Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20 doi: 10.1111/den.

13388

Reviews
Management of adverse events related to endoscopic resection of upper
gastrointestinal neoplasms

Management of adverse events related to endoscopic

resection of upper gastrointestinal neoplasms: Review of
the literature and recommendations from experts
Yorimasa Yamamoto,1 Daisuke Kikuchi,2 Yasuaki Nagami,3 Kouichi Nonaka,4 Yosuke Tsuji,5
Ai Fujimoto,6 Yoji Sanomura,7 Kyosuke Tanaka,8 Seiichiro Abe,9 Shuo Zhang,11 Mark
Anthony De Lusong12 and Noriya Uedo10
1
Division of Gastroenterology, Showa University Fujigaoka Hospital, Yokohama, 2Department of
Gastroenterology, Toranomon Hospital, Tokyo, 3Department of Gastroenterology, Osaka City University
Graduate School of Medicine, Osaka, 4Department of Gastroenterology, Saitama Medical University
International Medical Center, Hidaka, 5Department of Gastroenterology, Graduate School of Medicine, The
University of Tokyo, 6Department of Gastroenterology and Hepatology, National Hospital Organization Tokyo
Medical Center, Tokyo, 7Department of Endoscopy, Hiroshima Prefectural Hospital, Hiroshima, 8Department of
Endoscopic Medicine, Mie University Hospital, Tsu, 9Endoscopy Division, National Cancer Center Hospital, Tokyo,
10
Department of Gastrointestinal Oncology, Osaka International Cancer Institute, Osaka, Japan, 11Digestive
Department, Zhejiang Provincial Hospital of TCM, Hangzhou, China and 12Section of Gastroenterology,
Department of Medicine, Philippine General Hospital, University of the Philippines, Manila, Philippines

Prevention therapy is recommended for lesions >1/2 of the
esophageal circumference. Locoregional steroid injection is
recommended for lesions >1/2–3/4 of the esophageal circum-
ference and oral steroids are recommended for lesions >1/2 of
the subtotal circumference. For lesions of the entire circumfer-
ence, oral steroid combined with injection steroid is consid-
ered. Endoscopic balloon dilatation (EBD) is the first choice of
treatment for stricture after esophageal endoscopic submu-
cosal dissection (ESD). Radical incision and cutting or self-
expandable metallic stent can be considered for refractory
stricture after EBD. In case of intraoperative perforation during
esophageal ESD, endoscopic clip closure should be initially
attempted. Surgery is considered for treatment of delayed
perforation. Current standard practice for prevention of
delayed bleeding after gastric ESD includes prophylactic coag-
ulation of vessels on post-ESD ulcers and giving proton pump
inhibitors. Chronic kidney disease stage 4 or 5, multiple
antithrombotic drug use, anticoagulant use, and heparin
bridging therapy are high-risk factors for delayed bleeding
after gastric ESD. Intraoperative perforation during gastric ESD
is initially managed by endoscopic clip closure. If endoscopic
clip closure is difficult, other methods such as over-the-scope
clip (OTSC), polyglycolic acid (PGA) sheet shielding etc. are
attempted. Delayed perforation usually requires surgical inter-
vention, but endoscopic closure by OTSC or PGA sheet may be
considered. Resection of three-quarters of the circumference is
a risk factor for stenosis after gastric ESD. Giving prophylactic
local steroid injection and/or oral steroid is reported, but
effectiveness has not been fully verified as has been done for
esophageal stricture. The main management method for gastric
stenosis is EBD but it may cause perforation.
Key words: adverse event, endoscopic mucosal resection,
endoscopic submucosal dissection, esophageal neoplasm,
stomach neoplasm

methods for neoplasms in the upper gastrointestinal (GI)

INTRODUCTION
tract not only in Japan but also worldwide. Indication for

I NTEREST IN ENDOSCOPIC submucosal dissection

(ESD) is increasing as it is one of the standard treatment
Corresponding: Noriya Uedo, Department of Gastrointestinal
Oncology, Osaka International Cancer Institute, Osaka, Japan.
Email: uedou-no@mc.pref.osaka.jp
Received 19 January 2019; accepted 3 March 2019.
ESD of upper GI neoplasms is being established in some
guidelines.1,2
Although ESD is a minimally invasive treatment, adverse
events (AE) can occur during and after the procedure in a
certain percentage of patients. The major AE associated with
ESD include bleeding, perforation and stenosis.1,2 For these
AE, many preventive and therapeutic methods have been

