|Year : 2014 | Volume
| Issue : 6 | Page : 52-55
Submucosal tunneling endoscopic resection for upper gastrointestinal multiple submucosal tumors originating from the muscular propria layer: A feasibility study
C Zhang, JW Hu, T Chen, PH Zhou, YS Zhong, YQ Zhang, WF Chen, QL Li, LQ Yao, MD Xu
Endoscopy Center and Endoscopy Research Institute, Zhongshan Hospital, Fudan University, Shanghai 200032, China
|Date of Web Publication||24-Feb-2015|
Prof. M D Xu
Endoscopy Center and Endoscopy Research Institute, Zhongshan Hospital, Fudan University, Shanghai 200032
Source of Support: None, Conflict of Interest: None
Background and Aims: In recent years, submucosal tunneling endoscopic resection (STER) was applied more and more often for single gastrointestinal (GI) submucosal tumor (SMT). However, little is known about this technique for treating multiple SMTs in GI tract. In the present study, we investigated the feasibility and outcome of STER for upper GI multiple SMTs originating from the muscularis propria (MP) layer.Patients and Methods: A feasibility study was carried out including a consecutive cohort of 23 patients with multiple SMTs from MP layer in esophagus, cardia, and upper corpus who were treated by STER from June 2011 to June 2014. Clinicopathological, demographic, and endoscopic data were collected and analyzed. Results: All of the 49 SMTs were resected completely by STER technique. Furthermore, only one tunnel was built for multiple SMTs of each patient in this study. En bloc resection was achieved in all 49 tumors. The median size of all the resected tumors was 1.5 cm (range 0.8-3.5 cm). The pathological results showed that all the tumors were leiomyoma, and the margins of the resected specimens were negative. The median procedure time was 40 min (range: 20-75 min). Gas-related complications were of the main complications, the rates of subcutaneous emphysema and pneumomediastinum, pneumothorax, and pneumoperitoneum were 13.0%, 8.7% and 4.3%. Another common complication was thoracic effusion that occurred in 2 cases (8.7%), among which only 1 case (4.3%) with low-grade fever got the drainage. Delayed bleeding, esophageal fistula or hematocele, and infection in tunnel were not detected after the operation there were no treatment-related deaths. The median hospital stay was 4 days (range, 2-9 days). No residual or recurrent lesion was found during the follow-up period (median 18, ranging 3-36 months). Conclusion: Submucosal tunneling endoscopic resection is a safe and efficient technique for treating multiple esophageal SMTs originating from MP layer, which can avoid patients suffering repeated resections.
Keywords: Multiple, submucosal tumor, submucosal tunneling endoscopic resection
|How to cite this article:|
Zhang C, Hu J W, Chen T, Zhou P H, Zhong Y S, Zhang Y Q, Chen W F, Li Q L, Yao L Q, Xu M D. Submucosal tunneling endoscopic resection for upper gastrointestinal multiple submucosal tumors originating from the muscular propria layer: A feasibility study. Indian J Cancer 2014;51, Suppl S2:52-5
|How to cite this URL:|
Zhang C, Hu J W, Chen T, Zhou P H, Zhong Y S, Zhang Y Q, Chen W F, Li Q L, Yao L Q, Xu M D. Submucosal tunneling endoscopic resection for upper gastrointestinal multiple submucosal tumors originating from the muscular propria layer: A feasibility study. Indian J Cancer [serial online] 2014 [cited 2022 Jun 29];51, Suppl S2:52-5. Available from: https://www.indianjcancer.com/text.asp?2014/51/6/52/151989
C Zhang FNx01, J W Hu FNx01
FNx01Drs. Zhang Chen and Hu Jianwei contributed equally to this work
| » Introduction|| |
With the improvement of endoscopic diagnosis and the widespread application of endoscopic ultrasonography (EUS), more small submucosal tumors (SMTs) are detected in gastrointestinal (GI) tract. Sometimes, multiple SMTs could be even detected in GI tract of one patient. Previously, conventional endoscopic resections for those SMTs from the muscularis propria (MP) layer were used limitedly, mainly because of the high rate of complications. Inspired by natural orifice transluminal endoscopic surgery (NOTES) and peroral endoscopic myotomy (POEM), we developed a new technique, submucosal tunneling endoscopic resection (STER), for the treatment of upper GI SMTs originating from the MP layer.  Our preliminary study indicated that STER was a safe and effective technique that can keep the integrity of esophageal mucosa and provide a high rate of complete resection.  In recent years, STER was applied more and more often for single GI SMT. However, little is known about this technique for treating multiple SMTs in GI tract. Recently, we pioneered in using one tunnel for resecting multiple SMTs originating from the MP layer locating in esophagus, cardia, and upper corpus. Here, we reported the feasibility and outcome of STER for the multiple SMTs.
