Prospective clinical trial of traction device-assisted endoscopic submucosal dissection of large superficial colorectal tumors using the S-O clip

Prospective clinical trial of traction device-assisted endoscopic
submucosal dissection of large superficial colorectal tumors using
the S–O clip
Hideaki Ritsuno • Naoto Sakamoto • Taro Osada • Shingo P. Goto •
Takashi Murakami • Hiroya Ueyama • Hiroki Mori • Kenshi Matsumoto •
Kazuko Beppu • Tomoyoshi Shibuya • Akihito Nagahara • Tatsuo Ogihara •
Sumio Watanabe
Received: 28 January 2014 / Accepted: 20 April 2014 / Published online: 31 May 2014
Ó Springer Science+Business Media New York 2014
Abstract
Background Endoscopic submucosal dissection (ESD)
allows en bloc resection of superficial colorectal tumors
regardless of size. However, ESD is technically difficult,
hazardous, and time consuming. New devices may help
overcome these drawbacks. We focused on traction meth-
ods and designed a new traction device, the ‘‘S–O clip.’’ Its
main advantage is that it allows direct visualization of the
cutting line during submucosal dissection. Moreover, it can
be used at any location without withdrawing the endo-
scope. The purpose of this study was to evaluate the effi-
cacy and safety of traction device-assisted ESD for large
colorectal tumors using the S–O clip.
Methods Between August 2010 and December 2011,
ESD was performed in 70 patients with a superficial
colorectal tumor C20 mm in diameter in our department.
Patients were randomized into two groups: 27 cases in the
S–O clip-assisted ESD group and 23 cases in the conven-
tional ESD group. Included in the analysis were patient’s
gender and age, tumor form, size, and location, rate of en
bloc resection, procedure time, presence or absence of
intraoperative perforation or delayed bleeding, and patho-
logical findings. Subgroup analysis stratified by these fac-
tors and multivariate analyses were conducted.
Results In the S–O clip-assisted ESD group, all 27 tumors
were resected en bloc without any complications. Although
a micro perforation occurred in one patient in the
conventional ESD group, further surgical treatment was not
required. None of the other 22 cases in the conventional ESD
group experienced complications. The mean procedure time
for the S–O clip-assisted ESD group was significantly
shorter than for the conventional ESD group (37.4 ± 32.6
vs. 67.1 ± 44.1 min, p = 0.03). No significant between-
group differences were found for the other factors.
Conclusion Our results demonstrated that S–O clip-
assisted ESD is safe and fast for en bloc resection of large
superficial colorectal tumors.
Keywords S–O clip Á Traction device Á Colorectal ESD Á
Superficial colorectal tumors
Endoscopic mucosal resection (EMR) is established and
widely accepted as a minimally invasive treatment for
superficial gastrointestinal tumors [1–3]. However, it is
difficult to achieve en bloc resection for lesions C20 mm in
diameter [4]. En bloc resection is considered the standard
criterion for curative EMR because multifragmental
resection does not enable sufficient histologic evaluation
and the local recurrence rate after multifragmental resec-
tion was reported to be significantly higher than that after
en bloc resection [5–10].
Endoscopic submucosal dissection (ESD) is a recently
developed technique that allows en bloc resection of large
gastrointestinal neoplasms [5–8] and is gaining acceptance
for colorectal tumors. However, it is not widely used to
treat the colorectum because of its degree of technical
difficulty and risk of complications, such as perforation [9–
11]. To overcome these negative factors, refinements in
ESD techniques and perhaps new devices are necessary.
The performance of ESD would be easy if the submu-
cosal layer could be directly visualized after the initial
mucosal cut. Countertraction on the lesion could possibly
H. Ritsuno Á N. Sakamoto (&) Á T. Osada Á
S. P. Goto Á T. Murakami Á H. Ueyama Á H. Mori Á
K. Matsumoto Á K. Beppu Á T. Shibuya Á A. Nagahara Á
T. Ogihara Á S. Watanabe
Department of Gastroenterology, Juntendo University School of
Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan
e-mail: sakamoto@juntendo.ac.jp
123
Surg Endosc (2014) 28:3143–3149
DOI 10.1007/s00464-014-3572-0
and Other Interventional Techniques

facilitate accurate visualization and easier dissection.
Several techniques involving traction on the lesions have
been reported to be effective in performing ESDs for large
early gastric and colorectal cancers [12–17]. Although
these methods are effective in enabling good visualization
of the cutting line, traction-assisted methods are not widely
employed to date because some limitations still exist.