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Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20 AE related to upper GI ER 5

reported so far.3–5 However, countermeasures for AE have

MANAGEMENT OF ADVERSE EVENTS
been made mainly according to the experience of each
RELATED TO ESOPHAGEAL ESD
facility. The aim of the present review is, therefore, to
systematically collect and review the currently available Prevention of stenosis after esophageal ESD
literature regarding the management of AE associated with
esophageal and gastric ESD, and to propose standards of
care for the AE.
P REVENTION THERAPY IS recommended for lesions
>1/2 of the esophageal circumference (expected muco-
sal defect of ≥2/3 circumference). Locoregional steroid
injection is recommended for lesions >1/2–3/4 of the
METHODS esophageal circumference (expected mucosal defect of 2/
3–5/6). Oral steroids are recommended for lesions >1/2 of
F OR THIS LITERATURE review, algorithms for the
management of AE related to upper GI endoscopic
mucosal resection (EMR)/ESD were created, clinical ques-
the subtotal circumference. For lesions of the entire
circumference, systemic (oral) steroid combined with steroid
injection is considered (Fig. 1).
tions relevant to decision-making were raised, and they were
Widespread mucosal resection by esophageal ESD causes
distributed to a panel of expert endoscopists. Each endo-
stricture and impairs quality of life with dysphagia.6,7 Risk
scopist was put in charge of one topic of adverse events,
of esophageal stricture is increased in a tumor >59% of
carried out a systematic review, summarized currently
circumferential extent or in a resection wound >75% of
available evidence, and drafted recommendations for the
circumferential extent after ESD.6–9 Yamashina et al.10
management of AE. In the systematic review, relevant
reported that strictures occurred in 36% of cases with
publications from January 2000 to June 2018 were searched
lesions ≥50 mm that were <2/3 of circumferential extent.
from PubMed. In addition, manually inspected relevant
Shi et al.9 described that stricture did not occur in most
articles that were missed by the above search strategy were
cases with <1/2 circumferential mucosal defect, whereas
also included. On 21 July 2018, in the Endoscopy Forum
cases with 1/2–3/4 circumferential mucosal defect devel-
Japan held in Otaru, the review results and recommenda-
oped stricture in 28% and cases with >3/4 circumferential
tions were presented by each endoscopist, and overall
mucosal defect had stricture in 94%.
consensus was summarized after discussion. All authors had
Preventive EBD decreases the incidence of post-ESD
access to the statements, reviewed, and approved the final
stricture from 92% to 59% in patients with a resection
manuscript.

Figure 1 Prevention and management of stenosis after esophageal endoscopic submucosal dissection (ESD).

