Review Article
Laparoscopic-Endoscopic Cooperative Surgery for Gastric Gastrointestinal Stromal Tumors
Rong Wu and Zhen-Ling JI*
Department of General Surgery, Southeast University Medical School, China
*Corresponding author: Zhen-Ling JI, Department of General Surgery, Institute for Minimally Invasive Surgery, Zhongda Hospital, Southeast University Medical School, Nanjing, Jiangsu 210009, China
Published: 07 Dec, 2016
Cite this article as: Wu R, Zhen-Ling JI. Laparoscopic-
Endoscopic Cooperative Surgery
for Gastric Gastrointestinal Stromal
Tumors. Clin Surg. 2016; 1: 1234.
Abstract
Gastrointestinal stromal tumors (GISTs) are the most common mesenchymal tumors originating
in the gastrointestinal tract. Laparoscopic endoscopic cooperative surgery (LECS), consist of
endoscopic surgery in the form of endoscopic mucosal incision and laparoscopic surgery, is an
important advantage over conventional laparoscopic wedge resection(LWR) for local resection
of gastric gastrointestinal stromal tumors (GIST). The first LECS method was reported by Hiki
in 2008, which was named “classical LECS” to distinguish from subsequent modified methods,
for example, laparoscopic assisted endoscopic full-thickness resection (LAEFR), inverted LECS
and a combination of laparoscopic and endoscopic approaches to neoplasia with a non-exposure
technique (CLEAN-NET) and non-exposed endoscopic wall-inversion surgery (NEWS). Each of
these procedures has advantages and disadvantages. So we have reviewed these techniques, identify
the difference between them, define their indications and elaborate their characteristics. And in
conclusion, as a relative safe, feasible, and beneficial procedure, classical LECS technique, along
with subsequent modified methods substantially promote the development of surgical treatment
for gastrointestinal neoplasms especially for GISTs. Moreover, further studies such as large sample
prospective clinical trials are also required to confirm the feasibility and stability of these treatment
methods, especially with regard to safe and long-term outcomes.
Keywords: Laparoscopic-endoscopic cooperative surgery; Laparoscopic wedge resection; Gastrointestinal stromal tumors
Introduction
Gastrointestinal stromal tumors (GISTs) are the most common mesenchymal tumors
originating in the gastrointestinal tract, which usually occur in the stomach (60%) or small intestine
(30%) [1]. GISTs range in size from less than 1 cm to very large lesions measuring upwards of 35 cm.
Large tumors frequently present with hemorrhage, necrosis, and cystic degeneration. Size, mitosis,
primary site and rupture of tumor are considered the four most important risk factors for prognosis
of GISTs, which guide the selection of patients who may require adjuvant therapy [2].
Due to the high potential for malignancy of GIST, the first-line treatment of localised GISTs
is complete surgical excision of the lesion without residual tumor cells (R0) or tumor rupture, and
systematic locoregional lymph node dissection is usually unnecessary. For complete resection,
pseudocapsule should not be damaged during manipulation of the tumor and macroscopically
negative margin as well as adequate safety margin should be spared. Tumors >20 mm or growing
tumors should be surgically resected, because, if diagnosed as GIST, will imply a higher risk. The
preferred resection margin is 10-20 mm grossly. Since GISTs rarely metastasizes to local or regional
lymph nodes, lymphadenectomy is warranted only if metastasis is suspected, such as when enlarged
lymph nodes are noted.
Compared with open surgery, laparoscopic surgery has similar outcomes for GIST patients
in terms of oncologic prognosis with several advantages, such as less pain, less invasiveness,
early recovery, and better cosmetic results [2]. Some studies and consensuses have indicated that
laparoscopic surgery can only be safely performed for GISTs that are 5 cm or smaller in favorable
locations [3-4], while things were changed with the development of medical practice and technology.
Besides, laparoscopic-assisted surgery may also be recommended because of its good safety and short
operation time [3]. LWR has been used to treat GISTs for decades [5], many studies demonstrate
that LWR is feasible and safe with all the benefits of minimally invasive surgery even for GISTs
that are larger than 2 cm. However, determining the appropriate incision line is difficult from the
outside of the stomach when these lesions are intraluminal, which might result in transformation
of the stomach with consequent gastric stasis at food uptake. Besides,
it’s hard to ensure negative margins of large tumors and tumors
located at the esophagogastric junction (EGJ), near the pylorus,
or on the posterior gastric with LWR method. So laparoscopic
endoscopic rendezvous surgery has been described to determine the
appropriate incision line for local resection of the stomach [6-7], then
the formal concept of classical laparoscopic endoscopic cooperative
surgery (LECS) was first reported to treat GISTs by Hike in 2008 [8],
consisting of endoscopic surgery in the form of endoscopic mucosal
incision and laparoscopic surgery, which is an important advantage
over conventional laparoscopic wedge resection using linear staplers.