Therefore we designed a new traction device, the ‘‘S–O
clip,’’ for ESDs. The S–O clip-assisted ESD has several
advantages including its ease of use and that it can be used
at any location without withdrawing the endoscope. In
addition, the S–O clip is independent; thus its movement is
not limited by the colonoscope [18, 19]. Also, this tech-
nique does not require any additional extracorporeal sys-
tem or an additional endoscope [16, 17]. We previously
reported cases of large superficial colorectal tumors suc-
cessfully resected by ESD using the S–O clip [18, 19]. The
purpose of this study was to evaluate the efficacy and
safety of traction device-assisted ESD for large colorectal
tumors using the S–O clip.
Patients and methods
Between August 2010 and December 2011, ESD was
performed for 70 cases of superficial colorectal tumor, the
so-called laterally spreading tumor (LST) C20 mm in
diameter. Sixty-four patients gave written informed con-
sent and were eligible to participate in this research on the
use of the device. Exclusion criteria were preoperative
evidence of deep submucosal invasion as assessed by
colonoscopy, a recurrent lesion after EMR or the for single
balloon overtube-guided ESD. This study was approved by
the Institutional Review Board of the Juntendo University.
Patients presenting for ESD were randomized into two
groups using opaque envelopes; there were 27 cases in
the S–O clip-assisted ESD group (Group A) and 23 cases
in the conventional ESD group (Group B) (Fig. 1). In
Group A patients, the S–O clip could be removed if it
was not beneficial to the procedure or interfered with the
procedure. In Group B, conversion to the use of the S–O
clip for safety when removal of the lesion was technically
difficult due to poor visualization or if after a circum-
ferential incision is made an unfavorable situation does
not change after 5 min.
Included in the analysis were patient’s gender and age,
tumor form, size, and location, rate of en bloc resection,
procedure time, conversion rate, presence or absence of
intraoperative perforation, delayed bleeding and patholog-
ical findings. Furthermore, the recurrence rate was assessed
by a follow-up colonoscopy. Subgroup analysis stratified
by these factors and multivariate analyses were conducted.
Procedure time was measured from the submucosal injec-
tion of a solution to elevate the lesion till complete removal
of the tumor, including retrieval of the S–O clip.
Trial registration
UMIN-CTR UMIN 000008115
Design of the S–O clip
We have previously reported two types of S–O clip: a
rubber strip type and a spring type [18, 19]. In this study,
we used the spring type. This type consists of a metallic
clip (Zeoclip: Zeon Medical Co., Ltd., Tokyo, Japan)
attached to the end of a spring 5-mm long and 1.8 mm
wide, which is then connected on its other end to a single
nylon loop (Fig. 2). The S–O clip can be passed through
the working channel of a conventional colonoscope
(Fig. 3). The length of the spring is not altered by a 1 g
force, but it extends approximately tenfold at 20 g. The
Fig. 1 Trial profile
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123

device can pull up a lesion at any location without with-
drawing the endoscope (Figs. 4, 5).
Endoscopic procedure
All procedures were performed by a single colonoscopist
(N.S.) who has performed more than 1,500 colonoscopies
annually. Conscious sedation was induced with intravenous
midazolam (2–5 mg) and pethidine (35 mg), and hyoscine
butylbromide (5–40 mg) or glucagon 1 USP (1–2 vials)
was added to reduce colonic spasm. All lesions were
properly cleansed and examined thoroughly using high-
magnification colonoscopy (CF-Q240ZI, CF-H260AZI,
CF-FH260AZI, or PCF-Q260AZI; Olympus Optical Co.,
Ltd., Tokyo, Japan) preceding the resection. To predict the
depth of invasion and exclude non-resectable lesions, pit
pattern analysis based on Kudo’s classification [20] and the
classification reported by Sano [21] for narrow-band
imaging (Olympus Optical Co., Ltd.) were employed. For
the resection procedure itself, the endoscope was usually
switched to a more maneuverable endoscope with a for-
ward-directed water spray system, that is, the PCF-
Q260AZI or PCF-Q260JI (Olympus Optical Co., Ltd.).
Firstly, the lesion was elevated creating a submucosal
cushion by injecting a solution prepared with normal saline
solution, epinephrine (1:10,000), sterile indigo carmine,
and Mucoup (Johnson & Johnson, Tokyo, Japan or Sei-
kagaku Corporation, Tokyo, Japan). After making an
incision around the lesion with a Flush knife-BT 2.0
(Fujifilm Inc., Tokyo, Japan), submucosal dissection was
performed using the same device until complete removal.