© 2019 Japan Gastroenterological Endoscopy Society


6 Y. Yamamoto et al.
wound >3/4 circumference; however, the preventive effect
of EBD only is not sufficient in most cases.5
Steroid therapy decreases stricture better than preventive
EBD.11Efficacy of prophylactic steroid injection for post-
ESD ulcer was reported in four observational studies12–15
(Table 1). Most studies reported that steroid injection
decreased the incidence of post-ESD stricture in high-risk
patients, and one systematic review showed that injection
steroid was superior to oral steroid in prevention of post-
ESD stricture.18 However, in some patients, refractory
stricture occurred despite locoregional steroid injection.
Hanaoka et al. reported that >3/4 tumor circumferential
extent was an independent risk factor for refractory stric-
tures22, and Nagami et al. reported that >5/6 circumferential
mucosal defect was a risk factor for refractory stricture even
after prophylactic steroid injections.19
Efficacy of systemic (oral) steroids to decrease incidence
of post-ESD strictures was reported in three observational
studies (Table 1).11,16,17 Although these small retrospective
studies described no severe adverse events, long-term
systemic steroid therapy may cause adverse events. A
systematic review confirmed that high-dose steroids would
lead to serious complications such as gastrointestinal ulcer,
hyperglycemia, immunosuppression, osteoporosis and even
systemic infection.20 In particular, patients taking systemic
steroids for ≥21 days or >700 mg prednisolone had
increased risk of infection.21 Therefore, steroid injection is
preferred as a prophylactic treatment for post-ESD esopha-
geal stricture, but for lesions >3/4 circumference (expected
mucosal defect of 5/6 circumference), oral steroid should be
considered because the efficacy of injection steroid is
insufficient and may cause refractory stricture.
Giving oral steroids with/without steroid injection is
recommended for preventing stricture of entire circumfer-
ential lesions. Locoregional steroid injection only is usually
insufficient for the prevention of stricture of entire circum-
ferential lesions (Table 2).15,22,23 Some reports stated that
oral steroids only could not prevent stricture in most cases,
but that it decreased the number of subsequent EBD
treatments for refractory stricture.23–25 Recently, some
investigators suggested combination therapy of injection
steroid followed by oral steroid administration may prevent
stricture after entire circumferential ESD.26,27 Nevertheless,
development of other effective prophylactic methods is
needed for management of stricture after entire circumfer-
ential ESD.
Systematic literature search formula for English publica-
tion: [endoscopic submucosal dissection] OR [endoscopic
mucosal resection] AND [stricture] OR [stenosis] AND
[esophageal] OR [esophagus], Database: Pubmed (search
period of 2000–2018).
© 2019 Japan Gastroenterological Endoscopy Society
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Digestive Endoscopy 2019; 31: (Suppl. 1): 4–20
Management of stricture after esophageal
ESD
Endoscopic balloon dilation is the first choice of treatment
for stricture after esophageal ESD. However, careful
precaution is needed to avoid perforation. Radical incision
and cutting (RIC) or self-expandable metallic stent (SEMS)
can be considered for refractory stricture after EBD (Fig. 1).
A stricture is generally defined as a symptomatic
dysphagia and/or impossible passage of a standard endo-
scope at the stricture. EBD is conducted using a balloon
dilator, and is repeated until successful passage of a standard
scope at the stricture.
Currently, there is no standard criteria for balloon size.
A large-sized balloon may be more effective than a smaller
one, but the risk of perforation increases. Perforation rate
of EBD for post-ESD esophageal stricture was reported to
be approximately 4–9%.28,29 Tsujii et al.30 indicated that
the risk of perforation during EBD was higher in patients
who received prophylactic steroid injection or those that
had EBD with balloon >15 mm in diameter. In his animal
study, Nonaka et al.31 also suggested that the risk of
perforation during EBD increased when prophylactic
steroid injection was given. Accordingly, size of the
balloon dilator should be started from 12 mm to reduce
risk of perforation during EBD. The size can be increased
to the maximum of 15 mm as appropriate for each case.
Careful precaution is required in patients who were
previously given prophylactic steroid injection as the risk
of perforation increased.
Additional treatment is needed if EBD is insufficient for
the treatment of stricture. There is no consensus on the
number of subsequent sessions of EBD required before
switching to another treatment. Currently, RIC and SEMS
can be indicated for refractory esophageal stricture after
repeated EBD. RIC was developed for treatment of
refractory esophageal stricture after endoscopic resection
of esophageal neoplasms.32 In the original method, insu-
lated-tip (IT) knife was used for incision of fibrosis at the
stricture site, but a scissor-type knife can be used as it is
safer than the other knives. Subsequent EBD can be
repeated after RIC, and additional local steroid injection to
the post-EBD wound prevents recurrent stricture.33 SEMS
has risk of persistent chest pain, stent migration, and
recurrent stricture after removal.34 The biodegradable stent
(BDS) often cannot achieve sufficient patency for refractory
benign stricture by stent collapse or hyper-regeneration of
the mucosa.35,36 Collectively, there is currently no strong
evidence regarding advantage of stent placement over the
other methods of treatment for refractory stricture after
EBD.
 Table 1 Effect of preventive steroid therapy for esophageal stricture in subcircumferential lesions

Author, Design Intervention Dosage Sample Circumference Whole Follow-up Stricture Sessions Adverse Definition
year size of mucosal circumference period rate (%) of EBD event of stricture
(treated/ defect (%) n (%) required
control)
Hashimoto Retrospective Triamcinolone 18–60 mg 21/20 ≥75.0 0 (0) 1 year 19.0 vs 75.0 Mean 0 10.2-mm
(2011)13 injection days 3, (P < 0.01) 1.7 vs 6.6 scope
7, 10 (P < 0.01)
Hanaoka Prospective Triamcinolone 100 mg 30/29 ≥75.0 0 (0) 2 months 10.0 vs 66.0 Median 7% 9.2-mm
(2012)12 historical injection day 0 (P < 0.001) 0 vs 2 (submucosal scope
Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20

(P < 0.001) tear,

bleeding)
Takahashi RCT Triamcinolone 40 mg 16/16 ≥75.0 (>2/3 5 (31.3)/5 16.1  5.6 62.5 vs 87.5 Mean 0.5% vs 1.0% <11 mm
(2015)15 injection day 0 circumference) months (P = 0.22) 6.1 vs (perforation
12.5 (0.38) due to EBD)
Nagami Retrospective, Triamcinolone 80 mg 37/37 ≥66.7 0 (0) 2 months 18.9 vs 45.9 Mean 0 9.2-mm
(2017)14 matched injection day 0 (P = 0.016) 0.5 vs scope
1.7 (0.006)
Yamaguchi Retrospective Oral 30 mg 19 vs 22 ≥75.0 3 vs 3 3 months 5.3 vs 31.8 Mean 0 No
(2011)11 prednisolone tapered (P = 0.03) 1.7 vs 6.6 described
vs preventive every 2 (P < 0.001)
EBD weeks
Kataoka Retrospective Oral 30 mg 17 vs 16 >75.0 3 vs 2 Median 17.6 vs 68.7 Median 0 9.2-mm
(2015)16 prednisolone 1 week 12 months (P < 0.01) 4.6 vs 8.1 scope
20 mg (P < 0.01)
1 week
10 mg
1 week
Zhou Retrospective Oral 30 mg 13 vs 10 ≥75.0 2 vs 2 12 months 23.1 vs 80.0 Mean 0 10.2-mm
(2017)17 prednisolone tapered (P = 0.007) 0.69 vs 13.5 scope
every (P = 0.004)
2 weeks?
EBD, endoscopic balloon dilatation; RCT, randomized controlled trial.
7 AE related to upper GI ER

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 8

Table 2 Effect of preventive steroid therapy for esophageal stricture in entire circumferential lesions

Author, Design Intervention Dosage Sample size Circumference Whole Follow-up Stricture Sessions Adverse Definition
year (treated/ of mucosal circumference period rate (%) of EBD event of
control) defect (%) n (%) required stricture
Y. Yamamoto et al.

