Surg Endosc DOI 10.1007/s00464-015-4153-6
and Other Interventional Techniques
Adverse events associated with endoscopic dilation for gastric stenosis after endoscopic submucosal dissection for early gastric cancer Yoshihiro Kishida1 • Naomi Kakushima1 • Noboru Kawata1 • Masaki Tanaka1 • Kohei Takizawa1 • Kenichiro Imai1 • Kinichi Hotta1 • Hiroyuki Matsubayashi1 • Hiroyuki Ono1
Received: 5 January 2015 / Accepted: 6 March 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Gastric stenosis is a major problem after endoscopic submucosal dissection (ESD) for large early gastric cancer, but little is known about the incidence of adverse events associated with endoscopic dilation (ED) for stenosis caused by gastric ESD. The aims of this study were to determine the incidence and risk of bleeding and perforation associated with ED for gastric stenosis after ESD. Methods This was a single-center, retrospective cohort study conducted at a specialized center for treating cancer. A total of 342 procedures of wire-guided balloon ED were performed for stenosis after gastric ESD in 64 patients. The incidence of adverse events and related clinical characteristics was analyzed. Results The incidence of bleeding was 3.1 % (2/64) per patient and 0.6 % (2/342) per procedure. One bleeding case with incomplete cessation of antithrombotics before ED required blood transfusion. The incidence of perforation was 7.8 % (5/64) per patient and 1.5 % (5/342) per procedure. All perforations occurred in the lower part of the stomach. Two of the five perforation cases were inappropriate for nonoperative therapy, and thus, emergency surgery was performed. Among the other three perforation cases, one case required surgery for refractory stenosis and ED was continued in one case after nonoperative therapy.
& Yoshihiro Kishida [email protected] Naomi Kakushima [email protected] 1
Division of Endoscopy, Shizuoka Cancer Center, 1007, Shimonagakubo, Nagaizumi, Suntogun, Shizuoka 411-8777, Japan
Conclusions The incidence of bleeding caused by ED for gastric stenosis after ESD was small. Although not significant, ED in the lower stomach presents a substantial risk of perforation. Keywords Gastric stenosis Endoscopic submucosal dissection Endoscopic dilation Since its development, endoscopic submucosal dissection (ESD) has been applied for the treatment of many patients with early gastric cancer (EGC) in Japan to achieve en bloc curative resection and decrease the risk of local recurrence [1, 2]. At present, one of the expanding indications of EGC for endoscopic resection (ER) is a lesion with a preoperative endoscopic diagnosis of differentiated-type intramucosal cancer without ulcer findings irrespective of size [3]. If the pathological results of the resected specimen fulfill the curative criteria of nil risk of lymph node metastasis [3], additional gastric resection is theoretically unnecessary. Therefore, compared with those caused by endoscopic mucosal resection, larger artificial ulcers caused by ESD are treated by nonoperative therapy, namely administration of proton pump inhibitors [4–6]. Ulcers after ESD occurring in the stomach are reported to heal within 8 weeks regardless of size and location [4–6]. For large ulcers after ESD, particularly those located in the pyloric or cardiac region, stenosis occasionally occurs after scarring of the ulcer. Stenosis after gastric ESD has been reported to occur at a rate of 1.9–2.5 % [7, 8]. Resection larger than 3/4 of the circumferential extent and longitudinal extent larger than 5 cm in length are reported to be risk factors for gastric stenosis after ESD [7–9]. Endoscopic dilation (ED) is applied when stenosis causes clinical gastric outlet obstruction. However, ED is also
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associated with risks of clinically important adverse events, such as bleeding and perforation [7–10]. Previous studies have reported the efficacy of ED for benign stenosis [11–15]. The incidence of adverse events associated with ED performed for anastomotic stenosis after gastrectomy has been reported to be 0 % per patient for bleeding, and \4.9 % per patient and 2.2 % per procedure for perforation [11–15]. However, little is known about the incidence of adverse events associated with ED for stenosis caused by gastric ESD. The aims of this study were to determine the incidence and risk of bleeding and perforation associated with ED for gastric stenosis after ESD.
Materials and methods From September 2002 to December 2012, among 3162 gastric ESD cases, a total of 64 patients who underwent ED for stenosis after gastric ESD in our hospital were enrolled in the present study. The indications of ESD in our hospital are patients with EGC who meet the Japanese EGC criteria for ER [3]. Among these patients, the medical records were retrospectively assessed for the following factors: patientrelated factors, such as age, sex and use of antithrombotics; ESD-related factors, such as location, circumferential extent of the mucosal defect and diameter of the specimen; and ED-related factors, such as the number of procedures, period from ESD to starting ED, treatment duration and adverse events associated with ED. Because ED is considered a high-risk procedure for bleeding in the Japanese guidelines [16], antithrombotics were generally discontinued for a minimum of 3–7 days before ED. Indications of ED were determined as patients who exhibited symptoms of stenosis, those for whom a generalpurpose endoscope (GIF-H260, caliber 9.8 mm; Olympus, Tokyo, Japan) could not pass through stenosis and those at a risk of developing stenosis because of resection of larger than 3/4 of the circumferential extent [7–9]. ED was performed with balloon dilation using a through-the-scope tool (CRETM Wire-guided Balloon Dilators; Boston Scientific Corporation, Marlborough, MA, USA). The size of the tool was determined according to the severity of stenosis, and ED was repeatedly performed until stenosis was cleared. After each ED procedure, the dilated site was carefully examined for signs of bleeding, mucosal tear, or perforation and whether the endoscope could pass through stenosis. If there were any areas with suspected perforation, abdominal radiography or computed tomography (CT) was performed to check for the presence of abdominal free air. Patients were carefully observed for at least 1 h in the recovery room, and liquids were allowed 2 h after the procedure.
