posterior gastric wall lesions were commonly approa-

ched via the lesser sac through the gastrocolic ligament.

The greater curvature was elevated and rotated cephalad to

expose the posterior surface of the stomach. The lesion was

then resected with a technique similar to that described for

anterior lesions.

Tumors near the esophagogastric junction or pylorus

that left a defect in the gastric wall were closed using a

laparoscopic hand-suturing technique. The endoscopist

checked the passage and closure following the resection by

careful inspection and management of air insufflation.

Results

The preoperative evaluation of 18 patients with gastric

submucosal tumors is shown in Fig. 2. Two cases were

diagnosed with GIST by endoscopic biopsy. Endoscopic

ultrasound-guided FNAB diagnosed five GISTs, but could

not definitively diagnose one case, in which the final

pathological diagnosis was schwannoma. A GIST was

therefore diagnosed preoperatively in seven cases. Surgery

was indicated for the remaining 11 patients when images,

such as EUS or CT, showed a rapid increase in tumor size

since the previous examination.

The pathological diagnoses of the resected submucosal

tumors are shown in Fig. 3. There were 18 tumors smaller

than 5 cm, including 10 GISTs, 4 leiomyomas, 3 schwan-

nomas, and one heterotopic pancreas. Risk classification,

based on the tumor size and mitotic count under a high-

power field [15], revealed only one intermediate risk case

in the 11 GISTs smaller than 5 cm.

Table 1 lists the details of all 18 cases. Cases 15 and 16

were diagnosed to be leiomyomas located near the esoph-

agogastric junction, and direct hand-suturing was added to

close the defect in the gastric wall through a small incision

Surg Today (2012) 42:554–558 555

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in the upper abdominal wall. The average duration of the

operation was 128 ± 36 min and the estimated blood loss

was 25 ± 40 ml. The postoperative course was uneventful

except for one case with bleeding and one with reflux

esophagitis. Postoperative bleeding from the drainage tube

was observed in the recovery room 2 h after the first

operation in the patients with bleeding. Reoperation was

performed laparoscopically, and the bleeding point in an

arteriole was recognized in the resection line at the lesser

curvature. Hemostasis was performed with clipping. The

average time until the start of oral intake was

5.2 ± 3.1 days, and the average postoperative hospital stay

was 9.8 ± 3.6 days. Patients were followed for 1403

(range 311–2218) days postoperatively. No recurrence has

been experienced in any of these cases.

Discussion

Submucosal tumors are mesenchymal tumors and, as such,

they may have very diverse origins [16]. Submucosal

tumors were originally divided into those of muscular or

neural derivation. It is extremely important to accurately

distinguish potentially malignant GIST from benign SMT.

Fig. 1 Laparoscopic dissection of submucosal tumors. a The whole

layer of the stomach wall was dissected along the incision line using

ultrasonic coagulating shears. b Dissecting one-half of the

circumference, the tumor was turned over toward the abdominal cavity.

The incision line was closed with a laparoscopic stapling device.

c These procedures can dissect the tumor with minimal extra tissue area

EndoscopicBiopsyn

Imaging EUS-guided

n=211%

EUS, CTn=1161%

Fine NeedleAspiration Biopsy

n=528%

Fig. 2 Preoperative diagnosis of the gastric submucosal tumors.

Three cases were diagnosed as gastrointestinal stromal tumor by

endoscopic biopsy, and nine cases were diagnosed by endoscopic

ultrasound (EUS)-guided fine-needle aspiration biopsy. CT computed

tomography

14

16 Heterotopic pancreas

10

12

Leiomyoma

ch

6

8

GIST

2

4GIST

GIST

Leiomyoma

0< 2 2 5 cm

GIST

Tumor diameter

S hwannoma

Fig. 3 Pathological diagnoses of the resected submucosal tumors in

relation to the tumor diameter. GIST gastrointestinal stromal tumor

556 Surg Today (2012) 42:554–558

123

Some malignant findings in diagnostic images are consid-

ered to be sufficient indications for surgery [12], such as

ulceration, irregular margins, or rapid growth in endo-

scopic examinations; necrosis, hemorrhage, irregularity of

margins, or abundant blood flow on CT; or heterogeneous

parenchyma, irregular margins, and enlarged regional

lymph nodes on EUS. An accurate differential diagnosis

requires immunohistochemistry of a biopsied specimen.

Endoscopic ultrasound-guided fine-needle aspiration

(EUS-FNA) is a good method for obtaining cytological

samples [17, 18]. The sensitivity of cytological samples

achieved through EUS-FNA is 88–91%, and the specificity

is close to 100% for the diagnosis of malignant lesions

confirmed by surgical findings or long-term clinical follow-

up [19]. Use of EUS-FNA is therefore strongly recom-

mended to distinguish GIST from benign tumors that do

not require surgery.