Hanaoka Retrospective Triamcinolone 100 mg 12 100.0 12 (100) NA 91.7 Median 9.2-mm

(2016)22 injection day 0 13 (0–40) scope
Miwata Retrospective Prednisolone NA 6 100.0 6 (100) NA 100.0 >5, 33% 0 11.7-mm
(2016)23 injection scope
Takahashi RCT Triamcinolone 40 mg 5 100.0 6 (100) NA 100.0 Mean 0.5% vs 1.0% <11 mm
(2015)15 injection day 0 7.7  1.7 (perforation
due to EBD)
Isomoto Retrospective Oral 30 mg 4 vs 3 100.0 7 (100) 11 (5–22) 50.0 Mean 0 Dysphagia
(2011)24 case series prednisolone tapered months vs 100 3.3 vs 32.7
every (P < 0.05)
2 weeks

© 2019 Japan Gastroenterological Endoscopy Society

Sato Retrospective Oral 30 mg 10 vs 13 100.0 23 (100) 9 weeks 100 Mean 0 9.9-mm
(2013)25 prednisolone tapered vs 100 13.8 vs 33.5 scope
every (P < 0.01)
2 weeks
Miwata Retrospective Oral 0.5 mg/kg 13 100.0 13 (100) NA 100.0 >5, 67% 0 2T260M
(2016)23 prednisolone per day
tapered
every 1 week
Izuka Retrospective Oral (i) 30 mg 11 vs 11 100.0 22 (100) 20 36.4 Mean (i) Candida 9.8-mm
(2018)26 prednisolone tapered weeks vs 81.8 6.2 vs 19.4 esophagitis, scope
with every (P = 0.04) (P = 0.023) arthritis,
triamcinolone 3 weeks myopathy
injection (ii) 30 mg (ii)
tapered pneumoniae,
every oral herpes
2 weeks
Kadota Retrospective Oral 30 mg 14 100.0 14 (100) 12 71% NA Pneumoniae 9.2-mm
(2016)27 prednisolone tapered months scope
with every
triamcinolone 2 weeks,
injection and 50 mg
triamcinolone
EBD, endoscopic balloon dilatation; RCT, randomized controlled trial.
Digestive Endoscopy 2019; 31: (Suppl. 1): 4–20

