Digestive Endoscopy (2012) 24 (Suppl. 1), 73–79 doi:10.1111/j.1443-1661.2012.01252.

PROGESSING TOWARDS STANDARDIZATION OF COLORECTAL ESD den_1252 73..79

CURRENT STATUS AND FUTURE PERSPECTIVES OF ENDOSCOPIC

SUBMUCOSAL DISSECTION FOR COLORECTAL TUMORS

Shinji Tanaka,1 Motomi Terasaki,2 Hiroyuki Kanao,1 Shiro Oka1 and Kazuaki Chayama2
Departments of 1Endoscopy and 2Gastroenterology and Metabolism, Hiroshima University Hospital, Hiroshima, Japan

Endoscopic submucosal dissection (ESD) allows for en bloc tumor resection irrespective of the size of the lesion. In Japan,
ESD has been established as a standard method for endoscopic ablation of malignant tumors in the upper gastrointestinal
tract.Although the use of colorectal ESD has been gradually spreading with the development of numerous devices, ESD has
not yet been fully established as a standard therapeutic method for colorectal lesions. Currently, colorectal ESD is
performed as an ‘advanced medical treatment’ without national health insurance coverage. With the recent accumulation of
numerous cases, the safety and simplicity of colorectal ESD have improved remarkably. Currently in Japan, a prospective
multicenter cohort study organized by the Japan Gastroenterological Endoscopy Society is ongoing to clarify the safety and
efficacy of colorectal ESD to obtain remuneration from national health insurance. In this report, we showed the outcome
regarding safety and efficacy of colorectal ESD through a review of the published work. Of 2719 cases with colorectal ESD
at 13 institutions, the complete en bloc resection and perforation rates were 82.8% (61–98.2%, 2082/2516) and 4.7%
(1.4–8.2%, 127/2719), respectively. Additional surgery for perforation was very rare because perforations were tiny enough
to be closed endoscopically by clips in most of the cases and treated conservatively. In the near future, colorectal ESD will
be a common therapeutic method for early colorectal carcinoma.

Key words: colorectal tumor, endoscopic submucosal dissection, ESD, hybrid ESD.

INTRODUCTION efficacy from a review of the published work. Additionally,

Endoscopic submucosal dissection (ESD) enables en bloc
resection of a lesion irrespective of its size.1,2 Accurate histo-
pathological diagnosis can be attained using ESD, and the
affected organ can be preserved after the treatment. There-
fore, ESD is widely used for the treatment of carcinoma of
the upper gastrointestinal tract, particularly in the stomach,3,4
and in Japan, national health insurance covers the expense of
ESD as a therapeutic procedure for early gastric and esoph-
ageal carcinoma. ESD has also been increasingly applied to
the colon and rectum (Fig. 1). Although ESD has not yet
been recognized as a conventional therapeutic procedure for
early colorectal carcinoma due to its technical difficulty, it has
been made easier and safer by recent advances both in equip-
ment (Figs 2,3) and technique, as well as the experience of
many cases.5 In addition, the use of a carbon dioxide (CO2)
insufflation system has made it easier to perform colorectal
ESD.2,6 CO2 can be absorbed by tissue at a speed more than
100 times that of room air. The use of this system can
decrease colonic distension during ESD due to air insuffla-
tion. In addition, even when perforation occurs and the hole
is closed with a clip, the risk of peritonitis is remarkably
decreased.6 In this chapter, we will describe the indications
for colorectal ESD and the outcomes regarding safety and
Correspondence: Shinji Tanaka, Department of Endoscopy,
Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8551,
Japan. Email: colon@hiroshima-u.ac.jp
Received 9 December 2011; accepted 11 January 2012.
© 2012 The Authors
bs_bs_banner
we will discuss the future perspective of colorectal ESD.
INDICATIONS FOR ESD OF COLORECTAL
TUMORS
In general, the colorectal tumors that are difficult to remove
by en bloc endoscopic mucosal resection (EMR) are large
laterally spreading tumors (LST).7 Although LST larger than
20 mm in diameter tend to be removed by piecemeal EMR
due to the size limitation of the snare, cutting the adenoma-
tous portion never has significant effects on the pathological
examination or curability of the lesion. Granular-type LST
showing adenoma or focal cancer in adenoma is an indication
for piecemeal EMR under the condition that the cancerous
portion is perfectly resected en bloc. In such a procedure,
magnifying observation of the pit pattern is essential prior to
piecemeal EMR.8
In contrast, indications for colorectal ESD recommended
by the Colorectal ESD Standardization Implementation
Working Group are as follows (Table 1):1,2,5 (i) lesions diffi-
cult to remove en bloc with a snare EMR due to size, such as
non-granular LST (particularly pseudo-depressed type),
lesions showing a type Vi pit pattern and protruded-type
large lesions suspected to be carcinoma; (ii) lesions with
fibrosis due to biopsy or peristalsis; (iii) sporadic localized
lesions in chronic inflammation such as ulcerative colitis; and
(iv) local residual carcinoma after EMR.
However, ESD for lesions with severe fibrosis is technically
very difficult.9 To select the best therapy (piecemeal EMR,