| » Patients and Methods|| |
Twenty-three consecutive patients with multiple SMTs originating from the MP layer in upper GI tract were treated by STER in Endoscopy Center and Endoscopy Research Institute, Zhongshan Hospital, Fudan University between June 2011 and June 2014. This study was approved by the Institutional Review Board, and written informed consent was signed by every patient, who had been told possible procedure-related benefits and risks (including possible complications and corresponding managements).
Endoscopic equipment and accessories
Routine EUS examination (high-frequency miniprobe, UM-2R, 12 MHz, UM-3R, 20 MHz; Olympus Optical Co., Ltd., Tokyo, Japan) was done before STER to confirm that the tumors originated from the MP. A standard, single accessory channel gastroscope (GIF-Q260J; Olympus) was used during the procedure. Occasionally, a dual-channel gastroscope (GIF-2T240; Olympus) was used. A transparent cap (D-201-11802; Olympus) was attached to the front of the endoscope. Additional equipment and accessories included a high-frequency generator (ICC-200; ERBE, Tübingen, Germany), an argon plasma coagulation unit (APC300; ERBE), an injection needle (NM-4 L-1; Olympus), a hook knife (KD-620 LR; Olympus), an insulated-tip knife (KD-611 L, IT2; Olympus), a hybrid knife (ERBE), grasping forceps (FG-8U-1; Olympus), a snare (SD-230U-20; Olympus), Coagrasper (FD-410 LR, Olympus), and hemostatic clips (HX-600-135; Olympus). A carbon dioxide insufflator (Olympus) was used for carbon dioxide gas insufflation during the procedure. A mixed solution of 100 ml normal saline solution, 2-3 ml indigo carmine, and 1 ml epinephrine was prepared for submucosal injection.
A transparent cap was attached to the front of the endoscope. All procedures were carried out under tracheal intubation and general anesthesia. Patients were administered antibiotics intravenously to prevent infection half an hour before the operation.
Build the submucosal tunnel
The precondition of STER resecting multiple tumors simultaneously was that they located in a longitudinal line of esophagus, cardia, or/and upper corpus and could be exposed in one tunnel. The procedure was performed as following steps: (1) Confirmed the location of all the tumors and selected a proper direction of the tunnel to expose all the tumors in the tunnel simultaneously; (2) Built a submucosal tunnel and exposed all the tumor. A fluid cushion was made by injection needle at 3-5 cm proximal to the first tumor. A 2 cm longitudinal mucosal incision was made by hybrid knife or Hook knife at the esophageal mucosa as the entry point. With the help of cap, separated mucosa from muscular layer preliminarily at tunnel entrance and then pushed the end of the endoscope into the entrance to go on separating the two layers until the submucosal tunnel was beyond the farthest tumor 1-2 cm. Hereto, all the tumors were exposed and enough work space for resections were acquired; (3) when the tumors did not locate in a strict longitudinal line, the tunnel was built as wide as possible, so that satisfactory endoscopic view and enough working space could be made for resection of all the tumors. Mucosal damage should be avoided carefully during the STER procedure.
Resect the tumors
The tumor near to the tunnel entrance was resected first, the farther one, and then the farthest one. The tumors were separated from surrounding muscular layer and resected under direct endoscopic view using an insulated-tip knife, hook knife or hybrid knife. The mobilized SMT was removed out of the tunnel using a snare or basket through the mucosal entry. During the procedure, safe and complete resection of all the tumors, without interruption of the tumor capsule, was of highest priority. Unnecessary damage to the esophageal adventitia was cautiously avoided. After resection all of the tumors, the submucosal tunnel was lavaged with normal saline if the esophageal adventitia or gastric serosa was intact. All the hemorrhagic focus and small visible vessels were disposed with coagrasper. The endoscope was withdrawn from the submucosal tunnel. Several metal clips were employed to close the mucosal incision [Figure 1].