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Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20
Novel approaches for prevention of post-
esophageal ESD stricture
Novel preventive methods for post-esophageal ESD stricture
including: (i) mechanical method; (ii) antiproliferative
method; (iii) regenerative method; and (iv) protective
method are reported.37,38 Some methods may be suitable
for use but all are still investigational; thus further inves-
tigation is required before general implementation.
Mechanical method
Despite some observational investigations, efficacy of
SEMS for the prevention of stricture after esophageal ESD
remains indecisive.34,39 Migration of SEMS and stricture
after removal of SEMS are clinical problems. Saito et al.40
suggested the efficacy of prophylactic BDS placement in 13
cases with benign esophageal stricture including post-
esophageal ESD cases, but its preventive efficacy should
be validated in a large-scale study.
Antiproliferative method
Considering esophageal stricture occurs in parallel with the
healing process of the wound, the antiproliferative method
might be effective in preventing stricture. Some observa-
tional studies showed reduction of stricture rate by
botulinum toxin type A (BTX-A) injection (11.4% vs
37.8% for control, P = 0.02),41 tranilast oral dosage (33.3%
vs 68.8% for control, P = 0.04)42 and mitomycin C
injection in patients with refractory post-esophageal ESD
stricture.43
Regenerative method
Application of regenerative medicine to post-esophageal
ESD ulcer promotes wound healing and suppresses inflam-
matory and profibrotic changes.38 Ohki et al.44 reported that
autologous cell sheet transplantation reduced the incidence
of stricture after high-risk ESD (>3/4 of the circumference
resection) at a success rate of 25%. This method is
promising but the high cost is a concern regarding adoption
of this method in clinical practice.
Protective method
If exposed submucosa on a widespread ESD ulcer base is
protected with any covering material, it might prevent
stricture formation. Lua et al.45 suggested safety and
efficacy of carboxymethyl cellulose (CMC) sheet, which is
widely used in general or gynecological surgery for
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AE related to upper GI ER 9
prevention of intraperitoneal adhesion, for prevention of
post-ESD stricture (stricture rate of 57%: 4/7). Takeuchi
et al. reported that polyglycolic acid (PGA) sheet, which is a
biodegradable suture-reinforcing material, minimized scar
contraction after partial glossectomy, and it suggested
potential efficacy of PGA sheet for prevention of esophageal
stricture after ESD.46 Stricture rates reported by Sakaguchi
et al. and Iizuka et al. were 7.7% (1/13) and 37.5% (3/8),
respectively.47,48 Moreover, Sakaguchi et al. showed the
synergic effect of triamcinolone injection and PGA shield-
ing for near-circumferential ESD cases with a stricture rate
of 11.1% (1/9).49 Chai et al. showed that when PGA was
used with SEMS, it significantly reduced stricture rate
compared to SEMS only (20.6% vs 46.9%, P = 0.024).50
Prevention and management of perforation
in esophageal ESD
In case of intraoperative perforation during esophageal ESD,
endoscopic clip closure should be attempted initially.
Surgery is considered for treatment of delayed perforation
(Fig. 2).
Five meta-analyses reported the incidence of intraopera-
tive esophageal perforation ranging from 1.5% to 5.0%.51–55
One meta-analysis53 reported there was no difference in
perforation rate between EMR and ESD, whereas another54
reported that ESD had a significantly higher incidence of
perforation. The different incidences may be caused by the
different definitions of perforation, suggesting the impor-
tance of the use of standardized criteria for AE in such
analyses. Some literature suggested that the risk of perfo-
ration increased in cases with large lesions56 or for
procedures in less experienced facilities.57
Most literature studied intraoperative perforation only.
Literature that directly examined the management of
perforations is limited to case series and case reports,
probably because the number of esophageal ESD proce-
dures in each institution and the incidence of intraoperative
perforations were small. Therefore, appropriate manage-
ment for perforation was not systematically elucidated.
Some reports suggested even conservative treatment (e.g.
fasting, i.v. fluids, and antibiotic treatment) without
endoscopic closure was sufficient in cases of small
perforation. Endoscopic clip closure is the first-line of
treatment for intraoperative perforation. Recently, the
usefulness of application of PGA sheets has been
reported.58–60 For perforations that were difficult to close
with both methods, case reports suggested the efficacy of
temporary SEMS placement, and over-the-scope clip
(OTSC) treatment with coil embolization as nonsurgical
treatment.61,62
© 2019 Japan Gastroenterological Endoscopy Society

10 Y. Yamamoto et al.
Figure 2 Management of perforation in esophageal endoscopic submucosal dissection (ESD). CM, contrast medium; CT,
computed tomography; NG, nasogastric.
Delayed perforation is quite rare but can be serious.63,64
Delayed perforation occurred more frequently in patients
with large lesions, lesions with fibrosis, and in those who
were given steroids. Some patients with delayed perforation
treated with SEMS could avoid surgery, but half of the cases
required esophagectomy.
Systematic literature search formula for English publica-
tion was: [endoscopic submucosal dissection] AND [esoph-
agus] OR [esophageal] AND [perforation]. Database:
PubMed (search period of 2000–2018).
ADVERSE EVENTS RELATED TO GASTRIC ESD
Prevention and management of delayed
bleeding after gastric ESD
C URRENT STANDARD PRACTICE for prevention of
delayed bleeding after gastric ESD includes prophy-
lactic coagulation of vessels on post-ESD ulcers and proton
pump inhibitors (PPI). Chronic kidney disease (CKD) stage
4 or 5, multiple antithrombotic drug use, anticoagulant use,
and heparin bridging therapy are high-risk factors for
delayed bleeding after gastric ESD (Fig. 3). New prevention
methods may be considered for high-risk patients for
delayed bleeding.
A retrospective observational study indicated prophylac-
tic coagulation for all visible vessels at the base of post-ESD
ulcer reduced incidence of delayed bleeding, and is
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Digestive Endoscopy 2019; 31: (Suppl. 1): 4–20
commonly carried out in ESD practice.4 Several randomized
trials and a meta-analysis indicated that giving PPI signif-
icantly reduced the incidence of delayed bleeding compared
to histamine-2 receptor antagonist (H2RA); thus it is
recommended.65
A meta-analysis indicated that the significant risk factors
for delayed bleeding after gastric ESD were antithrombotic
drug intake, CKD, resected specimen size >30 mm, and use
of a H2RA instead of a PPI.66 Among these risk factors,
CKD had the highest risk (odds ratio of 3.38) of delayed
bleeding ranging from 13.5% to 33.3% (Table 3).67–69
Use of antithrombotic agents is also one of the risk factors
for delayed bleeding after gastric ESD. Japanese Gastroen-
terological Endoscopy Society (JGES) guidelines, however,
recommend carrying out high-bleeding-risk procedure with-
out interruption of low-dose aspirin (LDA) therapy in
patients who are at high risk for thromboembolic events.70
Several comparative studies showed a delayed bleeding rate
in patients who underwent gastric ESD under continuation
of LDA ranging from 3.6% to 21.1%, whereas that in those
who interrupted LDA was similar (3.6%–23.8%)
(Table 4).71–77 Two meta-analyses of observational studies
indicated similar delayed bleeding rate after gastric ESD
between continuation and interruption of LDA.77,78 In terms
of multiple antithrombotic therapies, the JGES guidelines
recommend that thienopyridine should be withdrawn or
replaced by aspirin or cilostazol monotherapy for high-risk
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Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20 AE related to upper GI ER 11