However LECS has some inherent risks suck as peritoneal infection
and cancer cell seeding due to the necessity for gastric perforation,
so many attempts have been made to improve the reliability and
feasibility of this technique.
With the development of the original LECS procedure or
“classical LECS”, a number of modified LECS procedures have been
investigated by numerous researchers, for example, laparoscopic
assisted endoscopic full thickness resection (LAEFR) [9], inverted
LECS, combination of laparoscopic and endoscopic approaches
to neoplasia with a non-exposure technique(CLEAN-NET) [10]
and non-exposed endoscopic wall inversion surgery (NEWS)
[11-12]. These techniques are advantageous because a more precise
resection area can be determined using intraluminal endoscopy, thus
minimizing the resection area. This will result in less deformity and
better surgical margins.
Here we review the application of classical and further modified
LECS techniques, identify and classify the different techniques
described, define their indications and elaborate their characteristics
(Table 1).
Table 1
Classical LECS
Laparoscopic wedge resection is safe and feasible treatment for
gastric submucosal tumors, while a major difficulty with this type of
tumor resection lies in determining the appropriate resection line. In
order to solve this problem, Hiki et al. [8] first report the classical
laparoscopic and endoscopic cooperative surgery (LECS) for gastric
wedge resection, which is applicable for submucosal tumor resection
independent of tumor location and size.
The LECS procedure combines gastrointestinal endoscopy
and laparoscopy: the lesion is located and partially dissected by
Endoscopic Submucosal Dissection (ESD) and the resection is
completed by laparoscopy.
First, the setup for laparoscopic surgery is similar with standard
LWR method, including the position of surgeons and operative ports.
Then the tumor location is confirmed by intraluminal endoscopy,
besides, the tumor location of laparoscopic image is confirmed
by maneuvered the stomach wall with biopsy forceps from the
mucosal side. Ultrasonically activated device and Ligasure are used
to manipulate blood vessels periphery of the lesion. Then endoscopic
submucosal resection around the tumor is manipulated. An Argon
plasma coagulation is used to mark the periphery of the tumor and
10% glycerin is injected into the submucosal layer, then a small
initial incision is made with a standard needle knife and the tip of
the insulation-tipped diathermic electrosurgical (IT) knife inserted
into the submucosal layer, three-fourths of the marked area was
cut circumferentially using the IT knife. An artificial perforation is
performed with the needle knife which allow the insertion of the tip
of the ultrasonically activated device, thus further seromuscular layer
is dissected along the incision line using the Ligasure vascular sealing
system. The tumor is turned over toward the abdominal cavity after
seromuscular three-fourths of the circumference around the tumor
had been dissected. At last, the tumor (non resected part) and the
edge of the incision line then was lifted up, and the closure of gastric
wall is performed by laparoscopic stapling device or a laparoscopic
hand sewn suture technique.
Many studies demonstrated the feasibility and satisfactory
outcome of LECS for GIST, including minimizes the surgical
specimen and providing a sufficient surgical margin to successfully
cure gastric GIST [13-17]. Furthermore, the classical LECS procedure
is believed not affected by tumor location or size [16,18].
However, as classical LECS needs to open the gastric wall during
the dissection, the artificial perforation might result in spillage of
gastric contents and lead to bacterial contamination of peritoneal
cavity and dissemination of peritoneal tumor cells. After all, classical
LECS is a feasible technique for the treatment of tumors including
GIST if the tumor is unable to seed elsewhere.
Laparoscopy-Assisted Endoscopic Full- Thickness Resection (LAEFR)
As LWR may lead to excessive normal tissue removal, Abe et al.
[9] proposed a concept of modified LECS technique, which known
as laparoscopy-assisted endoscopic full-thickness resection (LAEFR).
This technique is performed under the same principles of LECS
except the endoscopic full thickness resection around the tumor. The
standard LAEFR consists of four major steps: 1) a circumferential
incision as deep as the submucosal layer around the lesion by the
ESD technique; 2) endoscopic full-thickness (from the muscle layer
to the serosal layer) incision around the three-fourths or two-thirds
circumference on the submucosal incision under laparoscopic
supervision; 3) laparoscopic full-thickness incision around the
remaining one-fourth or one-third circumference from inside the
peritoneal cavity; 4) hand sewn closure of the gastric-wall defect. At
last the specimen is retrieved either per orally or protected in a plastic
bag through a port site.