|Figure 1: Key procedures of submucosal tunneling endoscopic resection. (a) Three submucosal tumors located in lower esophagus under endoscopic view. (b) A submucosal tunnel was created with a hybrid knife, and the mucosal damage was carefully avoided. (c) Precoagulation was made to visible vessels. (d) The tunnel was made beyond the lowest tumor since they near to each other, and all the tumors were exposed. (e) Separated the tumor carefully from the surrounding muscularis propria layer one by one. (f) All the tumors were resected without mucosal damage and perforation. (g) Closed the tunnel entrance completely with several metal clips. (h) The size of the tumors were 0.3 cm × 0.4 cm, 0.6 cm × 1.0 cm and 0.8 cm × 1.5 cm respectively|
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All the patients were observed if there were symptoms such as chest distress, dyspnea, cyanosis, stomachache, and abdominal distension, or signs of peritonitis. PPIs, preventive antibiotics, and hemostatic agents were applied routinely. The patients fasted at the 1 st day after operation, and were allowed to take fluids the 2 nd day only when there was no fever, stomachache, chest distress or dyspnea and no pleural effusion or seroperitoneum revealed in ultrasonography or computed tomography. All patients were asked for taking reexaminations, mainly including gastroscopy and EUS, in the 3 rd , 6 th and 12 th month after the operation, to observe wound healing and whether there was any residual or recurrent lesion.
| » Results|| |
Twenty-three consecutive patients were included in this study. The mean age of the patients was 52.26 ± 8.61 years (median 52-year, range 26-72 years) and the male:female ratio was 3.6:1 (18/5). The list showed originating location of the multiple tumors. Among all 23 patients, there were 20 with simultaneous 2 tumors, including 8 with 2 tumors in middle esophagus, 6 with 2 tumors in lower esophagus, 4 with 1 in lower esophagus while another in cardia, 2 with 1 in lower esophagus while another in lesser curvature of upper stomach body. The rest 3 cases had 3 simultaneous tumors, including one case with 2 tumors in esophagus and 1 in cardia, 2 cases with 3 tumors in the middle and lower esophagus. The detailed location of tumors is shown in [Table 1]. During the operations, 11 tumors were found originating from superficial MP layer while 38 were found from deep MP layer. In addition, 30 SMTs were round shape and the rest 19 tumors were irregular. STER was performed successfully in all of the 23 patients with a single tunnel for each patient. En bloc resection was achieved in all 49 tumors. The median size (the largest diameter) of all the resected tumors was 1.5 cm (range 0.8-3.5 cm). The pathological results showed that all the tumors were leiomyoma, and the margins of the resected specimens were negative Air insufflation was employed in 9 cases while CO 2 was used in 14 cases. The median procedure time was 40 min (range 20-75 min) [Table 1].
|Table 1: Clinicopathological characteristics of 23 patients with multiple SMTs in upper GI tract|
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Subcutaneous emphysema and pneumomediastinum occurred in 3 patients (13.0%). pneumothorax occurred in 2 patients (8.7%), pneumoperitoneum appeared in 1 patient (4.3%). Another common complication was thoracic effusion that occurred in 2 cases (8.7%), among which only 1 cases (4.3%) with low-grade fever got the drainage Emphysema in 4 patients insufflated by CO 2 was resolved spontaneously in 1-2 h, but 5-10 days were needed for gas absorption in 2 patients insufflated by air. All of the patients with those complications were cured by conservative treatment, mainly including fasting, antibiotics, and fluid infusion. Delayed bleeding, esophageal fistula or hematocele, and infection in tunnel were not detected after the operation there were no treatment-related deaths. The median hospital stay was 4 days (range, 2-9 days). No residual or recurrent lesion was found during the follow-up period (median 18, ranging 3-36 months).
During the follow-up period of 18 months (median, range 3-36 months), wound healing of all cases was satisfied, and no residual or recurrent lesions were found.
| » Discussion|| |
Submucosal tumor represents protuberant lesions or bumps covered with intact mucosa,  and it is the second most frequently found in the esophagus.  Though the major tumor in the esophagus is leiomyoma,  which does not represent a presage of a leiomyosarcoma in most cases, ,, there are some potentially malignant tumors in the esophagus as well, like gastrointestinal stromal tumors (GISTs), of which about 20-30% display malignant behavior. , According to recent guidelines from the National Comprehensive Cancer Network, all GISTs have malignant potential and all GISTs larger than 2 cm should be resected; the treatment options for incidental tumors smaller than 2 cm are resection or surveillance. ,,
In the past, open or laparoscopic surgery was performed to remove SMT even without an accurate diagnosis before treatment. , Open surgery results in large surgical trauma, delayed postoperative recovery, and a certain percentage of operation-related complications. Better than open surgery, laparoscopic surgery for SMTs has quicker recovery, higher quality of life after operation and shorter hospital stay. However, SMTs protruding into the lumen are often difficult to identify without the assistance of a gastroscope during the procedure. Laparoscopic wedge resection is still an invasive procedure and is relatively expensive. Some conventional endoscopic resections, such as endoscopic submucosal dissection (ESD), endoscopic submucosal excavation, and endoscopic full-thickness resection, are used recently to resect SMTs originating from the MP layer as a minimally invasive surgery, ,, but these technique may result in GI fistula and secondary infection in some cases, because of complete sealing of the perforation is sometimes difficult to achieve through endoscopic repair. Inspired by NOTES and POEM, Xu et al.  invented a new endoscopic technique named STER for those SMTs and acquired a satisfactory outcome.