Figure 3 Prevention and management of delayed bleeding after gastric endoscopic submucosal dissection (ESD). CKD, chronic
kidney disease.

Table 3 Rates of bleeding after gastric ESD in patients with CKD drugs is one of the high risk factors. A meta-analysis
Author, year Lesions, Delayed Delayed CKD indicated that the risk of delayed bleeding after gastric ESD
n bleeding, bleeding, stage in regular users of multiple antithrombotic drugs was
n % significantly higher than never users (odds ratio 5.17 [95%
CI: 3.13–8.54]).77
Numata (2013)67 15 5 33.3 5
Yoshioka (2015)68 52 7 13.5 4 or 5 Recently published supplementary issue of JGES guide-
Choi (2018)69 41 10 24.4 4 or 5 lines for management of patients taking anticoagulants
suggests the possibility of continuation of warfarin instead
CKD, chronic kidney disease; ESD, endoscopic submucosal dissec-
tion.
of heparin bridging therapy during high-bleeding-risk
endoscopic procedures86 because many studies showed a
high incidence of delayed bleeding after gastric ESD in
bleeding procedure.70 Because of the high delayed bleeding patients received heparin bridging therapy (10.8–61.5%;
rates after gastric ESD in patients taking multiple antithrom- Table 6).76,79,82–85,87,88
botics including anticoagulants, ranging from 11.1% to Systematic literature search formula for English publica-
45.4% (Table 5),75,76,79–85 use of multiple antithrombotic tion: [endoscopic submucosal dissection] AND [bleeding]

Table 4 Rates of bleeding after gastric ESD between patients with continued LDA use and interrupted LDA use

Author, year Continued LDA use, n Delayed bleeding, n (%) Interrupted LDA use, n Delayed bleeding, n (%)
71
Cho (2012) 19 4 (21.1) 56 2 (3.6)
Lim (2012)72 116 16 (13.8) 90 5 (5.6)
Matsumura (2014)73 21 2 (9.5) 21 5 (23.8)
Sanomura (2014)74 28 1 (3.6) 66 3 (4.5)
Tounou (2015)75 14 2 (14.3) – –
Igarashi (2017)76 33 4 (12.1) 171 19 (11.1)
Dong (2017)77 Continued use of LDA does not increase the risk of bleeding after gastric ESD compared
with interrupted use of LDA (meta-analysis)
ESD, endoscopic submucosal dissection; LDA, low-dose aspirin.

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12 Y. Yamamoto et al. Digestive Endoscopy 2019; 31: (Suppl. 1): 4–20

Table 5 Rates of bleeding after gastric ESD in patients taking post-ESD wound through the working channel was techni-
multiple antithrombotic drugs cal; however, in a prospective study, Mori et al.92 developed
Author, year Lesions, Delayed Delayed a delivery station system and showed feasibility of the
n bleeding, n bleeding, % delivery device.
Usefulness of endoscopic closure of a post-ESD wound
Yoshio (2013)79 17 3 17.6 was also investigated to prevent post-ESD bleeding in the
Takeuchi (2013)80 23 3 13.0
stomach. Choi et al.93showed that endoclip closure of post-
Tounou (2015)75 7 3 42.9
ESD ulcer significantly reduced delayed bleeding rate
Ono (2015)81 14 6 42.9
Igarashi (2017)76 37 6 16.2 compared to the control group (3.3% vs 13.3%, P = 0.04).
Furuhata (2017)82 36 6 16.7 There were small case series suggesting the usefulness of
Yoshio (2017)83 22 10 45.4 endoscopic closure of the post-ESD ulcer using endoclip-
Gotoda (2017)84 22 4 18.2 and-loop, OTSC device, overstitch suturing, or hand-sewn
Sanomura (2018)85 18 2 11.1 suturing,94–96 although they were not comparative studies.
ESD, endoscopic submucosal dissection. Systemic literature search formula for English publica-
tion: [endoscopic submucosal dissection], [stomach] OR
[gastric] AND [bleeding], Database: Pubmed (search period
Table 6 Rates of bleeding after gastric ESD in patients
of 2000–2018).
undergoing heparin bridging therapy