With S–O clip-assisted ESD (Group A), the initial steps
of the procedure were similar to those of conventional
ESD. After separating the tumor from the surrounding
normal mucosa, the S–O clip was attached to the proximal
edge of the lesion. Then, a regular clip was used to hook
the nylon loop of the S–O clip that was attached to the
lesion and fasten the nylon loop to the colonic wall
opposite of the lesion.
The traction applied by the device on the edge of the
lesion allowed good visualization of the cutting line of the
submucosal layer, resulting in a safe and easier dissection
(Figs. 3, 4). After complete dissection, the S–O clip was
detached from the colonic wall and extracted together with
the specimen. The endoscope was not withdrawn during
the entire procedure.
An electrosurgical unit, VIO300D (Erbe Elektromedi-
zin, Tubingen, Germany) at 40 W Effect 2 Endocut, and
carbon dioxide (CO2) for insufflation were used in all
cases.
Statistical analyses
Analysis was made according to intention-to-treat, i.e.,
patients in whom the S–O clip was removed remained in
Group A and patients who had intraoperative conversion to
the use of the S–O clip remained in Group B. The rela-
tionships between the groups were evaluated by the v2
test
or Fisher’s exact test for categorical data (form, location,
gender, and pathological finding) and the Student’s t test
for numerical data (age, procedure time), as appropriate. In
the multivariate analysis, procedure time (median time of
all cases) was analyzed with logistic regression analysis.
Fig. 2 Spring S–O clip The spring S–O clip consists of a spring
5-mm long and 1.8 mm wide with an attached metal clip at one end
and a nylon loop at the other. The length of the spring, which is not
altered by a 1 g force, extends approximately tenfold at 20 g
Fig. 3 The S–O clip can be passed through the working channel of
the endoscope
Fig. 4 Illustration depicting S–O clip-assisted ESD
Surg Endosc (2014) 28:3143–3149 3145
123

A p value 0.05 was considered statistically significant.
Statistical analysis was performed using the SPSS 19.0
software package for Windows (SPSS Inc., Chicago, IL,
USA).
Results
Of the 70 patients who underwent ESD for a superficial
colorectal tumor C20 mm in diameter during the study
period, 64 patients gave written informed consent to par-
ticipate in the study. Among those patients, 7 were excluded
because of deep submucosal invasive cancer, 5 had recurrent
lesions, and 2 because they were single balloon overtube-
guided cases. The remaining 50 patients (30 males, 20
females; mean age 66.3 years, range 42–88) were enrolled.
Twenty-seven (54 %) of the 50 lesions were the LST gran-
ular-type (LST-G) and 23 (46 %) were the LST non-gran-
ular type (LST-NG). Each was diagnosed preoperatively as
an intramucosal neoplastic lesion or slightly submucosal
invasive cancer. Mean tumor size was 35.5 ± 13 mm.
Thirty of the lesions were adenomas and 20 were adeno-
carcinomas (16 intramucosal carcinoma; 4 submucosal
invasive cancer). Forty of the lesions were located in the
colon, and 10 in the rectum. Patients were randomly
assigned to Group A (N = 27) and Group B (N = 23); 8 of
the Group B patients were conversion cases (Fig. 1). Char-
acteristics of patients are summarized in Table 1.
There were 27 tumors (mean size 33.5 ± 12.5 mm) in
Group A, with 24 located in the colon and 3 in the rectum.
The mean procedure time was 37.4 ± 32.6 min
(mean ± SD), which included the few additional minutes
required for the application of the S–O clip. All tumors
were resected en bloc without any complications.
In Group B, there were 23 tumors (mean size
37.8 ± 13.1 mm) with 16 tumors located in the colon and 7
in the rectum. The mean procedure time was
67.1 ± 44.1 min (mean ± SD), and the en bloc resection
rate was 95.7 % (22/23). In 1 case, a conventional snare was
employed to complete the resection. Eight of the 23 cases
initially assigned to Group B were converted and required
the use of the S–O clip. Although the mean size of the tumor
in these converted cases (36.4 ± 11.1 mm) was similar to
that in the non-converted cases (37.7 ± 14.0 mm), a longer
procedure time was required for the converted cases
(88.3 ± 53.3 vs. 55.9 ± 33.3 min). In the converted cases,
some tumors were in flexural portions, such as the sigmoid
colon (3 cases), hepatic flexure (1 case), and splenic flexure
(1 case) and the tumor in 1 case was in the cecum. Micro
perforation occurred in 1 of these cases, a patient in which a
40-mm LST granular-type was located in the sigmoid colon;
the perforation was resolved endoscopically using the S–O
clip. No complications occurred in the other 22 cases. In
Group A 24/27 (88.9 %) patients were followed for
8 months (median, range 1–34), while 21/23 (91.3 %) of
Group B patients were followed for 11 months (median,
range 1–23). There were no recurrences in either group.