Since STER allowed a high en bloc and complete resection rate, and considered to be flexible, the technique became widely acceptable. ,,,, However, for multiple SMTs, repeated resections by STER procedure in a different tunnel seems to be a time-consuming effort and make patients suffer too much. In this study, we first focused on using STER technique to resect upper GI multiple SMTs originating from the MP layer. STER was performed successfully in all of the 23 patients with a single tunnel for each patient, and the tumor size ranged 0.8-3.5 cm (median 1.5 cm). The en bloc and complete resection rate was both 100%. The pathological results showed that all the tumors were leiomyoma, and the margins of the resected specimens were negative.
The major superiority of STER is to keep the integrity of GI tract during the operation. No perforation was found using STER to treat single SMT in the previous study , the main complication of STER was gas-related complication. ,, The results of this study showed that, Subcutaneous emphysema and pneumomediastinum occurred in 3 patients (13.0%). pneumothorax occurred in 2 patients (8.7%), pneumoperitoneum appeared in 1 patient (4.3%). CO 2 was considered to diffuse and be absorbed quickly in the human body.  Maeda et al.  reported that insufflation with CO 2 , rather than air, during esophageal ESD, significantly reduced postprocedural mediastinal emphysema. In all the cases of this study, 9 employed air insufflation while 14 employed CO 2 insufflation. Gas-related complication rate in air insufflation group was 44.4% (4/9) while the rate was 14.3% (2/14) in CO 2 group. Therefore, CO 2 insufflation is recommended to reduce gas-related complications and to alleviate relevant symptoms. Gas-related complications could be avoided by following points from our experience: (1) Be careful to retain the integrity of esophageal adventitia during the procedure. (2) The tunnel should be created and extended strictly along the MP layer rather than the mucosal layer. (3) Precoagulation of visible vessels could reduce the incidence of bleeding and help to gain a clear view. Another complication of STER is pleural effusion. A reported rate of postoperative pleural effusion combined with low fever of STER for single SMT was 3.5%, and that rate of STER for multiple SMTs in the present study was 4.3% (1/23).
Though complications of STER for multiple SMTs were unavoidable, the complications and their incidence rate mentioned above were limited and low. What is more, one tunnel STER procedure for multiple SMTs rather than repeated procedures could avoid repeat complications and make patients suffer less so that the prognosis might be better. All the complications mentioned above was disappeared with conservative treatments, mainly including fasting, antibiotics, fluid infusion, after a few days. No delayed bleeding, esophageal fistula or hematocele, and infection in tunnel were found after the operation. The median hospital stay was 4 days (range, 2-9 days).
One of the limitations of the present study is the potential selection bias because our institute is in a tertiary referral center and is the main endoscopy center in China with many experienced endoscopists. So our results may not represent that in other hospitals or countries. What is more, the sample size of the study is small and follow-up period is relatively short. A randomized controlled trial needs to be studied further to verify the long-term follow-up result of STER for treating multiple SMTs originating from the MP layer.
In summary, according to this 3-year study, STER, as a novel endoscopic therapeutic resection technique, appears to be a feasible, safe and effective method for treating multiple SMTs originating from the MP layer in the esophagus.
| » References|| |
Xu MD, Cai MY, Zhou PH, Qin XY, Zhong YS, Chen WF, et al.
Submucosal tunneling endoscopic resection: A new technique for treating upper GI submucosal tumors originating from the muscularis propria layer (with videos). Gastrointest Endosc 2012;75:195-9.
Wiech T, Walch A, Werner M. Histopathological classification of nonneoplastic and neoplastic gastrointestinal submucosal lesions. Endoscopy 2005;37:630-4.
Nishida T, Kawai N, Yamaguchi S, Nishida Y. Submucosal tumors: Comprehensive guide for the diagnosis and therapy of gastrointestinal submucosal tumors. Dig Endosc 2013;25:479-89.