Author, year Lesions, Delayed Delayed Prevention and management of perforation

n bleeding, n bleeding, % during gastric ESD
Yoshio (2013)79 24 9 37.5 Intraoperative perforation during gastric ESD is initially
Shindo (2016)87 13 8 61.5 managed by endoscopic clip closure. For unstable vital
Igarashi (2017)76 37 4 10.8 signs of pneumoperitoneum, needle paracentesis is con-
Gotoda (2017)84 16 6 37.5 sidered. If endoscopic clip closure is difficult, other
Furuhata (2017)82 52 16 30.8 methods (OTSC, PGA sheet shielding, purse string
Yoshio (2017)83 73 22 30.1 closure with endoclip-and-loop etc.) are attempted. Unsuc-
Harada (2017)88 23 5 21.7
cessful endoclip closure requires surgical intervention.
Sanomura (2018)85 37 5 13.5
Delayed perforation usually requires surgical intervention,
ESD, endoscopic submucosal dissection. but endoscopic closure by OTSC or PGA sheet may be
considered (Fig. 4).
Among a total of 18 articles identified, the perforation rate
AND [gastric] OR [stomach]), Database: Pubmed (search was 3.02% (512/16 941) and 98.8% of patients (506/512)
period of 2000–2018). recovered without surgical interven-
tion.3,101,102,104,105,108,109,112,113,122,123,125,131–136 Risk fac-
tors for intraoperative perforation during gastric ESD are
New endoscopic approaches for prevention
listed in Table 7. For location, upper third,98–105 middle
of delayed bleeding
third,105,106greater curvature and remnant stomach,107 were
There are some reports regarding new endoscopic approach reported to be high-risk areas for intraoperative perforation.
for prevention of delayed bleeding after ESD in high-risk Other risk factors included tumor size,99,102 invasion
patients. depth,108,109submucosal fibrosis,107,110 elevated macroscopic
Tissue-shielding method using PGA sheet and fibrin glue type107 and old age.108 Long procedure time103,107,108,112 and
was one of the most common approaches for prevention of piecemeal resection103 were also reported to be associated
delayed bleeding after gastric ESD. Two prospective non- with the incidence of perforation, those might be due to not
randomized studies that enrolled patients taking antithrom- only tumor-related factor but also the endoscopist-related
botic agents showed that the delayed bleeding rate was factor. Interestingly, Lim et al.111 suggested prior workload
significantly lower in the tissue-shielding group than in the (i.e. regular endoscopy work of outpatient clinic before ESD
control group (6.7% vs 22.0%, P = 0.04; and 5.8% vs increased risk of intraoperative perforation).
20.8%, P = 0.041, respectively).89,90 Kikuchi et al.91 also Incidence of delayed perforation after gastric ESD is rare
showed favorable results of the PGA sheet shielding method (0.04–0.7%), but it usually requires emergency
in a single arm study. Difficulty of PGA sheet delivery to the surgery65,98,102,108,113–115,122–126 (Table 8). Although

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Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20 AE related to upper GI ER 13

Figure 4 Management of perforation during gastric endoscopic submucosal dissection (ESD). CM, contrast medium; CT,
computed tomography.

Table 7 Risk factors for perforation during gastric ESD Table 8 Delayed perforation cases reported in case series or
clinical trials
Risk factors Details
Author, year Patients Lesions Delayed Emergency
Location of Upper third98–105
perforation surgery
the lesion Middle third105,106Greater curvature,
cases (%) cases (%)
remnant stomach107
Size of the lesion Larger than 20 mm99,102 Onozato 160 171 1 (0.6) 0 (0)
Depth of invasion Muscularis mucosa108Submucosa109 (2016)98
Submucosal fibrosis Scar,107 severe fibrosis110 Uedo (2007)65 143 143 1 (0.7) ND
Prior workload Prior routine diagnostic endoscopies Kato (2011)113 468 468 2 (0.43) 2 (100)
of endoscopist or outpatient clinic work111 Hanaoka 1159 1329 6 (0.45) 5 (83.3)
Long procedure Longer than 60 min.103,107Longer than (2010)114
time 120 min.108,112 Yoo (2012)108 729 823 1 (0.12) 1 (100)
Other Piecemeal resection103Elevated Ohta (2012)102 1500 1795 1 (0.06) 1 (100)
macroscopic type106 Kosaka (2014)122 438 438 1 (0.2) 1 (100)
Patient age ≥81 years108 Chinda (2015)123 307 318 1 (0.3) ND
Miyagi (2015)124 22 2730 1 (0.04) ND
ESD, endoscopic submucosal dissection.
Suzuki (2015)115 4943 4943 7 (0.1) 3 (42.9)
Sumiyoshi 177 209 1 (0.6) 1 (100)
(2017)125
detailed pathogenesis is unclear, several reports suggested
Yamamoto 1158 1199 5 (0.42) 0 (0)
that lesions in the gastric tube, lesions in the upper stomach (2017)126
and excessive electrocautery during hemostasis are associ-
ND, not described.
ated with occurrence of delayed perforation.115,126
For clip closure technique, simple closure method is
indicated for small linear incised perforation, whereas
omental-patch method is indicated for large muscular defect linear incision of the muscularis propria and managed by
especially when it is located at the greater curvature of the simple clip closure. Air deflation is helpful to close
gastric body.127 Usually, ESD perforation is developed as the incised perforation when clip is applied. Recently,