Successful laparoscopic wedge resection has been

reported for 2–5-cm gastric GISTs or SMTs suspected of

being GISTs [9, 10]. Laparoscopic and endoscopic coop-

erative surgery for gastric wedge resection has also been

introduced [20, 21], which is applicable for SMT resection

independent of the tumor location and size. Detecting the

precise tumor location endoluminally by endoscopy and

exogastrically by laparoscopy facilitates the resection of

the SMT with a sufficient and minimal margin of normal

Table 1 Cases with submucosal tumors smaller than 5 cm that were resected laparoscopically

Case Age

(years)

Sex Tumor

diameter

(cm)

Pathological

diagnosis

Gross

appearance

Location

of tumor

Operation

time

(min)

Blood

loss

(g)

Oral

intake

(days)

Postop.

hospital

stay (days)

Postop.

complications

1 57 F 1.5 GIST Endoluminal Upper,

ant

66 0 6 8

2 56 M 1.5 GIST Exogastric Middle,

ant

88 0 4 8

3 66 M 2.1 GIST Exogastric Lower,

ant

126 25 3 10

4 83 F 2.5 GIST Endoluminal Middle,

less

164 20 4 7

5 60 M 2.5 GIST Endoluminal Upper,

post

106 5 4 8 Bleeding

6 73 M 3.7 GIST Endoluminal Upper,

gre

83 0 3 8

7 49 F 4.0 GIST Endoluminal Lower,

less

189 0 5 8

8 58 M 4.2 GIST Endoluminal Middle,

gre

99 0 2 7

9 72 F 5.0 GIST Endoluminal Middle,

less

178 66 4 7

10 55 M 5.0 GIST Endoluminal Middle,

post

145 0 5 9

11 52 F 3.0 Schwannoma Exogastric Upper,

ant

121 13 5 8

12 28 F 3.3 Schwannoma Endoluminal Middle,

gre

142 138 4 9

13 42 M 4.5 Schwannoma Exogastric Lower,

ant

141 103 7 10

14 31 F 1.4 Leiomyoma Endoluminal Middle,

less

131 0 3 6

15 38 F 3.0 Leiomyoma Endoluminal Upper,

gre

491 276 9 17 Reflux

esophagitis

16 35 F 3.8 Leiomyoma Endoluminal Upper,

post

330 400 4 16

17 37 F 5.0 Leiomyoma Endoluminal Upper,

less

89 12 6 11

18 39 F 3.8 Heterotopic

pancreas

Exogastric Middle,

less

176 18 16 19

GIST gastrointestinal stromal tumor, ant anterior wall, post posterior wall, less lesser curvature, gre greater curvature

Surg Today (2012) 42:554–558 557

123

tissue. Although the methods of Hiki et al. [21]. include

endoscopic submucosal dissection via intraluminal endos-

copy, the current series highlights the advantages of dis-

secting one-half of the circumference around the tumor

exogastrically using ultrasonic coagulating shears. This

method does not require an expert endoscopist in the

operating room. Endoscopy is used only to observe the

SMT endoluminally and to prevent stenosis in the esoph-

agogastric junction or in the pylorus. The endoscope

inserted into the stomach can maintain the passage of the

lumen.

The ongoing advances in laparoscopic techniques have

allowed almost all GISTs or SMTs \5 cm in size to be

resected laparoscopically. Laparoscopic-assisted surgery

may also be recommended because of its safety and shorter

operation time. By contrast, open surgery may be recom-

mended if tumors have abundant blood flow and high

vascularity, if they are fragile, or if they appear to be high

grade [12]. A skillful surgeon who is thoroughly familiar

with the neoplastic characteristics of GIST should perform

the operation. The tumor itself should not be held with

forceps to avoid the potential for contamination. No

recurrence has been observed in the current series since

2005. In the cases of high to intermediate risk, the potential

benefits and risks of adjuvant chemotherapy should be

explained to the patient.

The developments in the diagnosis and laparoscopic

techniques have improved the surgical treatment for GISTs

and SMTs. Gastrointestinal stromal tumors can be safely

resected by laparoscopy with a sufficient margin and

minimal deformity of the stomach.

Conflict of interest Yoshihiro Kakeji and co-authors have no

conflict of interest.

References

1. Nishida T, Hirota S. Biological and clinical review of stromal

tumors in the gastrointestinal tract. Histol Histopathol.

2000;15:1293–301.

2. Rubin BP, Heinrich MC, Corless CL. Gastrointestinal stromal

tumour. Lancet. 2007;369:1731–41.

3. Miettinen M, Lasota J. Gastrointestinal stromal tumors—defini-

tion, clinical, histological, immunohistochemical, and molecular

genetic features and differential diagnosis. Virchows Arch.