The LAEFR method consist of Endoscopic full-thickness resection
(EFTR) and laparoscopic hand sewn closure of the gastric wall defect,
the combination of these 2 procedures makes the full-thickness
resection more accurate and as small as possible [19]. An increasing
number of studies have focused on this technique [20-22], specifically
Hirohito Mori et al. [23] believed that for GISTs that do not require
lymphadenectomy and can be cured by radical tumor enucleation,
LAEFR is a safe and established surgical endoscopy procedure.
However compared to classical LECS, the complicated procedure of
LAEFR may leads to longer operation time and learning curve.
Inverted LECS
As described above, LECS may leads to peritoneal infection or
cancer cell seeding due to the necessity for gastric perforation. So
in order to reduce the risk of these complications, Souya Nunobe et
al. [24] developed a new modified LECS technique named “inverted
LECS”.
The procedures of inverted LECS are identical to classical LECS
before laparoscopic seromuscular dissection and formation of
artificial perforation. To prevent contact between the tumor and the
visceral tissue, the tumor is inverted to face the intragastric cavity
using the traction of the stitch at the edge of the resected specimen,
and the resection line of the stomach is also pulled up by these stitches.
Then the tumor is resected into the gastric cavity and collected via the
per-oral route, the edge of the incision line was closed temporarily
using hand sewn sutures. At last a laparoscopic stapling device is used
to close the incision line as the conventional method of the classical
LECS procedure.
With inverted LECS procedure, the lesion is kept inside the
stomach, thus the direct contact between tumor and the perigastric
viscera is prevented effectively. However, there is still risk of gastric
content contamination and tumor cells seeding as artificial perforation
of gastric wall and instruments contact are inevitable [25,26].
Clean-Net
CLEAN-NET, which is known as a combined laparoscopic and
endoscopic approach for non-exposure full thickness gastric wall
resection, was first described by Inoue et al. [10] in 2012 to completely
prevent the risk of cancer cell dissemination. This technique preserves
the continuity of the mucosa as a barrier (a clean net) by using a
seromuscular incision. Then the mucosal tissue is pulled out toward
the outside of the stomach, thus maintains a sufficient epithelial
margin around the cancer tissue, in this way can keep a minimal
defect of stomach wall.
First, endoscopic markings are made approximately 5 mm
from the lesion margin on the mucosa with an electrocautery knife.
Then fix the mucosal layer to the seromuscular layer with full-layer
stitches using 4 stay sutures under the guidance of laparoscope and
endoscope. Next 4 stitches are pulled upward with laparoscopic
forceps, a selective seromuscular dissection along the outside of the
4 stitches is performed using an laparoscopic electrocautery knife,
and the mucosal layer maintains its continuity in this method which
prevents gastric contents from flowing out into the peritoneal cavity.
A full-layer specimen with sufficient lateral mucosal margin is cut and
taken out with a laparoscopic stapling device.
After all, CLEAN-NET allows full-layer gastric wall resection to
be completed with minimal risk of contamination of abdominal cavity
from gastric content. However, as the mucosal layer must maintains
its continuity when be pulled out toward the outside of the stomach,
then specimen size is limited to avoid mucosal laceration. Besides, the
appropriate mucosal incision might be difficult to determine for the
incision line is determined from the serosal side [26].
News
Non-exposed endoscopic wall in version surgery (NEWS) was
first performed in 2011 in an ex vivo porcine model by Osamu
Goto et al. [11]. This non-exposure technique enables full-thickness
resection of the gastric wall without transmural communication,
thus preventing tumor dissemination into the abdominal space.
Interestingly, the procedures of NEWS also resemble “inverted” kind
of CLEAN-NET to some extent.
The NEWS method can be manipulated as following steps: First,
markings of lesion are made with endoscope, then inject 0.9% normal
saline with indigo carmine into the sub mucosa around the markings.
Second, a circumferential sero-muscular incision is made from the
outside with an electrocautery knife, guided by the color of the sub
mucosal injection and intragastric navigation with the endoscope.
Third, the muscle layer is linearly sutured with the lesion inverted
into the inside. Finally, a circumferential muco-submucosal incision
is made with an electrocautery knife employed with the endoscope
and the tumor is retrieved per orally [11].