Digestive Endoscopy © 2012 Japan Gastroenterological Endoscopy Society

74 S TANAKA ET AL.

Fig. 1. (a) Standard endoscopic submucosal dissection (ESD) case for granular-type laterally spreading tumors, nodular mixed type,
Rectsigmoid, 90 mm in diameter. Left, standard colonoscopic view; right, indigo carmine dye spraying view. (b) ESD procedures of
this case. Main knife was Dual knife and SB knife Jr was used to assist. (c) ESD specimen and pathological findings (HE staining,
cross section, ¥ 40). Adenocarcinoma in high-grade tubulovillous adenoma, pSM (5 mm), budding grade 1, tumor margin negative.
Lymph node metastasis was detected after additional surgery.
© 2012 The Authors
Digestive Endoscopy © 2012 Japan Gastroenterological Endoscopy Society
ESD FOR COLORECTAL TUMOR 75

Fig. 2. Each knife for colorectal ESD and its release year.

Fig. 3. Single balloon sliding tube for

colon. This sliding tube is easy to use
and improves colonoscope manipula-
tion in proximal colon, flexure or palace
where paradoxical movement occurs.
(Colorectal Endoscopic Submucosal
Dissection Standardization Implemen-
tation Working Group.)

Table 1. Indication of ESD for colorectal tumor by colorectal ESD standardization implementation working group

1. Large sized (>20 mm in diameter) lesions in which en bloc resection using snare EMR is difficult, although it is indicative for
endoscopic treatment
LST-NG, particularly those of the pseudo-depressed type
Lesions showing VI type pit pattern
Carcinoma with submucosal infiltration
Large depressed type lesion
Large elevated lesion suspected to be carcinoma†
2. Mucosal lesions with fibrosis caused by prolapse due to biopsy or peristalsis of the lesions
3. Sporadic localized tumors in chronic inflammation such as ulcerative colitis
4. Local residual early carcinoma after endoscopic resection
†
Including granular-type laterally spreading tumors (LST-G), nodular mixed type. EMR, endoscopic mucosal resection.

© 2012 The Authors

Digestive Endoscopy © 2012 Japan Gastroenterological Endoscopy Society
76 S TANAKA ET AL.

M SM

Fig. 4. (a) Hybrid endoscopic submucosal dissection (ESD with combination use of endoscopic mucosal resection [EMR]) case for
non-granular laterally spreading tumors, pseudo-depressed type, Rectsigmoid, 25 mm in diameter. Left, standard colonoscopic view;
Right, indigo carmine dye spraying view. (b) Hybrid ESD procedures of this case (as in [a]). Main knife was Dual knife. Subsequently,
after ESD procedures EMR technique was applied. (c) Hybrid ESD specimen and pathological findings (HE staining). Well-
differentiated adenocarcinoma, pSM (500 mm), ly0, v0, tumor margin negative.
© 2012 The Authors
Digestive Endoscopy © 2012 Japan Gastroenterological Endoscopy Society
ESD FOR COLORECTAL TUMOR 77

Table 2. Outcome of colorectal ESD by summary of precious reports by a single institution (no multicenter study)

Authors Year No. of Size En bloc resection Complete en bloc Complications Local recurrence
cases (mm) rate (%) resection rate (%) Perforation (%) Bleeding (%) (%)