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Adverse events were evaluated after each ED procedure. Bleeding determined as apparent hematemesis or melena was treated by emergency endoscopy. Perforation was considered as deep mucosal tears with abdominal free air. All statistical analyses were performed using Stata SE statistical software for Windows (version 10.1; StataCorp LP, College Station, TX, USA). This retrospective study was approved by the institutional review board of our hospital (26-J60-26-1-3).
Results Characteristics of patients and factors related to ESD and ED are shown in Table 1. Of 64 patients included in analysis, 46 were men and 18 were women, with a median age of 75 years (range 46–90 years). Among them, 19 patients (30 %) had a history of daily usage of antithrombotics. The lower stomach was the most common location of stenosis after ESD (57.8 %, 37/64). The mucosal defect was larger than 3/4 of the circumferential extent in 46 patients (71.9 %), and the median diameter of the resected specimen was 66 mm (range 27–147 mm). A total of 342 ED procedures were performed with a median of four per patient (range 1–25 procedures). The first ED procedure was performed at a median of 29 days (range 2–91 days) after ESD, and the median treatment duration was 30 days (range 1–282 days). The rates of adverse events associated with ED are shown in Table 2. The incidence of bleeding was 3.1 % (2/ 64) per patient and 0.6 % (2/342) per procedure. One case of bleeding occurred in an 82-year-old male who underwent a second ED procedure in the lesser curvature of the gastric cardia with a mucosal defect of 1/2–3/4 of the circumferential extent. This patient was on warfarin therapy for atrial fibrillation, which was discontinued only 1 day before ED and was restarted the day after ED. Three days after the ED procedure, he was admitted to our hospital for melena. Laboratory data showed a decrease in hemoglobin level from 14.5 to 8.7 g/dL and a prothrombin time and international normalized ratio of 23.6 s and 2.25, respectively. Emergency endoscopy revealed bleeding which was stopped by coagulation, and blood transfusion was performed. A second case of bleeding occurred in the lower stomach with a mucosal defect of 3/4-semicircular circumference in a 72-year-old female who did not take daily antithrombotics. Bleeding occurred during the second ED procedure, which was performed 70 days after ESD. Emergency endoscopy confirmed bleeding from the dilated site, which was stopped by coagulation. The incidence of perforation was 7.8 % (5/64) per patient and 1.5 % (5/342) per procedure. Details of the five perforation cases are shown in Table 3. All five
Surg Endosc Table 1 Characteristics of 64 patients who underwent endoscopic dilation after gastric ESD
Age in years [median (range)]
75 (46–90)
Sex (male:female)
46:18
Use of antithrombotics [% (n)]
30 % (19/64)
Use of steroids [% (n)] Location of lesion resected by ESD [% (n)]
Circumferential extent of mucosal defect [% (n)]
U
22 % (14/64) 37.5 % (24/64)
M
4.7 % (3/64)
L
57.8 % (37/64)
\1/2
6.2 % (4/64)
1/2–3/4
21.9 % (14/64)
[3/4-semicircular
62.5 % (40/64)
Whole circular
9.4 % (6/64)
Diameter of mucosal resection [median (range), mm] Number of ED procedures
66 (27–147) Total
342
per patient [median (range)]
4 (1–25)
Period from ESD to first ED [median (range), days]
28 (5–90)
Duration of ED [median (range), days]
30.5 (1–282)
U upper stomach, M middle stomach, L lower stomach, ED endoscopic dilation, ESD endoscopic submucosal dissection
Table 2 Adverse events associated with ED after gastric ESD
Per patient (n = 64) (%)
Per procedure (n = 342) (%)
Bleeding (n = 2)
3.1
0.6
Blood transfusion (n = 1)
1.6
0.3
7.8 10.9
1.5 2.0
Perforation (n = 5)a Hospitalization (n = 7)
ED endoscopic dilation, ESD endoscopic submucosal dissection a
Two cases underwent emergency surgery
perforations occurred in the lower part of the stomach. The size of the mucosal defect in each of these patients was larger than 3/4 of the circumferential extent. Perforation occurred at a median of three ED procedures (range 2–5 procedures), a median of 17 days (range 5–21 days) after starting ED and a median of 43 days (range 29–63 days) after ESD. Among these patients, two were considered inappropriate for nonoperative therapy and, therefore, underwent emergency surgery (Fig. 1). Among the three
patients who had improvement in symptoms by nonoperative therapy, one received additional ED and another underwent surgery for refractory stenosis. Of all 64 patients, seven (10.9 %) required hospitalization for adverse events associated with ED (two cases of bleeding and five of perforation). There were no other adverse events associated with the ED procedure. There were no significant risk factors related to perforation among the patient- or ESD-related factors (Table 4).
