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ORIGINAL ARTICLE
Year : 2014  |  Volume : 10  |  Issue : 8  |  Page : 281-286

Submucosal tunneling endoscopic resection for the treatment of rectal submucosal tumors originating from the muscular propria layer


Endoscopy Center and Endoscopy Research Institute, Endoscopy Center, Zhongshan Hospital, Fudan University, Shanghai 200032, China

Date of Web Publication17-Feb-2015

Correspondence Address:
Mei-Dong Xu
Endoscopy Center, Zhongshan Hospital of Fudan University, 180 Fenglin Road, Shanghai 200032
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.151533

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 > Abstract 

Objective: The objective was to evaluate the clinical value of submucosal tunneling endoscopic resection (STER) for the treatment of submucosal tumors (SMTs) originating from the muscular propria (MP) in the rectum.
Patients and Methods: The clinicopathological data of 12 cases with rectal SMTs originating from the MP layer performed STER in our center from January 2012 to June 2014 were analyzed retrospectively.
Results: Three males and nine females (M/F, 1/3) were studied in this series. The median age of the patients was 53.5 (range, 41-84) years. The tumors located 5-10 cm from the anal verge. En bloc STER was performed successfully in all of the 12 cases. The median size of resected specimens was 1.4 cm (range 1.0-3.0 cm). The median procedure time was 49.5 min (range 40-70 min). Three patients developed low fever after the operation and were all recovered after receiving intravenous antibiotics. One of these three cases developed mucosa perforation, which was closed immediately with metal clips. One patient developed subcutaneous emphysema in one lower limb, which disappeared with conservative treatments 2 weeks after the STER procedure. The median hospital stays were 3.1 (range 2-8) days. Postoperative pathological outcomes revealed schwannoma in 3 cases, leiomyoma in 2 cases, stromal tumor in 5 cases, and proliferation of collagen fibers nodular degeneration in 2 cases. No lesion residual or recurrence was found during postoperative follow-up of 4-33 months.
Conclusion: STER is a feasible, safe, and effective method for treating SMTs originating from the MP layer in the rectum.

Keywords: Rectal, submucosal tumor, submucosal tunneling endoscopic resection


How to cite this article:
Hu JW, Zhang C, Chen T, Zhou PH, Zhong YS, Zhang YQ, Chen WF, Li QL, Yao LQ, Xu MD. Submucosal tunneling endoscopic resection for the treatment of rectal submucosal tumors originating from the muscular propria layer. J Can Res Ther 2014;10, Suppl S4:281-6

How to cite this URL:
Hu JW, Zhang C, Chen T, Zhou PH, Zhong YS, Zhang YQ, Chen WF, Li QL, Yao LQ, Xu MD. Submucosal tunneling endoscopic resection for the treatment of rectal submucosal tumors originating from the muscular propria layer. J Can Res Ther [serial online] 2014 [cited 2019 Oct 18];10:281-6. Available from: http://www.cancerjournal.net/text.asp?2014/10/8/281/151533


 > Introduction Top


The tunnel endoscopy technique, a novel therapeutic management based on natural orifice transluminal endoscopic surgery (NOTES) and endoscopic submucosal dissection (ESD), developed in recent years. Now, this technique has been applied for treating achalasia of cardia and submucosal tumors (SMTs) originating the muscular propria (MP) layer in upper gastrointestinal (GI) tract, which not only can be comparable to surgery in short-term effects, but also shows unique advantages including safety, minimal invasion, quicker recovery, and shorter hospital stay. Based on the experience in performing submucosal tunneling endoscopic resection (STER) for SMTs originating from the MP layer in upper GI tract, [1] we applied STER technique for treating rectal SMTs originating from the MP layer in 12 cases, and achieved satisfactory outcomes.