Tamegai11 2007 71 32.7 70/71 (98.6%) 68/71 (95.6%) 1/71 (1.4%) 0/71 (0%)
Hurilstome12 2007 42 31 33/42 (84%) 31/42 (70%) 1/42 (2.1%) 4/42 (9.5%) 4/36 (11%)
Fujishiro13 2007 200 29.9 183/200 (91.5%) 141/200 (70.5%) 12/200 (6.0%) 1/200 (1.0%)
Zho14 2009 74 32.6 69/74 (93.2%) 66/74 (89.2%) 6/74 (8.1%) 1/74 (1.4%) 0/74 (0%)
Isomoto15 2009 292 26.8 263/292 (90.1%) 233/292 (79.8%) 23/292 (8.2%) 2/292 (0.7%) 1/220 (0.5%)
Saito16 2009 405 40 352/405 (87%) 14/405 (3.5%) 4/405 (1.0%)
Iizuka17 2009 38 39 23/38 (61%) 22/38 (58%) 3/38 (8%)
Hotta18 2010 120 35 112/120 (93.3%) 102/200 (85%) 9/120 (7.5%)
Niimi19 2010 310 28.9 280/310 (90.3%) 231/310 (74.5%) 15/310 (4.8%) 5/310 (1.6%) 4/202 (2.0%)
Yoshida20 2010 250 29.1 217/250 (86.8%) 203/250 (81.2%) 15/250 (6%) 6/250 (2.4%)
Toyonaga21 2010 512 29 503/512 (98.2%) 9/512 (1.8%) 8/512 (1.6%)
Matsumoto9 2010 203 32.4 174/203 (85.7%) 14/203 (6.9%)
Uraoka22 2011 202 39.9 185/202 (91.6%) 5/202 (2.5%) 1/202 (0.5%) 0/165 (0%)
The newest report was selected from institutions that published several reports.

ESD or surgical resection) in practice, we should Table 3. Overall data from outcome of colorectal ESD by
consider not only the features of the lesions including clinico- summary of previous reports by single institution (non-
pathological aspects and the location but also the skill level of multicenter study)
the colonoscopist including ability in scope handling and the
predicted duration of the procedure. Each item Overall data Range
Recently, the usefulness of hybrid ESD, which is combina-
tion of both ESD and EMR techniques, has been reported for En bloc resection 82.8% (2082/2516) 61–98.2%
relatively small lesions.10 Hybrid ESD provides the time Complete en bloc resection 75.7% (1271/1680) 58–95.6%
benefit and technical support of the dissection technique for Perforation 4.7% (127/2719) 1.4–8.2%
non-experts in colorectal ESD (Fig. 4). Postoperative bleeding 1.5% (31/2087) 0.5–9.5%
Local recurrence 1.2% (9/768) 0–11%
Data from 2719 cases in 13 institutions described in Table 1.
OUTCOMES OF COLORECTAL ESD IN THE
PUBLISHED WORK
The PubMed database was used to search for publica-
period to more recent period of colorectal ESD with-
tions through August 2011 related to colorectal ESD
out considering the learning curve, en bloc resection
using the key words ESD and colon. The MEDLINE data-
(endoscopic) and complete en bloc resection (histological)
base was used to search for publications through August
rates were 88.8% and 83.8%, respectively. The perforation
2011 related to ESD using the above-mentioned key words.
rate was 3.3–14.0%. The delayed perforation rate was
A manual search of the citations of relevant articles was
0.4–0.7%. Postoperative bleeding occurred in 1.5–2.1% of
also performed. Pertinent studies published in English
cases.
and Japanese were reviewed. If an institution had pub-
lished several reports on colorectal ESD, the newest report
was selected for the summary of outcomes of colorectal
OUTCOMES OF COLORECTAL ESD IN
ESD.
A MULTICENTER PROSPECTIVE COHORT
A summary of outcomes of colorectal ESD using previous
STUDY BY THE JAPANESE SOCIETY
reports from single institution studies is described in
FOR CANCER OF THE COLON AND
Table 2.9,11–22 The overall data of outcomes by a summary of
RECTUM (JSCCR)
previous reports from single institution studies are described
in Table 3. Regarding efficacy, the en bloc resection (endo- Partial outcomes of colorectal ESD in a multicenter prospec-
scopic) and complete en bloc resection (histological) rates tive cohort study by the JSCCR, the ‘Prospective multicenter
were 82.8% (61–98.2%, 2082/2516) and 75.7% (58–95.5%, cohort study on local curability and complication in each
1271/1680), respectively. Regarding complications, the perfo- endoscopic treatment for colorectal tumor larger than
ration and postoperative bleeding rates were 4.7% (1.4– 20 mm’ was reported at UEGW 2011 (Stockholm).27 Briefly,
8.2%, 127/2719) and 1.5% (0.5–9.5%, 31/2087), respectively. the en bloc resection and perforation rates of 805 cases
Local recurrence was detected in 1.2% (0–11%, 9/768) of treated with ESD at 19 institutions familiar with colorectal
cases. EMR/ESD were 95% and 1.4% for lesions 20–29 mm in size,
Outcomes of colorectal ESD by a summary of previous 96% and 2.7% for lesions 29–39 mm in size, and 93% and
reports from multicenter studies are shown in Table 4.5,23–26 1.5% for lesions more than 40 mm in size, respectively.
Although these reports include data from both the early Detailed data are now in submission.
© 2012 The Authors
Digestive Endoscopy © 2012 Japan Gastroenterological Endoscopy Society
78 S TANAKA ET AL.