Table 3 Details of perforation related to endoscopic dilation for stenosis after ESD Sex
Age
Location
Circumferential extent
M
70
L
3/4-semicircular
M
46
L
F F
81 76
L L
M
88
L
Resection size (mm)
Initiation of ED (day)
Day of perforation (day)
Number of ED at perforation
Emergent surgery/ nonoperative therapy
80
23
40
3
Nonoperativea
3/4-semicircular
130
36
63
5
Nonoperative
3/4-semicircular 3/4-semicircular
35 76
15 38
29 43
3 2
Surgery Nonoperative
3/4-semicircular
66
26
44
5
Surgery
M male, F female, L lower stomach, ESD endoscopic submucosal dissection, ED endoscopic dilation a
Recovered by nonoperative therapy, although underwent surgery for refractory stenosis
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Surg Endosc Fig. 1 Case of perforation caused by endoscopic dilation for stenosis after gastric endoscopic submucosal dissection (ESD), which was treated by emergency surgery: A A semicircular ulcer was created after ESD of two lesions in the lower stomach. B Stenosis occurred 16 days after ESD. C Perforation occurred after the third endoscopic balloon dilation performed 29 days after ESD. D Emergency surgery was performed for gastric perforation. Resected gastric specimen showed the perforation, which was recognized in the bed of the mucosal defect of ESD
There was only one post-ESD bleeding episode among the perforation cases of ED, which was successfully treated by endoscopic hemostasis. Thus, there was no relation between adverse events at the time of ESD and those of ED (ESD perforation: p = 0.43, post-ESD bleeding: p = 0.41). However, all instances of perforation occurred in the lower part of the stomach. The median duration of ED treatment among cases with and without perforation was 17 days (range 14–50 days) and 34 days (range 1–282 days), respectively (p = 0.49).
Discussion In the present study, we evaluated the incidence of adverse events associated with ED for gastric stenosis caused by ESD among a relatively large number of patients. Ulcer scars after ESD are composed of fibrotic tissues covered by a thin layer of regenerative mucosa [5]. Anatomically, stenosis caused by scarring after ESD differs from anastomotic strictures after gastrectomy, in which all layers of the gastric wall are maintained. We assumed that ED for stenosis after ESD would increase the risk of perforation due to the thinness of the gastric wall. Therefore, we focused on the incidence and risks of adverse events associated with ED for stenosis after gastric ESD.
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The stenosis after gastric ESD occurred in 64 cases out of 3,164 gastric ESD cases, with a rate of 2.02 %. This rate was almost as same as previous reports of 1.9–2.5 % [7, 8]. The incidence of bleeding associated with ED in the present study was 3.1 % per patient and 0.6 % per procedure. Previous studies have reported a bleeding rate of 0–11.1 % per patient for benign stenosis (peptic ulcer, 0 %; corrosive, 0–11.1 %; chronic pancreatitis, 0 %; postgastrectomy, 4.2 %) and 2.0 % per procedure for anastomotic stricture after gastrectomy (Table 5) [11–15, 17–21]. Regarding ED for stenosis after gastric ESD, Coda et al. [9] reported a bleeding rate of 0 % per patient in a case study of 15 patients. Together with our results, the risk of bleeding associated with ED for stenosis caused by ESD compared with other benign causes seems to be similar. No previous study has specifically evaluated the risk of bleeding associated with ED in patients on antithrombotic therapy. Therefore, the issue of cessation of antithrombotic therapy during ED in patients routinely receiving these drugs has not been fully resolved. The current Japanese guidelines rank ED as a high-risk procedure for bleeding [16]. Similarly, the American [22] and British [23] guidelines propose ED as a high-risk procedure for bleeding, whereas it is considered as a low-risk procedure by the European guidelines [24]. The results of the present study showed that the overall risk of bleeding associated with ED
Surg Endosc Table 4 Perforation risk of ED after gastric ESD Perforation? (n = 5)
Perforation- (n = 337)
P value
Age in years [median (range)]
76 (46–88)
76 (46–90)
0.99b
Sex (male:female)
3:2
233:103
0.65a
Daily usage of antithrombotics
2
118
0.82a
Use of steroid
0
96
0.16a
U
0
102
0.09b
M
0
25
L
5
210
\1/2
0
9
1/2–3/4
0
43
[3/4-semicircular
5
240
Whole circular
0 76 (35–130)
45 73 (27–147)
Location
Circumferential extent of mucosal defect
Diameter of resection median (range), mm]
0.92b
0.88b
ESD perforation
0
38
0.43
Post-ESD bleeding
1
31
0.41
Number of ED procedure [median (range)]
5 (3–7)
4 (1–25)
0.67b
Period from ESD to first ED [median (range), days]
26 (15–38)
28 (5–90)
0.79b
Duration of ED [median (range), days]
17 (14–50)
34 (1–282)
0.49b
ED endoscopic dilation, ESD endoscopic submucosal dissection, U upper stomach, M middle stomach, L lower stomach a
Chi-squared test
b
Wilcoxon rank-sum test