 > Patients and methods Top


Patient information

A total of 12 patients with single SMT originating from the MP in the rectum was performed STER in Endoscopy Center and Endoscopy Research Institute, Zhongshan Hospital, Fudan University between January 2012 and June 2014. All SMTs were identified originating from the MP layer by endoscopic ultrasonography (EUS). Three males and nine females were included in the series, and their median age was 53.5 (range 41-84) years. 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

A standard single-accessory-channel colonoscope (PCF-Q260JI, Olympus Corp., Tokyo, Japan) was used during the procedures. EUS system (EU-M30, high-frequency miniprobe, UM-2R, 12 MHz, UM-3R, 20 MHz; Olympus Optical Co. Ltd., Tokyo, Japan) was used to confirm that the tumors originated from the MP layer. A transparent cap (D-201-10704; Olympus) was attached to the front of the colonoscope. Other equipment included an injection needle (NM-200U-0423; Olympus), a hook knife (KD-620UR; Olympus), an insulated tip knife (KD-611L; Olympus), a hybrid knife (ERBE), grasping forceps (FR-44NR-1; Olympus), snares (SD-230U-20; Olympus), hot biopsy forceps (FD-410LR; Olympus), Coagrasper (FD-410LR, Olympus), hemostatic clips (HX-610-135; Olympus), and an argon plasma coagulation unit (APC300; ERBE). A carbon dioxide insufflator (Olympus) was used for carbon dioxide gas insufflator during the procedure. The high-frequency electric generator (VIO 200D; ERBE).

Submucosal tunneling endoscopic resection procedure

Before the procedure, a transparent cap, exceeding the front end of the colonoscope 3 mm, was taped to the front of the colonoscope. All patients were asked to finish bowel preparation according to established principles of bowel preparation for colorectal surgery, and were administered antibiotics intravenously half an hour before the procedure to prevent infections. All cases were performed STER under intravenous anesthesia. STER procedures were as follows referring to the literature. [ 1 ] (1) Finding the tumor and locating the tumor site endoscopically. (2) Creating a submucosal tunnel and exposuring the tumor. Longitudinal mucosal incision was made 2-3 cm proximal to the tumor, and oblique incision was selected if necessary. A fluid cushion was created by injecting 2-3 ml of mixed solution of 100 ml normal saline, 2-3 ml indigo carmine and 1 ml epinephrine into the submucosa. The 1.5-2.0 cm transversal mucosal incision, as the tunnel entrance, was made using a hybrid knife or hook knife, and mucosa was separated preliminarily from the muscular layer there. Then, an endoscope could pass into the tunnel entrance with the help of the transparent cap. A longitudinal tunnel could be created between mucosa and muscular layer by separating submucosa gradually with a hybrid knife or hook knife. The tunnel was made 1-2 cm distal to the tumor to acquire an adequate exposure of the tumor and enough space for resection. Mucosal damage was avoided carefully during creating the tunnel. (3) Resecting the tumor completely under direct endoscopic visualization. Separating muscular layer around the tumor with a hybrid knife, hook knife or IT knife. Completeness of the tumor capsule was ensured, and the tumor was separated from the muscular layer and taken out of the tunnel. (4) Suturing the mucosal incision. After resection of the tumor, hemorrhagic focus and small visible vessels were disposed with coagrasper. Then, the endoscope was withdrawn from the submucosal tunnel, and complete suture of the mucosal incision was made under the endoscope using metal clips [Figure 1].
Figure 1: Key procedures of submucosal tunneling endoscopic resection. (a) The rectal submucosal tumor located 3 cm from the anal verge. (b) Endoscopic ultrasonography revealed that the tumor originated from the muscular propria (MP) layer, its size was 9.2 mm × 6.4 mm. (c) 1.5 cm oblique mucosa incision was made 2 cm from the tumor to the anal side, submucosal tunnel was created between the mucosa and the MP layer. (d) Exposuring the tumor. (e) The tumor was resected completely under direct endoscopic visualization. (f) Taking the tumor out of the tunnel. (g) The resected tumor. (h) Closing the mucosal incision with suturing technique. (i) Postoperative subcutaneous emphysema in the right lower limb. (j-l) No lesion residual or recurrence was found during postoperative follow-up, and only scars can be seen

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Postoperative managements

The patients were kept off food and water routinely, and resumed diet gradually. Observing the patients if there was any signs of subcutaneous emphysema, fever, abdominal pain, abdominal distension, and peritonitis. Preventive antibiotics and hemostatic agents were applied, and stool was softened for patients. After STER procedures, patients were fasted for 1 day. If there were no discomforts including fever, abdominal pain, and abdominal distension, and no computed tomography (CT) confirmed pelvic effusion or retroperitoneal emphysema, patients were given liquid diet on the next day.