© 2019 Japan Gastroenterological Endoscopy Society


14 Y. Yamamoto et al.
new devices and methods such as OTSC,128 PGA sheet
shielding,129,130 closure using endoclip-and-loop116,126 were
reported in several case studies. All of them could be used
as back-up methods when simple clip closure failed.
Seven articles describe in detail how to manage intraop-
erative perforation during gastric ESD.98,102,105,117,127,131,137
According to these articles, the most important decision
regarding indication for emergency surgery is the condition
of the patient, especially that associated with status of
peritonitis (mediastinitis for gastric tube cases).115 When
pan-peritonitis develops, emergency surgery should be
indicated. Endoscopic closure can be attempted only if
peritonitis is none or localized. When complete clip closure
was achieved, patients followed a favorable course with
conservative treatment.126 Incomplete closure, however,
usually required emergency surgery.105,127 Even after clip
closure, it is better to insert a nasogastric tube, give
antibiotics and follow up carefully under nil per os.
In case of delayed perforation, management is basically
the same as that of intraoperative perforation. The difference
may be high comorbid rate of pan-peritonitis in delayed
perforation cases, and friability of the tissues around the
perforation hole that may make simple clip closure difficult.
Patients with delayed perforation who recovered with
conservative management were mostly those who developed
AE before dietary intake and/or received endoscopic
intervention within 24 h after onset.115,126
Systematic literature search formula for English publica-
tion: [gastric cancer] AND [endoscopic submucosal dissec-
tion] AND [perforation] Database: PubMed (search period
of 2000–2018).
Figure 5 Prevention and management of stenosis after gastric endoscopic submucosal dissection. EBD, endoscopic balloon
dilatation.
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Digestive Endoscopy 2019; 31: (Suppl. 1): 4–20
Prevention and management of stenosis
after gastric ESD
Three-quarter circumference resection is a risk factor for
stenosis after gastric ESD. Giving prophylactic local
injection and/or oral steroid is reported but their effective-
ness has not been fully verified as for esophageal stricture.
The main management method for gastric stenosis is EBD,
but it may cause perforation (Fig. 5).
Some observational studies indicated that one of the
important risk factors for stenosis after gastric ESD in both
cardia and pylorus was circumference of resection wound
>3/4.118–121,138–140
Methods and efficacy of prevention for gastric stenosis is
controversial. One study reported prophylactic EBD was not
effective in reducing the total number of EBD sessions.119
Although it was a small study, combination treatment of oral
and injection steroid had preventive effects for gastric
stenosis.141 Three studies investigated stenosis after pyloric
ESD and they indicated effectiveness of prophylactic EBD
for prevention of pyloric stenosis, whereas steroid injection
was ineffective in one of four cases. Some reports described
use of steroid (triamcinolone) solution for submucosal
injection during ESD.119,141,142 For prevention of stenosis
after both cardiac and pyloric ESD, giving oral steroid was
more effective than injection of steroid, and combination of
injection steroid with oral steroid did not seem to increase
the preventive effect on stenosis.138,141,143
Stenosis after gastric ESD is mainly treated by EBD. Two
articles reported that there was no perforation related to
EBD for cardiac stenosis,118,119 whereas perforation that

Digestive Endoscopy 2019; 31 (Suppl. 1): 4–20
developed during EBD for pyloric stenosis required emer-
gency surgery.118–120,144 Two interesting reports described
the usefulness of mucosal incision of stenotic ulcer scar and
subsequent steroid injection.143,145
Systematic literature search formula for English publica-
tion was [gastric endoscopic submucosal dissection] AND
[stenosis] OR [stricture]. Database: Pubmed (search period
of 2000–2018).
CONCLUSION
A LTHOUGH ESD BEGAN about 20 years ago in Japan
and many articles describe the procedure of ESD and
management of AE, to the best of our knowledge, this is the
first report to summarize the management of AE associated
with upper gastrointestinal ESD using a systematic review.
Prevention is more important than management; however,
even with careful precautions, AE occur in some patients.
Therefore, in their practice, endoscopists must prepare how
to deal with AE. In case of any AE, early explanation to the
patient and their family and early consultation with surgeons
are important. We expect our review article and the
algorithms to be useful for many endoscopists to safely
carry out the ESD procedure.
CONFLICTS OF INTEREST
A UTHORS DECLARE NO conflicts of interest for this
article.
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