was very low with intermittent cessation of antithrombotics, in accordance with the current guidelines. On the other hand, one case with incomplete cessation of warfarin presented delayed bleeding that required blood transfusion. Further studies are needed to clarify optimal management strategies during the periprocedural period of ED. When repetitive ED is required, as shown by a median number of four ED procedures required per patient in this study, an extended duration of antithrombotic cessation may increase the risk of thromboembolic events in susceptible patients. The incidence of perforation in this study was 7.8 % per patient and 1.5 % per procedure, while the perforation rate of ED in other reports was 0–27.8 % per patient for benign stenosis (peptic ulcer, 0–9.1 %; corrosive, 0–27.8 %; chronic pancreatitis, 0 %; anastomotic stricture after gastrectomy, 0–4.9 %) [11–15, 17–21, 25]. Regarding ED for stenosis after gastric ESD, previous studies with a small number of cases reported a rate of 0–50 % per patient (Table 5) [7, 9, 10]. In the present study, which included the largest number of cases to date, we found that the risk of perforation caused by ED for stenosis due to ESD was similar to or lower than that of benign causes. All five cases of perforation in this study occurred in patients who received B5 ED procedures, and all were located in the lower stomach. Interestingly, previous reports of perforation among ED for stenosis after ESD were also in the lower part of the stomach [7, 10]. Although the location of ED
was not a significant risk factor for perforation, the ED procedure itself was rather difficult to perform in the lower stomach compared with that in the upper portion due to the gastric curvature. In addition, among cases with stenosis in the lower part of the stomach, there was often considerable gastric residue complicating the ED procedure. In two of five perforation cases, emergency surgery was performed for fear of leakage of gastric residue. An 18- to 20-mm-diameter balloon was used in four of the five perforation cases, and a 15- to 18-mm-diameter balloon was used in one case. The same size of the balloon was used along the same line; however, the pressure of the balloon dilator was different at each procedure. The pressure was usually set at the minimum at the first procedure and gradually increased along the same line. Three perforation cases using an 18- to 20-mm balloon occurred with a maximum pressure of 6 mmHg (20 mm). Coda et al. [9] reported no complication using a 15- to 18–mm-diameter or an 18- to 20-mm-diameter balloon, whereas Tsunada et al. [10] reported two cases of perforation using a 12- to 15-mm-diameter balloon, and Iizuka et al. [7] reported one case of perforation using a 15- to 18-mm-diameter balloon. Therefore, the optimum size of balloon is not clarified at present. However, using larger balloon dilators such as 20 mm diameter or performing dilation with the maximum pressure might become a risk of perforation.
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Surg Endosc Table 5 Incidence of adverse events associated with endoscopic dilation Cause of stenosis
Author
Bleeding Per patient
Benign Anastomotic stricture
Peptic ulcer
Corrosive
Crohn’s disease Chronic pancreatitis ESD
ESD
Perforation Per procedure
Per patient
Per procedure
Lau [26]
1.9 % (1/54)
1.4 % (1/73)
11.1 % (6/54)
8.2 % (6/73)
Lam [27]
–
–
6.1 % (2/33)
–
Solt [17]
4.2 % (1/24)
2.0 % (1/49)
0 % (0/24)
0 % (0/49)
Kim [11]
0 % (0/17)
0 % (0/19)
0 % (0/17)
0 % (0/19)
Ahmad [12]
0 % (0/14)
0 % (0/23)
0 % (0/14)
0 % (0/23)
Go [13]
–
–
2.6 % (1/38)
–
Ukleja [14] Frutos [15]
– 0 % (0/23)
– –
4.9 % (3/61) 0 % (0/23)
2.2 % (3/128) –
Solt [17]
0 % (0/30)
0 % (0/57)
3.3 % (1/30)
1.8 % (1/57)
Kochhar [19]
0 % (0/11)
–
0 % (0/11)
–
Rana [21]
0 % (0/11)
–
9.1 % (1/11)
–
Solt [17]
0 % (017)
0 % (0/66)
5.9 (1/17)
1.5 % (1/66)
Chiu [18]
11.1 % (2/18)
–
27.8 % (5/18)
–
Kochhar [19]
0 % (0/8)
–
0 % (0/8)
–
Kochhar [20]
0 % (0/41)
–
2.4 % (1/41)
–
Rana [21]
0 % (0/7)
–
14.3 % (1/7)
–
Solt [17]
0 % (0/1)
0 % (0/5)
0 % (0/1)
0 % (0/5)
Kochhar [19]
0 % (0/4)
–
0 % (0/4)
–
Rana [21]
0 % (0/4)
–
0 % (0/4)
–
Coda [9]
0 % (0/15)
–
0 % (0/15)
–
Tsunada [10]
–
–
50 % (2/4)
–
Iizuka [7] Present study
– 3.1 % (2/64)
– 0.6 (2/342)
17 % (1/6) 7.8 % (5/64)
– 1.5 % (5/342)
– not mentioned, ESD endoscopic submucosal dissection
All of the perforation holes were located in the bed of ESD ulcer near the most stenotic area. When the dilation balloon is dilated, the narrowest area will receive the strongest pressure. Even though the ulcer is in the process of healing, the area is thought to be fragile, as it lacks the mucosal and submucosal layer. Therefore, we consider that to avoid overpressure to the stenotic area, choosing smaller diameter of balloon is important. The limitations of this study include its retrospective design in a single institute. The timing of starting ED in patients at a risk of stenosis was decided by the doctors in charge. Nonetheless, these data should prove quite helpful because we enrolled a relatively large number of cases to focus on adverse events associated with ED. In addition, we included only patients who underwent ED for stenosis caused by gastric ESD. In conclusion, the risk of bleeding was very low among patients receiving ED for stenosis after gastric ESD. The risk of bleeding without cessation of antithrombotic agents should be confirmed by a prospective study in the near future. Although not significant, ED in the lower stomach presents a substantial risk of perforation.
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Disclosures Y Kishida, N Kakushima, N Kawata, M Tanaka, K Takizawa, K Imai, K Hotta, H Matsubayashi and H Ono have no conflict of interest or financial interests to declare in association with this study.