Table 4. Overall data from outcome of colorectal ESD by summary of previous multicenter study reports

Authors Years No. of No. of En block Complete en Complication

institutions cases resection block resection Perforation Delayed perforation Post-ESD bleeding

Tsuda S23 2006 19 1367 5.4% 0.6% 2.1%

Taku K24 2007 4 43 14.0%
Tanaka S5 2010 194 8303 83.8% 4.8%† 0.7% 1.6%
Saito Y25 2010 10 1111 88% 4.9% 0.4% 1.5%
Oka S26 2010 39 688 3.3% 1.7%
†
Intraoperative perforation 4.1%.

Table 5. Indications of colorectal ESD as ‘Advanced medical
treatment’ in Japan
1. Early carcinoma larger than 20 mm which is difficult to
resect en bloc by EMR. Also, curability should be expected
by magnification or EUS.
2. Adenoma showing non-lifting sign
3. Residual lesion after EMR larger than 10 mm, which is
difficult to resect by EMR
EMR, endoscopic mucosal resection; EUS,
ultrasonography.
MULTICENTER PROSPECTIVE COHORT
STUDY BY THE JAPAN
GASTROENTEROLOGICAL ENDOSCOPY
SOCIETY (JGES)
At present, colorectal ESD is performed as an advanced
medical treatment without national health insurance cover-
age. Indications for colorectal ESD as an advanced medical
treatment in Japan are shown in Table 5. From September
2010, colorectal ESD cases performed as an advanced
medical treatment were registered in a multicenter prospec-
tive cohort study by the JGES to obtain medical remunera-
tion from national health insurance using data from this
study (efficacy and safety). More than 1500 cases have
already been entered into this study by 60 institutions in
Japan. In the very near future, the outcomes of this study will
be reported.
DISCUSSION
As a result of the improvements in ESD devices, peripheral
equipment and the development of the colorectal ESD tech-
nique, use of colorectal ESD has spread extensively in Japan.
As shown by the outcomes in our summary of the published
work and in the study by the JSCCR, colorectal ESD has
already become a not too difficult or dangerous technique.
Even if perforation occurs in an ESD procedure, it is a
microperforation and patients can be treated conservatively
by closure of the hole with a clip. In the very near future,
JGES will apply to the Japanese government to provide the
remuneration from national health insurance. We expect that
colorectal ESD will be a common method for large early
colorectal carcinoma that cannot be treated by en bloc
EMR.
However, because colorectal ESD takes longer, requires
more labor and costs more than EMR, we should strictly
determine the indications for colorectal ESD (Table 1).1,2,5
Because tumors of the colon and rectum differ from tumors of
the upper gastrointestinal tract, there are many benign
adenomatous lesions in the colon and rectum that must be
distinguished from carcinoma.1,2,5,28–30 Adenomatous lesions
can be treated by piecemeal EMR, and piecemeal EMR is
sufficient for treatment of adenoma.1,2,5,28–30 Indeed, good
outcome was shown in the published work.10,28,31 From this
point of view, exact diagnosis with magnification (pit pattern
endoscopic diagnosis8 or image-enhanced endoscopy by narrow-band
imaging and flexible spectral imaging color enhancement)32–36
prior to endoscopic treatment is very important to distinguish
among adenoma, cancer in adenoma, and cancer without
adenomatous component. After a detailed examination
prior to endoscopic treatment and with this information,
we should select adequate therapeutic methods considering
curability, safety, simplicity and cost–benefit. In addition,
we should consider the qualifications for colorectal
ESD according to the endoscopic skill and experience in
colorectal ESD. Although live demonstrations and hands-on
seminars of ESD using animal models have been periodically
held in Japan, establishment of an effective training system for
colorectal ESD will be increasingly important in the future.
CONFLICT OF INTEREST
None declared.
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