2001;438:1–12.

4. Demetri GD, Benjamin RS, Blanke CD, Blay JY, Casali P, Choi

H, et al. NCCN Task Force report: management of patients with

gastrointestinal stromal tumor (GIST)–update of the NCCN

clinical practice guidelines. J Natl Compr Canc Netw. 2007;5

suppl 2:S1–29 (quiz S30).

5. Blay JY, Bonvalot S, Casali P, Choi H, Debiec-Richter M, Dei

Tos AP, et al. Consensus meeting for the management of gas-

trointestinal stromal tumors. Report of the GIST Consensus

Conference of 20–21 March 2004, under the auspices of ESMO.

Ann Oncol. 2005;16:566–78.

6. DeMatteo RP, Lewis JJ, Leung D, Mudan SS, Woodruff JM,

Brennan MF. Two hundred gastrointestinal stromal tumors:

recurrence patterns and prognostic factors for survival. Ann Surg.

2000;231:51–8.

7. Novitsky YW, Kercher KW, Sing RF, Heniford BT. Long-term

outcomes of laparoscopic resection of gastric gastrointestinal

stromal tumors. Ann Surg. 2006;243:738–45. discussion 745–7.

8. Sexton JA, Pierce RA, Halpin VJ, Eagon JC, Hawkins WG,

Linehan DC, et al. Laparoscopic gastric resection for gastroin-

testinal stromal tumors. Surg Endosc. 2008;22:2583–7.

9. Otani Y, Furukawa T, Yoshida M, Saikawa Y, Wada N, Ueda M,

et al. Operative indications for relatively small (2–5 cm) gas-

trointestinal stromal tumor of the stomach based on analysis of 60

operated cases. Surgery. 2006;139:484–92.

10. Sasaki A, Koeda K, Obuchi T, Nakajima J, Nishizuka S, Tera-

shima M, et al. Tailored laparoscopic resection for suspected

gastric gastrointestinal stromal tumors. Surgery. 2010;147:

516–20.

11. Karakousis GC, Singer S, Zheng J, Gonen M, Coit D, Dematteo

RP, et al. Laparoscopic versus open gastric resections for primary

gastrointestinal stromal tumors (GISTs): a size-matched com-

parison. Ann Surg Oncol. 2011;18:1599–605.

12. Nishida T, Hirota S, Yanagisawa A, Sugino Y, Minami M,

Yamamura Y, et al. Clinical practice guidelines for gastrointes-

tinal stromal tumor (GIST) in Japan: English version. Int J Clin

Oncol. 2008;13:416–30.

13. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T,

Ishiguro S, et al. Gain-of-function mutations of c-kit in human

gastrointestinal stromal tumors. Science. 1998;279:577–80.

14. Miettinen M, Sarlomo-Rikala M, Lasota J. Gastrointestinal stro-

mal tumors: recent advances in understanding of their biology.

Hum Pathol. 1999;30:1213–20.

15. Fletcher CD, Berman JJ, Corless C, Gorstein F, Lasota J, Longley

BJ, et al. Diagnosis of gastrointestinal stromal tumors: a con-

sensus approach. Hum Pathol. 2002;33:459–65.

16. Ponsaing LG, Kiss K, Hansen MB. Classification of submucosal

tumors in the gastrointestinal tract. World J Gastroenterol.

2007;13:3311–5.

17. Chang KJ, Katz KD, Durbin TE, Erickson RA, Butler JA, Lin F,

et al. Endoscopic ultrasound-guided fine-needle aspiration. Gas-

trointest Endosc. 1994;40:694–9.

18. Ando N, Goto H, Niwa Y, Hirooka Y, Ohmiya N, Nagasaka T,

et al. The diagnosis of GI stromal tumors with EUS-guided fine

needle aspiration with immunohistochemical analysis. Gastroin-

test Endosc. 2002;55:37–43.

19. Ponsaing LG, Kiss K, Loft A, Jensen LI, Hansen MB. Diagnostic

procedures for submucosal tumors in the gastrointestinal tract.

World J Gastroenterol. 2007;13:3301–10.

20. Ludwig K, Wilhelm L, Scharlau U, Amtsberg G, Bernhardt J.

Laparoscopic-endoscopic rendezvous resection of gastric tumors.

Surg Endosc. 2002;16:1561–5.

21. Hiki N, Yamamoto Y, Fukunaga T, Yamaguchi T, Nunobe S,

Tokunaga M, et al. Laparoscopic and endoscopic cooperative

surgery for gastrointestinal stromal tumor dissection. Surg En-

dosc. 2008;22:1729–35.

558 Surg Today (2012) 42:554–558

123