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and Other Interventional Techniques
Adverse events associated with endoscopic dilation for gastric stenosis after endoscopic submucosal dissection for early gastric cancer Yoshihiro Kishida1 • Naomi Kakushima1 • Noboru Kawata1 • Masaki Tanaka1 • Kohei Takizawa1 • Kenichiro Imai1 • Kinichi Hotta1 • Hiroyuki Matsubayashi1 • Hiroyuki Ono1
Received: 5 January 2015 / Accepted: 6 March 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Gastric stenosis is a major problem after endoscopic submucosal dissection (ESD) for large early gastric cancer, but little is known about the incidence of adverse events associated with endoscopic dilation (ED) for stenosis caused by gastric ESD. The aims of this study were to determine the incidence and risk of bleeding and perforation associated with ED for gastric stenosis after ESD. Methods This was a single-center, retrospective cohort study conducted at a specialized center for treating cancer. A total of 342 procedures of wire-guided balloon ED were performed for stenosis after gastric ESD in 64 patients. The incidence of adverse events and related clinical characteristics was analyzed. Results The incidence of bleeding was 3.1 % (2/64) per patient and 0.6 % (2/342) per procedure. One bleeding case with incomplete cessation of antithrombotics before ED required blood transfusion. The incidence of perforation was 7.8 % (5/64) per patient and 1.5 % (5/342) per procedure. All perforations occurred in the lower part of the stomach. Two of the five perforation cases were inappropriate for nonoperative therapy, and thus, emergency surgery was performed. Among the other three perforation cases, one case required surgery for refractory stenosis and ED was continued in one case after nonoperative therapy.
& Yoshihiro Kishida [email protected] Naomi Kakushima [email protected] 1
Division of Endoscopy, Shizuoka Cancer Center, 1007, Shimonagakubo, Nagaizumi, Suntogun, Shizuoka 411-8777, Japan
Conclusions The incidence of bleeding caused by ED for gastric stenosis after ESD was small. Although not significant, ED in the lower stomach presents a substantial risk of perforation. Keywords Gastric stenosis Endoscopic submucosal dissection Endoscopic dilation Since its development, endoscopic submucosal dissection (ESD) has been applied for the treatment of many patients with early gastric cancer (EGC) in Japan to achieve en bloc curative resection and decrease the risk of local recurrence [1, 2]. At present, one of the expanding indications of EGC for endoscopic resection (ER) is a lesion with a preoperative endoscopic diagnosis of differentiated-type intramucosal cancer without ulcer findings irrespective of size [3]. If the pathological results of the resected specimen fulfill the curative criteria of nil risk of lymph node metastasis [3], additional gastric resection is theoretically unnecessary. Therefore, compared with those caused by endoscopic mucosal resection, larger artificial ulcers caused by ESD are treated by nonoperative therapy, namely administration of proton pump inhibitors [4–6]. Ulcers after ESD occurring in the stomach are reported to heal within 8 weeks regardless of size and location [4–6]. For large ulcers after ESD, particularly those located in the pyloric or cardiac region, stenosis occasionally occurs after scarring of the ulcer. Stenosis after gastric ESD has been reported to occur at a rate of 1.9–2.5 % [7, 8]. Resection larger than 3/4 of the circumferential extent and longitudinal extent larger than 5 cm in length are reported to be risk factors for gastric stenosis after ESD [7–9]. Endoscopic dilation (ED) is applied when stenosis causes clinical gastric outlet obstruction. However, ED is also
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associated with risks of clinically important adverse events, such as bleeding and perforation [7–10]. Previous studies have reported the efficacy of ED for benign stenosis [11–15]. The incidence of adverse events associated with ED performed for anastomotic stenosis after gastrectomy has been reported to be 0 % per patient for bleeding, and \4.9 % per patient and 2.2 % per procedure for perforation [11–15]. However, little is known about the incidence of adverse events associated with ED for stenosis caused by gastric ESD. The aims of this study were to determine the incidence and risk of bleeding and perforation associated with ED for gastric stenosis after ESD.
Materials and methods From September 2002 to December 2012, among 3162 gastric ESD cases, a total of 64 patients who underwent ED for stenosis after gastric ESD in our hospital were enrolled in the present study. The indications of ESD in our hospital are patients with EGC who meet the Japanese EGC criteria for ER [3]. Among these patients, the medical records were retrospectively assessed for the following factors: patientrelated factors, such as age, sex and use of antithrombotics; ESD-related factors, such as location, circumferential extent of the mucosal defect and diameter of the specimen; and ED-related factors, such as the number of procedures, period from ESD to starting ED, treatment duration and adverse events associated with ED. Because ED is considered a high-risk procedure for bleeding in the Japanese guidelines [16], antithrombotics were generally discontinued for a minimum of 3–7 days before ED. Indications of ED were determined as patients who exhibited symptoms of stenosis, those for whom a generalpurpose endoscope (GIF-H260, caliber 9.8 mm; Olympus, Tokyo, Japan) could not pass through stenosis and those at a risk of developing stenosis because of resection of larger than 3/4 of the circumferential extent [7–9]. ED was performed with balloon dilation using a through-the-scope tool (CRETM Wire-guided Balloon Dilators; Boston Scientific Corporation, Marlborough, MA, USA). The size of the tool was determined according to the severity of stenosis, and ED was repeatedly performed until stenosis was cleared. After each ED procedure, the dilated site was carefully examined for signs of bleeding, mucosal tear, or perforation and whether the endoscope could pass through stenosis. If there were any areas with suspected perforation, abdominal radiography or computed tomography (CT) was performed to check for the presence of abdominal free air. Patients were carefully observed for at least 1 h in the recovery room, and liquids were allowed 2 h after the procedure.