Between-group comparisons showed that the mean
procedure time was significantly shorter when using the
S–O clip (37.4 ± 32.6 vs. 67.1 ± 44.1 min, p = 0.03).
(Table 2; Fig. 6). Logistic regression analysis for resection
time within 36 min, which is the median time of all cases,
showed the following odds ratios: gender (male/female)
0.23 (95 % CI [0.04–1.10], p = 0.07); age 0.99 (95 % CI
[0.92–1.07], p = 0.91); tumor form (LST-G/LST-NG) 0.88
(95 % CI [0.12–6.05], p = 0.89), tumor size 1.12 (95 % CI
[1.01–1.24], p = 0.03), pathology (adenoma/cancer) 0.75
(95 % CI [0.14–3.93], p = 0.73), and location (rectum/
Fig. 5 Submucosal layer is well exfoliated by direct visualization.
A, B A lateral spreading tumor—granular type is located in the
transverse colon. C After separating the tumor from the surrounding
normal mucosa, the S–O clip is attached to the edge of the exfoliated
mucosa. A regular clip used to grasp the distal nylon loop attached to
the S–O clip is then inserted and applied to the colon wall. The
regular clip is generally applied opposite the lesion, enabling traction
that opens the resection margin. Traction on the lesion maintains
visualization of the tissue cutting line of the submucosal layer,
resulting in a safe and successful en bloc dissection. After dissection,
the nylon loop is cut with a loop cutter. The endoscope remains in
position during the entire procedure, and the specimen is removed
with forceps
3146 Surg Endosc (2014) 28:3143–3149
123

colon) 1.60 (95 % CI [0.20–12.2], p = 0.65), and the use
of the S–O clip 0.15 (95 % CI [0.02–0.86], p = 0.03).
Therefore, tumor size and use of traction were strongly
associated with procedure time within 36 min (Table 3).
Discussion
The present study is the first clinical trial of the use of traction
device-assisted ESD for colorectal tumors. The duration of
colorectal ESDs with the traction device was significantly
shorter than that of conventional ESDs (p = 0.03). Further-
more, there were no differences in tumor form, size, and
location, and pathological findings between the two groups.
Although the rates of en bloc resection and complications did
not differ between groups, resection by conventional ESD
was difficult in some cases. To prioritize patient safety above
the research goals, conversion of conventional ESD to S–O
clip-assisted ESD was necessary in 34.8 % (8/23) of patients.
In most of those patients, the tumor was located in flexural
areas, which could increase the risk of perforation due to
perpendicular positioning of the colonoscope with respect to
the colonic wall. In the remaining patients (15/23) in the
conventional group, a longer procedure time was required
(55.9 ± 33.3 min) than in the S–O clip-assisted group
(37.4 ± 32.6 min) even though these cases were initially
considered to be simple. This suggests that the S–O clip is
effective not only for difficult cases but also for cases con-
sidered as being ordinary.
ESD of the colorectum is technically difficult compared
to gastroesophageal ESD due to the unfavorable
Table 1 Characteristics of
patients
Group A S–O clip-assisted ESD,
Group B conventional ESD.