Pathological examination

All the tumors resected using STER technique were fixed in formalin and sent to the pathology department. For those tumors which were hard to diagnose using the common approach, we recommended immunohistochemistry for them. The characters of the tumors were described by the pathologists. The lateral and basal resection margins were examined to identify if they were negative.

Evaluation of complete resection

Every resected tumor was collected to confirm if it was complete, and we checked the wound if there was any residual lesion. The result of complete resection was recorded for analysis.

Complications

We usually did preliminary estimate of complications by the operation situation and doing physical examination for the patients during the operation. After the operation, the complaints of the patients and their symptoms and signs could give us clues about complications. When complications were suspected, we did X-ray, B ultrasound, or CT for the patients to make a confirmed diagnosis.

Follow-up

Follow-up colonoscopies and EUS were rechecked on months 3, 6, 12 after the procedures to observe local healing situations and ensure if there was any tumor residual or recurrence. After that, patients were recommended rechecking every 6-12 months according to the actual situations.

Data collection and analysis

All the clinicopathological data of the cases were collected, and which were analyzed using a statistical approach.


 > Results Top


The basic information of demographic, pathologic, and clinical data of the 12 patients with rectal SMTs are shown in [Table 1]. And the detailed information of each patient is shown in [Table 2].
Table 1: Demographic data, clinical and pathologic features, and outcome of treatment in 12 patients undergoing STER for rectal SMTs originating from the MP

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Table 2: Clinicopathologic data of patients with rectal SMTs treated with STER*

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Clinicopathological characteristics

Twelve cases, including 3 males and 9 females (M/F, 1/3), with single rectal SMT, were studied in this series [Table 1]. The median age of the patients was 53.5 (range, 41-84) years. STER procedures were performed successfully in all of the 12 cases. En bloc resection was achieved in one time for all SMTs. The tumors located 5-10 cm away from the anal verge. Among which, 1 located in the intra-peritoneal rectum, and 11 located in the extra-peritoneal rectum. The dividing line of intra- and extra-peritoneal rectum was the peritoneal reflection, which was referred to some surgical books proposing the anatomic reference of the second rectal valve as the location of the anterior peritoneal reflection, and it should be approximately 8 cm from the anal verge. [2],[3] EUS before the operation revealed that 2 tumors (16.7%, 2/12) were originating from the superficial MP, while the rest 10 tumors (83.3%, 10/12) were originating from the deep MP. The maximum diameter of all resected lesions ranged 1.0-3.0 (median, 1.4) cm. The tunnel entrance located 2-3 cm away from the tumor. The length of all tunnels ranged 3-4 cm. Procedure time was 40-70 (median, 49.5) min. Among all 12 cases, 9 were insufflated carbon dioxide during the procedures, while the rest 3 insufflated air.

Postoperative pathological outcomes revealed schwannoma in 3 cases, leiomyoma in 2 cases, stromal tumor in 5 case, and proliferation of collagen fibers nodular degeneration in 2 cases. Resecting margins of all specimens were negative.

Evaluation of resectability and complications

Submucosal tunneling endoscopic resection procedures were performed successfully in all of the 12 cases. En bloc resection was achieved in one time for all SMTs. Minimal bleeding occurred in every case, and all managed successfully with electric coagulation hemostasis endoscopically. No massive hemorrhage or postoperative delayed bleeding developed. Five cases developed fever after the procedures, and maximum body temperature was 38°C. All of them recovered after the treatments of anti-infection. Among those 5 cases, one developed intraoperative mucosal perforation, which was clipped with metal clips. This patient only developed low-grade fever, and no further complications occurred. One patient developed subcutaneous emphysema in one lower extremity, which disappeared with conservative treatments 2 weeks after the procedure [Figure 1]. The length of hospital stays ranged 2-8 (median, 3.1) days.


 > Follow-up results Top


No lesion residual or recurrence was found during postoperative follow-up period ranging 4-33 (median, 22.7) months [Figure 1].


 > Discussion Top


Recently, more and more colorectal SMTs have been discovered than before, with the development of EUS which supports a novel method of diagnosing these "hiding" tumors. EUS could show not only relationship between the lesion and the layer of the GI tract, but also inner structure of the tumor. According to the characteristics of the tumor's inner echo, size, involved layer, the probable histological properties could be estimated. [4 ] In the series, EUS was performed to every patient before the operation. The results revealed that 2 tumors were originating from the superficial MP layer while other 10 tumors were from the deep MP layer. And the results were verified during the operation. Though the echo of the tumors could give us clues to realize their characters, we diagnosed the tumors mainly according to the pathological outcome.