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Adverse events were evaluated after each ED procedure. Bleeding determined as apparent hematemesis or melena was treated by emergency endoscopy. Perforation was considered as deep mucosal tears with abdominal free air. All statistical analyses were performed using Stata SE statistical software for Windows (version 10.1; StataCorp LP, College Station, TX, USA). This retrospective study was approved by the institutional review board of our hospital (26-J60-26-1-3).
Results Characteristics of patients and factors related to ESD and ED are shown in Table 1. Of 64 patients included in analysis, 46 were men and 18 were women, with a median age of 75 years (range 46–90 years). Among them, 19 patients (30 %) had a history of daily usage of antithrombotics. The lower stomach was the most common location of stenosis after ESD (57.8 %, 37/64). The mucosal defect was larger than 3/4 of the circumferential extent in 46 patients (71.9 %), and the median diameter of the resected specimen was 66 mm (range 27–147 mm). A total of 342 ED procedures were performed with a median of four per patient (range 1–25 procedures). The first ED procedure was performed at a median of 29 days (range 2–91 days) after ESD, and the median treatment duration was 30 days (range 1–282 days). The rates of adverse events associated with ED are shown in Table 2. The incidence of bleeding was 3.1 % (2/ 64) per patient and 0.6 % (2/342) per procedure. One case of bleeding occurred in an 82-year-old male who underwent a second ED procedure in the lesser curvature of the gastric cardia with a mucosal defect of 1/2–3/4 of the circumferential extent. This patient was on warfarin therapy for atrial fibrillation, which was discontinued only 1 day before ED and was restarted the day after ED. Three days after the ED procedure, he was admitted to our hospital for melena. Laboratory data showed a decrease in hemoglobin level from 14.5 to 8.7 g/dL and a prothrombin time and international normalized ratio of 23.6 s and 2.25, respectively. Emergency endoscopy revealed bleeding which was stopped by coagulation, and blood transfusion was performed. A second case of bleeding occurred in the lower stomach with a mucosal defect of 3/4-semicircular circumference in a 72-year-old female who did not take daily antithrombotics. Bleeding occurred during the second ED procedure, which was performed 70 days after ESD. Emergency endoscopy confirmed bleeding from the dilated site, which was stopped by coagulation. The incidence of perforation was 7.8 % (5/64) per patient and 1.5 % (5/342) per procedure. Details of the five perforation cases are shown in Table 3. All five
Surg Endosc Table 1 Characteristics of 64 patients who underwent endoscopic dilation after gastric ESD
Age in years [median (range)]
75 (46–90)
Sex (male:female)
46:18
Use of antithrombotics [% (n)]
30 % (19/64)
Use of steroids [% (n)] Location of lesion resected by ESD [% (n)]
Circumferential extent of mucosal defect [% (n)]
U
22 % (14/64) 37.5 % (24/64)
M
4.7 % (3/64)
L
57.8 % (37/64)
\1/2
6.2 % (4/64)
1/2–3/4
21.9 % (14/64)
[3/4-semicircular
62.5 % (40/64)
Whole circular
9.4 % (6/64)
Diameter of mucosal resection [median (range), mm] Number of ED procedures
66 (27–147) Total
342
per patient [median (range)]
4 (1–25)
Period from ESD to first ED [median (range), days]
28 (5–90)
Duration of ED [median (range), days]
30.5 (1–282)
U upper stomach, M middle stomach, L lower stomach, ED endoscopic dilation, ESD endoscopic submucosal dissection
Table 2 Adverse events associated with ED after gastric ESD
Per patient (n = 64) (%)
Per procedure (n = 342) (%)
Bleeding (n = 2)
3.1
0.6
Blood transfusion (n = 1)
1.6
0.3
7.8 10.9
1.5 2.0
Perforation (n = 5)a Hospitalization (n = 7)
ED endoscopic dilation, ESD endoscopic submucosal dissection a
Two cases underwent emergency surgery
perforations occurred in the lower part of the stomach. The size of the mucosal defect in each of these patients was larger than 3/4 of the circumferential extent. Perforation occurred at a median of three ED procedures (range 2–5 procedures), a median of 17 days (range 5–21 days) after starting ED and a median of 43 days (range 29–63 days) after ESD. Among these patients, two were considered inappropriate for nonoperative therapy and, therefore, underwent emergency surgery (Fig. 1). Among the three
patients who had improvement in symptoms by nonoperative therapy, one received additional ED and another underwent surgery for refractory stenosis. Of all 64 patients, seven (10.9 %) required hospitalization for adverse events associated with ED (two cases of bleeding and five of perforation). There were no other adverse events associated with the ED procedure. There were no significant risk factors related to perforation among the patient- or ESD-related factors (Table 4).