M mucosal cancer, SM
submucosal invasive cancer
Overall Group A Group B p value
Patients 50 27 23
Gender (male/female) 30/20 18/9 12/11 0.30
Age (year, mean ± SD) 66.3 ± 9.3 66.2 ± 9.6 66.4 ± 8.9 0.95
Tumor form (LST-G/LST-NG) 27/23 14/13 13/10 0.74
Tumor size (mean ± SD) 35.5 ± 13.0 33.5 ± 12.5 37.8 ± 13.1 0.25
Pathology (adenoma/cancer) 30/20 19/8 11/12 0.10
Depth of cancer (M/SM) 16/4 5/3 11/1 0.11
Location (rectum/colon) 10/40 3/24 7/16 0.09
Table 2 Results of colorectal endoscopic submucosal dissection
Overall Group A Group B p value
En bloc resection rate 98 % (49/50) 100 % (27/27) 95.7 % (22/23) 0.28
Procedure time (min, mean ± SD) 51.12 ± 41.1 37.4 ± 32.6 67.1 ± 44.1 0.03*
Perforation 1 0 1 0.28
Delayed bleeding 0 0 0 1.00
*
A p value of 0.05 was considered statistically significant
Group A S–O clip-assisted ESD, Group B conventional ESD
Fig. 6 The mean procedure time for ESD was significantly shorter
with the device than without the device
Table 3 Multivariate analyses for successful en block resection rate
within the median resection time of all cases (36 min)
En bloc resection rate within 36 min
OR (95 % CI) p value
Gender 0.23 (0.04–1.1) 0.07
Age 0.99 (0.92–1.07) 0.91
Tumor form 0.88 (0.12–6.05) 0.89
Tumor size 1.12 (1.01–1.24) 0.03*
Pathology 0.75 (0.14–3.93) 0.73
Location 1.60 (0.20–12.2) 0.65
Traction 0.15 (0.02–0.86) 0.03*
*
A p value of 0.05 was considered statistically significant
By logistic regression, OR odds ratio
Surg Endosc (2014) 28:3143–3149 3147
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characteristics of the colon such as the thin wall, presence
of folds and flexions, existence of peristalsis, and fecal
fluid. It is especially dangerous when the cutting line of the
submucosal layer is not clear and a lack of full control over
the scope can cause unexpected incisions, resulting in a
serious complication, such as perforation. The rate of
complications in this trial was not significantly different
between the groups. Even though our study was of a lim-
ited number of cases, the overall rate of complications
(2 %) was much lower than previous studies. The perfo-
ration rate in two reports analyzing the results of more than
1,000 colorectal ESDs performed in specialized centers for
endoscopic treatment in Japan and Korea were 4.1 and
5.3 %, respectively [22, 23]. A possible reason for this
difference is that for all cases, including those in the con-
ventional ESD group, we had the S–O clip available as an
alternative for use in technically difficult lesions. The only
case of perforation that we experienced was in the con-
ventional group. This patient had an LST-G measuring
40 mm located in the sigmoid colon and unfavorable
conditions arose for resection during the procedure. As this
case required a long procedure time and perforation
occurred, we decided to use the S–O clip, which allowed us
to obtain better visualization. Finally, the lesion was
completely resected and the perforation was closed endo-
scopically without surgical intervention. The lesion would
have been easy to resect if the case had been assigned to
the S–O clip-assisted group from the beginning.
A major disadvantage of colorectal ESD compared to
EMR is the longer procedure time as reported in a previous
study, which varied considerably from 45.5 to 134.5 min
[24]. Procedure time is an important factor, since a long
procedure time can result in mental and physical exhaus-
tion of the operator, causing at the same time unstable and
imprecise movements of the scalpel. A long procedure time
was reported as a risk factor for perforation in gastric ESDs
[25]. Since colorectal ESD was approved by the Japanese
government’s medical insurance system only for lesions
C20 mm, it can be considered that ESDs for larger colo-
rectal lesions require a longer operative time than gastric
ESDs. Added to the inherent characteristics of the colo-
rectum and its contents, a long procedure time for colo-
rectal ESDs can increase the risk of perforation and
resultant peritonitis. Shortening the operative time with the
use of devices like the S–O clip would be valuable in
overcoming this drawback.
The S–O clip was simple to use, and no difficulties were
encountered during or after the procedure, with resections
successful without obstacles in all 27 cases. As we reported
[18, 19], the S–O clip was indeed applicable and helpful for
any lesion throughout the large bowel, including those
located in the right colon. Also the recurrence rate using
the S–O clip was as low as that previously reported [22].
Since dissection of the submucosal layer is considered to
be the most difficult step in ESD and since the S–O clip is
effective at this step, it can play an important role in the
development of ESD in non-specialized centers.
Although our study showed the efficacy of the traction
device, the study had some limitations. Firstly, the sample
size was relatively small. In the future, a trial with a larger
sample size could address this limitation. Secondly, all
ESDs were performed by an extremely experienced col-
onoscopist in a single high-volume center. To address the
question of generalizability of the present results, a multi-
institutional trial would be ideal.
In conclusion, this prospective clinical trial proved that
the time required for colorectal ESD was reduced by the S–
O clip, while maintaining a high en bloc resection rate with
no serious complications. The S–O clip-assisted ESD can
be expected to become the standard for colorectal ESDs.
Acknowledgments This work was supported in part by Grant-in-
Aid for Scientific Research (C) (No. 23591023 to T.O. and N.S.) from
the Ministry of Education, Culture, Sports, Science and Technology
of Japan.
Disclosures Hideaki Ritsuno, Naoto Sakamoto, Taro Osada, Shingo
P. Goto, Takashi Murakami, Hiroya Ueyama, Hiroki Mori, Kenshi
Matsumoto, Kazuko Beppu, Tomoyoshi Shibuya, Akihito Nagahara,
Tatsuo Ogihara, Sumio Watanabe have no conflicts of interest or
financial ties to disclose.
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