For colorectal SMTs, clinical follow-up observation or surgical operation was applied before because conventional endoscopic trepanned resection or endoscopic resection with ligation for SMTs often lead to bleeding, perforation, tumor residual, and recurrence. [ 5 ] With widespread application of ESD technique, ESD for superficial colorectal SMTs, like neuroendocrine neoplasm, could achieve en bloc resection in one time and have advantages including safety and low occurrence of complications. [ 6],[7] But for SMTs originating from the MP layer, endoscopic full-thickness resection, including the MP layer and the serosa resection, may be required. [ 8 ] Although perforation could be repaired successfully with multiple endoscopic suture methods in most cases, complete closure is hardly achieved using endoscopic suture technique sometimes, and postoperative complications including severe infection, may develop in some cases. Perforation after endoscopic operation in the middle and lower rectum, which is extra-peritoneal, usually does not cause complications, like infectious peritonitis. However, pelvic tissues around the middle and lower rectum are loose, the space of them communicates with retroperitoneal space, and even fascia space of lower limbs, so mismanagement may lead to pelvic infection around the rectum, or even retroperitoneal infection and lower limb infection. [ 2],[3 ] Such infections are uneasy to detect at clinical early stage, once those infections evolve, it may result in diffused necrotizing fasciitis of retroperitoneum and lower limbs, which represents an extremely dangerous state and difficulty in clinical management. Now, both domestic and foreign reports of endoscopic treatments for rectal SMT originating from the MP layer are less.

With the maturity of the endoscopic therapeutic techniques and the inspiration of ESD and NOTES, STER as a novel endoscopic operating method, is invented to resect SMTs which locate in deeper layer of GI tract, [1],[9],[10] since conventional endoscopic resections for those SMTs could lead to more complications and surgery no doubt brings greater trauma. STER technique was used in upper GI tract initially, and our center have reported several studies stating the advantages of STER, such as the flexibility, safety, efficiency, minimally invasion. [1],[11],[12] Some other centers also shared the studies of STER, and they verified those advantages further. [13],[14]

Because of the difference in anatomical structures, creating a tunnel and performing tumor resection in the rectum is quite different from in the upper GI tract in technical details. Rectal wall goes with some degree of radian, which is not beneficial to make a tunnel entrance. [ 2],[3 ] Mucosal incision in difficult site should be avoided, and enough length of the tunnel should be retained for the operation. For rectal SMTs originating from the MP layer, we choose 2-3 cm proximal to the tumor as the tunnel entrance, and the length of the tunnel is at least 3-4 cm, so that in case of mucosa tear at tunnel entrance, the mucosa on the tumor can be still intact for sure. For SMTs in the lower rectum, in order to ensure enough length of the tunnel, oblique incision usually required in tumor oblique below instead of in tumor vertical below. For creating submucosal tunnel easily, the caliber of the endoscope should be as fine as possible. We choose therapeutic colonoscope PCF-Q260JI with flush function or gastroscope GIF-H260 with smaller diameter for operation. In our study, the median procedure time was 49.5 min (range 40-70 min), and the median hospital stays was 3.1 (range 2-8) days, which showed the flexibility, safety and minimally invasion of the technique. More remarkable, besides the advantages mentioned above, the greatest superiority is allowing complete and en bloc resection, and R0 resection rate is high according to those reports. In our study, STER was performed successfully in all cases. And en bloc resection was achieved in one time for all SMTs. Postoperative pathological results showed that all resected margins of the specimens were negative. And this resulted in no residual and recurrence of the tumors during the follow-up period of the patients.

Complication rate of STER is low. [1],[5],[6],[7],[8],[9] In the series, minimal bleeding occurred in every case, and all managed successfully with electric coagulation hemostasis endoscopically. No massive hemorrhage or postoperative delayed bleeding developed because of adequate hemostasis. Three cases (25.0%, 3/12) developed fever after the procedures, and maximum body temperature was 38°C. All of them recovered after the treatments of anti-infection. Among those 3 cases, one (8.3%, 1/12) developed intraoperative mucosal perforation, which was clipped with metal clips. This patient only developed low-grade fever, and no further complications occurred.