Table 3 Details of perforation related to endoscopic dilation for stenosis after ESD Sex
Age
Location
Circumferential extent
M
70
L
3/4-semicircular
M
46
L
F F
81 76
L L
M
88
L
Resection size (mm)
Initiation of ED (day)
Day of perforation (day)
Number of ED at perforation
Emergent surgery/ nonoperative therapy
80
23
40
3
Nonoperativea
3/4-semicircular
130
36
63
5
Nonoperative
3/4-semicircular 3/4-semicircular
35 76
15 38
29 43
3 2
Surgery Nonoperative
3/4-semicircular
66
26
44
5
Surgery
M male, F female, L lower stomach, ESD endoscopic submucosal dissection, ED endoscopic dilation a
Recovered by nonoperative therapy, although underwent surgery for refractory stenosis
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Surg Endosc Fig. 1 Case of perforation caused by endoscopic dilation for stenosis after gastric endoscopic submucosal dissection (ESD), which was treated by emergency surgery: A A semicircular ulcer was created after ESD of two lesions in the lower stomach. B Stenosis occurred 16 days after ESD. C Perforation occurred after the third endoscopic balloon dilation performed 29 days after ESD. D Emergency surgery was performed for gastric perforation. Resected gastric specimen showed the perforation, which was recognized in the bed of the mucosal defect of ESD
There was only one post-ESD bleeding episode among the perforation cases of ED, which was successfully treated by endoscopic hemostasis. Thus, there was no relation between adverse events at the time of ESD and those of ED (ESD perforation: p = 0.43, post-ESD bleeding: p = 0.41). However, all instances of perforation occurred in the lower part of the stomach. The median duration of ED treatment among cases with and without perforation was 17 days (range 14–50 days) and 34 days (range 1–282 days), respectively (p = 0.49).
Discussion In the present study, we evaluated the incidence of adverse events associated with ED for gastric stenosis caused by ESD among a relatively large number of patients. Ulcer scars after ESD are composed of fibrotic tissues covered by a thin layer of regenerative mucosa [5]. Anatomically, stenosis caused by scarring after ESD differs from anastomotic strictures after gastrectomy, in which all layers of the gastric wall are maintained. We assumed that ED for stenosis after ESD would increase the risk of perforation due to the thinness of the gastric wall. Therefore, we focused on the incidence and risks of adverse events associated with ED for stenosis after gastric ESD.
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The stenosis after gastric ESD occurred in 64 cases out of 3,164 gastric ESD cases, with a rate of 2.02 %. This rate was almost as same as previous reports of 1.9–2.5 % [7, 8]. The incidence of bleeding associated with ED in the present study was 3.1 % per patient and 0.6 % per procedure. Previous studies have reported a bleeding rate of 0–11.1 % per patient for benign stenosis (peptic ulcer, 0 %; corrosive, 0–11.1 %; chronic pancreatitis, 0 %; postgastrectomy, 4.2 %) and 2.0 % per procedure for anastomotic stricture after gastrectomy (Table 5) [11–15, 17–21]. Regarding ED for stenosis after gastric ESD, Coda et al. [9] reported a bleeding rate of 0 % per patient in a case study of 15 patients. Together with our results, the risk of bleeding associated with ED for stenosis caused by ESD compared with other benign causes seems to be similar. No previous study has specifically evaluated the risk of bleeding associated with ED in patients on antithrombotic therapy. Therefore, the issue of cessation of antithrombotic therapy during ED in patients routinely receiving these drugs has not been fully resolved. The current Japanese guidelines rank ED as a high-risk procedure for bleeding [16]. Similarly, the American [22] and British [23] guidelines propose ED as a high-risk procedure for bleeding, whereas it is considered as a low-risk procedure by the European guidelines [24]. The results of the present study showed that the overall risk of bleeding associated with ED
Surg Endosc Table 4 Perforation risk of ED after gastric ESD Perforation? (n = 5)
Perforation- (n = 337)
P value
Age in years [median (range)]
76 (46–88)
76 (46–90)
0.99b
Sex (male:female)
3:2
233:103
0.65a
Daily usage of antithrombotics
2
118
0.82a
Use of steroid
0
96
0.16a
U
0
102
0.09b
M
0
25
L
5
210
\1/2
0
9
1/2–3/4
0
43
[3/4-semicircular
5
240
Whole circular
0 76 (35–130)
45 73 (27–147)
Location
Circumferential extent of mucosal defect
Diameter of resection median (range), mm]
0.92b
0.88b
ESD perforation
0
38
0.43
Post-ESD bleeding
1
31
0.41
Number of ED procedure [median (range)]
5 (3–7)
4 (1–25)
0.67b
Period from ESD to first ED [median (range), days]
26 (15–38)
28 (5–90)
0.79b
Duration of ED [median (range), days]
17 (14–50)
34 (1–282)
0.49b
ED endoscopic dilation, ESD endoscopic submucosal dissection, U upper stomach, M middle stomach, L lower stomach a
Chi-squared test
b
Wilcoxon rank-sum test