The method was originally performed for 3 lesions, including 1
anterior wall, 1 lesser curve and 1 posterior wall of the gastric body,
all lesions were resected successfully with no apparent complications
occurred such as air leakage or perforation, thereby proving NEWS
is effective as a minimally invasive, and minimal-size surgery for
gastric submucosal tumors, which also reflected by several other
studies [12,27,28]. However, as tumors are retrieved per orally, so its
application is limited by tumor size. Besides, compared to CLEANNET,
the seromuscular hand suturing and circumferential mucosal
incision process are time consuming. At last, it’s complicate to
determine proper mucosal incision, which may result in a relatively
large resection area.
Discussion
Compared with open surgery, laparoscopic surgery has similar
outcomes for GIST patients in terms of oncologic prognosis with
several advantages, such as less pain, less invasiveness, early recovery,
and better cosmetic results. Although tumors with an extra gastric
growth pattern can be easily treated using conventional laparoscopic
wedge resection, laparoscopic methods alone have some limitations
for the resection of GISTs. Laparoscopy is less efficient than open
surgery in removing small tumors and tumors located in the posterior
gastric wall and lesser curvature of the stomach. In addition, the
removal of large tumors and those located near the cardia or pylorus
can result in post-operative complications, such as stenosis or
damage to the cardia or pylorus. Furthermore, for single laparoscopic
technique, it’s difficult to determine the appropriate incision line for
intraluminal lesions from the outside of the stomach. Therefore Hike
et al proposed the concept of “Laparoscopic-endoscopic cooperative
surgery” (classical LECS) in 2008 [8], which indicates that endoscopic
support is crucial for reducing complications, such as bleeding,
stenosis or damage to the cardia or pylorus, especially for the tumors
that are located in the gastric fundus or antrum, besides, with direct
intraluminal visualization, the tumor can be totally removed with
accurate incision line. However, classical LECS procedure still has
some inherent disadvantages, for example, tumor cell seeding and
bacterial contamination of the abdominal cavity. So many attempts
have been made to improve the reliability and feasibility of this
technique.
In order to prevent excessive normal tissue removal, Abe et al.
[9] invented the LAEFR technique, which familiar to LECS but
instead of a full thickness endoscopic resection. The combination of
EFTR and laparoscopic hand sewn closure of the gastric wall defect
makes the full-thickness resection more accurate and as small as
possible. As for Inverted LECS, the lesion is kept inside the stomach,
thus the direct contact between tumor and the perigastric viscera is
prevented effectively. While these 2 techniques have some common
disadvantages, for example, inevitable artificial gastric perforation,
which may lead to abdominal contamination and tumor cell seeding,
even its morbidity is extremely low according to present studies. So
how to solve this “inevitable” problem? Thereafter, “non-exposure”
techniques have been developed to further refine LECS methods.
CLEAN-NET and NEWS, which both known as combined
laparoscopic and endoscopic approach for non-exposure full thickness
gastric wall resection, preserve the continuity of the mucosa as a
barrier and thus allow a minimal risk of contamination of abdominal
cavity from gastric content. Besides, NEWS can also achieve accurate
resection line for tumors. While for multiple reasons describe above,
both CLEAN-NET and NEWS techniques are not appropriate for
resection of tumors with big size or in difficult locations, such as close
to the EGJ or pyloric ring.
For now, all the main techniques base on LECS have some
disadvantages that prevent their further application. Thus new
attempts have been made to improve the feasibility and stability of
LECS technique and expand its application. For example, Eri Maeda
et al. [29] reported the first case of multiple gastric GISTs treated by
LECS with no intraoperative or postoperative complications, therefore
indicates that this procedure is feasible and safe as a GIST treatment
even in cases of multiple lesions. YE YAN et al. [30] reported an
innovative procedure of laparoscope combined with endoscopy for
GIST resection and cholecystectomy, which demonstrated that LECS
is feasible and would be an ideal choice for invisible abdominal scar
surgery, in particular for multi-visceral resection. Besides, LECS is
now also applied as a safe and useful procedure to other organs such
as the duodenum and colon [31-33].
Conclusion
As a relative safe, feasible, and beneficial procedure, classical LECS technique, along with subsequent modified methods substantially promote the development of surgical treatment for gastrointestinal neoplasms especially for GISTs. Moreover, further studies such as large sample prospective clinical trials are required to confirm the feasibility and stability of these treatment methods, especially with regard to safe and long-term outcomes.
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