Davis GB, Blanchard DK, Hatch GF 3 rd
, Wertheimer-Hatch L, Hatch KF, Foster RS Jr, et al.
Tumors of the stomach. World J Surg 2000;24:412-20.
Lee YT. Leiomyosarcoma of the gastro-intestinal tract: General pattern of metastasis and recurrence. Cancer Treat Rev 1983;10:91-101.
Hatch GF 3 rd
, Wertheimer-Hatch L, Hatch KF, Davis GB, Blanchard DK, Foster RS Jr, et al.
Tumors of the esophagus. World J Surg 2000;24:401-11.
Kida M, Araki M, Miyazawa S, Ikeda H, Takezawa M, Kikuchi H, et al
. Comparison of diagnostic accuracy of endoscopic ultrasound-guided fine-needle aspiration with 22- and 25-gauge needles in the same patients. J Interv Gastroenterol 2011;1:102-107.
Nowain A, Bhakta H, Pais S, Kanel G, Verma S. Gastrointestinal stromal tumors: Clinical profile, pathogenesis, treatment strategies and prognosis. J Gastroenterol Hepatol 2005;20:818-24.
Demetri GD, von Mehren M, Antonescu CR, DeMatteo RP, Ganjoo KN, Maki RG, et al.
NCCN Task Force report: Update on the management of patients with gastrointestinal stromal tumors. J Natl Compr Canc Netw 2010;8 Suppl 2:S1-41.
Walsh RM, Heniford BT. Laparoendoscopic treatment of gastric stromal tumors. Semin Laparosc Surg 2001;8:189-94.
Chiu PW, Wong TC, Teoh AY, To KF, Liu SY, Wong SK, Chan FK, Ng EK. Recognition of changes in microvascular and microstructural patterns upon magnifying endoscopy predicted the presence of extranodal gastric MALToma. J Interv Gastroenterol 2012;2:3-7.
Zhang Y, Ye LP, Zhu LH, Zhou XB, Mao XL, Ding JX. Endoscopic muscularis excavation for subepithelial tumors of the esophagogastric junction originating from the muscularis propria layer. Dig Dis Sci 2013;58:1335-40.
Huang LY, Cui J, Liu YX, Wu CR, Yi DL. Endoscopic therapy for gastric stromal tumors originating from the muscularis propria. World J Gastroenterol 2012;18:3465-71.
Li QL, Yao LQ, Zhou PH, Xu MD, Chen SY, Zhong YS, et al.
Submucosal tumors of the esophagogastric junction originating from the muscularis propria layer: A large study of endoscopic submucosal dissection (with video). Gastrointest Endosc 2012;75:1153-8.
Bialek A, Wiechowska-Kozlowska A, Pertkiewicz J, Karpinska K, Marlicz W, Milkiewicz P, et al.
Endoscopic submucosal dissection for the treatment of neoplastic lesions in the gastrointestinal tract. World J Gastroenterol 2013;19:1953-61.
Lu J, Jiao T, Zheng M, Lu X. Endoscopic resection of submucosal tumors in muscularis propria: The choice between direct excavation and tunneling resection. Surg Endosc 2014;28:3401-7.
Wang XY, Xu MD, Yao LQ, Zhou PH, Pleskow D, Li QL, et al.
Submucosal tunneling endoscopic resection for submucosal tumors of the esophagogastric junction originating from the muscularis propria layer: A feasibility study (with videos). Surg Endosc 2014;28:1971-7.
Xu M, Wang XY, Zhou PH, Li QL, Zhang Y, Zhong Y, et al.
Endoscopic full-thickness resection of colonic submucosal tumors originating from the muscularis propria: An evolving therapeutic strategy. Endoscopy 2013;45:770-3.
Wang L, Ren W, Zhang Z, Yu J, Li Y, Song Y. Retrospective study of endoscopic submucosal tunnel dissection (ESTD) for surgical resection of esophageal leiomyoma. Surg Endosc 2013;27:4259-66.
Inoue H, Minami H, Kobayashi Y, Sato Y, Kaga M, Suzuki M, et al.
Peroral endoscopic myotomy (POEM) for esophageal achalasia. Endoscopy 2010;42:265-71.
Maeda Y, Hirasawa D, Fujita N, Obana T, Sugawara T, Ohira T, et al.
A pilot study to assess mediastinal emphysema after esophageal endoscopic submucosal dissection with carbon dioxide insufflation. Endoscopy 2012;44:565-71.
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