was very low with intermittent cessation of antithrombotics, in accordance with the current guidelines. On the other hand, one case with incomplete cessation of warfarin presented delayed bleeding that required blood transfusion. Further studies are needed to clarify optimal management strategies during the periprocedural period of ED. When repetitive ED is required, as shown by a median number of four ED procedures required per patient in this study, an extended duration of antithrombotic cessation may increase the risk of thromboembolic events in susceptible patients. The incidence of perforation in this study was 7.8 % per patient and 1.5 % per procedure, while the perforation rate of ED in other reports was 0–27.8 % per patient for benign stenosis (peptic ulcer, 0–9.1 %; corrosive, 0–27.8 %; chronic pancreatitis, 0 %; anastomotic stricture after gastrectomy, 0–4.9 %) [11–15, 17–21, 25]. Regarding ED for stenosis after gastric ESD, previous studies with a small number of cases reported a rate of 0–50 % per patient (Table 5) [7, 9, 10]. In the present study, which included the largest number of cases to date, we found that the risk of perforation caused by ED for stenosis due to ESD was similar to or lower than that of benign causes. All five cases of perforation in this study occurred in patients who received B5 ED procedures, and all were located in the lower stomach. Interestingly, previous reports of perforation among ED for stenosis after ESD were also in the lower part of the stomach [7, 10]. Although the location of ED
was not a significant risk factor for perforation, the ED procedure itself was rather difficult to perform in the lower stomach compared with that in the upper portion due to the gastric curvature. In addition, among cases with stenosis in the lower part of the stomach, there was often considerable gastric residue complicating the ED procedure. In two of five perforation cases, emergency surgery was performed for fear of leakage of gastric residue. An 18- to 20-mm-diameter balloon was used in four of the five perforation cases, and a 15- to 18-mm-diameter balloon was used in one case. The same size of the balloon was used along the same line; however, the pressure of the balloon dilator was different at each procedure. The pressure was usually set at the minimum at the first procedure and gradually increased along the same line. Three perforation cases using an 18- to 20-mm balloon occurred with a maximum pressure of 6 mmHg (20 mm). Coda et al. [9] reported no complication using a 15- to 18–mm-diameter or an 18- to 20-mm-diameter balloon, whereas Tsunada et al. [10] reported two cases of perforation using a 12- to 15-mm-diameter balloon, and Iizuka et al. [7] reported one case of perforation using a 15- to 18-mm-diameter balloon. Therefore, the optimum size of balloon is not clarified at present. However, using larger balloon dilators such as 20 mm diameter or performing dilation with the maximum pressure might become a risk of perforation.
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Surg Endosc Table 5 Incidence of adverse events associated with endoscopic dilation Cause of stenosis
Author
Bleeding Per patient
Benign Anastomotic stricture
Peptic ulcer
Corrosive
Crohn’s disease Chronic pancreatitis ESD
ESD
Perforation Per procedure
Per patient
Per procedure
Lau [26]
1.9 % (1/54)
1.4 % (1/73)
11.1 % (6/54)
8.2 % (6/73)
Lam [27]
–
–
6.1 % (2/33)
–
Solt [17]
4.2 % (1/24)
2.0 % (1/49)
0 % (0/24)
0 % (0/49)
Kim [11]
0 % (0/17)
0 % (0/19)
0 % (0/17)
0 % (0/19)
Ahmad [12]
0 % (0/14)
0 % (0/23)
0 % (0/14)
0 % (0/23)
Go [13]
–
–
2.6 % (1/38)
–
Ukleja [14] Frutos [15]
– 0 % (0/23)
– –
4.9 % (3/61) 0 % (0/23)
2.2 % (3/128) –
Solt [17]
0 % (0/30)
0 % (0/57)
3.3 % (1/30)
1.8 % (1/57)
Kochhar [19]
0 % (0/11)
–
0 % (0/11)
–
Rana [21]
0 % (0/11)
–
9.1 % (1/11)
–
Solt [17]
0 % (017)
0 % (0/66)
5.9 (1/17)
1.5 % (1/66)
Chiu [18]
11.1 % (2/18)
–
27.8 % (5/18)
–
Kochhar [19]
0 % (0/8)
–
0 % (0/8)
–
Kochhar [20]
0 % (0/41)
–
2.4 % (1/41)
–
Rana [21]
0 % (0/7)
–
14.3 % (1/7)
–
Solt [17]
0 % (0/1)
0 % (0/5)
0 % (0/1)
0 % (0/5)
Kochhar [19]
0 % (0/4)
–
0 % (0/4)
–
Rana [21]
0 % (0/4)
–
0 % (0/4)
–
Coda [9]
0 % (0/15)
–
0 % (0/15)
–
Tsunada [10]
–
–
50 % (2/4)
–
Iizuka [7] Present study
– 3.1 % (2/64)
– 0.6 (2/342)
17 % (1/6) 7.8 % (5/64)
– 1.5 % (5/342)
– not mentioned, ESD endoscopic submucosal dissection
All of the perforation holes were located in the bed of ESD ulcer near the most stenotic area. When the dilation balloon is dilated, the narrowest area will receive the strongest pressure. Even though the ulcer is in the process of healing, the area is thought to be fragile, as it lacks the mucosal and submucosal layer. Therefore, we consider that to avoid overpressure to the stenotic area, choosing smaller diameter of balloon is important. The limitations of this study include its retrospective design in a single institute. The timing of starting ED in patients at a risk of stenosis was decided by the doctors in charge. Nonetheless, these data should prove quite helpful because we enrolled a relatively large number of cases to focus on adverse events associated with ED. In addition, we included only patients who underwent ED for stenosis caused by gastric ESD. In conclusion, the risk of bleeding was very low among patients receiving ED for stenosis after gastric ESD. The risk of bleeding without cessation of antithrombotic agents should be confirmed by a prospective study in the near future. Although not significant, ED in the lower stomach presents a substantial risk of perforation.
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Disclosures Y Kishida, N Kakushima, N Kawata, M Tanaka, K Takizawa, K Imai, K Hotta, H Matsubayashi and H Ono have no conflict of interest or financial interests to declare in association with this study.
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