The main complication of STER is gas-related events. Since retroperitoneal emphysema and subcutaneous emphysema once develop, quick exhaust with puncture is quite difficult. Since CO 2 can be diffused and absorbed quickly in the human body, [15],[16] it is safer to use CO 2 insufflation during the operation. In one of our studies about STER, we reported that CO 2 leaded to a low gas-related complication rate and made the complications lighter and easier to recover. [11] Hence, if conditions permit, carbon dioxide should be insufflated during the operation to reduce patients' discomforts due to postoperative subcutaneous emphysema and abdominal distension. In this study, 9 cases were insufflated CO 2 during the procedures while the rest 3 insufflated air. And in CO 2 group, no gas-related complication occurred, while in air insufflation group, one patient (8.3%, 1/12) developed postoperative subcutaneous emphysema in one lower extremity, which disappeared with conservative treatments 2 weeks after the procedure.

Being different from STER in the upper GI tract, gastric tube cannot be inserted for drainage after rectal STER. Hence, it is necessary to keep the stool less, soft, and easy to defecate for patients after operations. Dry stool and difficulty in defecating should be avoided, for that may cause wound avulsion and even infection. In this series, no conditions mentioned above developed in all patients. Mucosa perforation should be avoided in tunneling endoscopic operations as far as possible. When perforation develops and leads to fistula or infection after operation in the rectum, peritoneal irritation could not appear, and the condition would be hidden and harder to estimate than that of upper GI perforation. [ 2],[3 ] For that reason, patients' postoperative situations should be estimated combining careful observation in lower limbs, buttocks, perineum, and crissum by experienced physicians, vital signs and white blood cell count, and CT if necessary. In this series of patients, only one patient developed mucosa perforation, which was repaired with metal clips. This patient developed only low fever, but no obvious infectious signs, who recovered after symptomatic treatments.

Applying STER technique for resecting rectal SMTs originating from the MP layer could maintain the mucosa intact reduces infection and other complications occurrence due to perforation resulting from full-thickness resection. Our initial experiences showed that STER for rectal SMTs originating from the MP layer is feasible, safe, and effective, and helps to achieve high R0 resection rate. However, relevant research is still in early stage, more experiences in indications for rectal STER and managements for complications should be further accumulated.

 
 > References Top

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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.  Back to cited text no. 1
    
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Cheol WC, Dae HK, Hyung WK, Su BP, Woo SJ, Geun AS, et al. Comparison of endoscopic resection therapies for rectal carcinoid tumor endoscopic submucosal dissection versus endoscopic mucosal resection using band ligation. J Clin Gastroenterol 2013;47:432-6.  Back to cited text no. 7
    
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von Delius S, Gillen S, Doundoulakis E, Schneider A, Wilhelm D, Fiolka A, et al. Comparison of transgastric access techniques for natural orifice transluminal endoscopic surgery. Gastrointest Endosc 2008;68:940-7.  Back to cited text no. 9
    
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Isomoto H. Updates on endoscopic therapy of esophageal carcinoma. Thorac Cancer 2012;3:125-30.  Back to cited text no. 10
    
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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.  Back to cited text no. 11
    
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Xu MD, Lu W, Li QL, Zhou PH, Zhong YS, Chen WF, et al. Application and evaluation of submucosal tunneling endoscopic resection of gastric submucosal tumors originating from the muscularis propria layer. Zhonghua Wei Chang Wai Ke Za Zhi 2012;15:671-4.  Back to cited text no. 12
    
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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.  Back to cited text no. 13
    
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Ye LP, Zhang Y, Mao XL, Zhu LH, Zhou X, Chen JY. Submucosal tunneling endoscopic resection for small upper gastrointestinal subepithelial tumors originating from the muscularis propria layer. Surg Endosc 2014;28:524-30.  Back to cited text no. 14
    
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Wang WL, Wu ZH, Sun Q, Wei JF, Chen XF, Zhou DK, et al. Meta-analysis: The use of carbon dioxide insufflation vs. room air insufflation for gastrointestinal endoscopy. Aliment Pharmacol Ther 2012;35:1145-54.  Back to cited text no. 15
    
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