doi:10.1111/codi.12899
Original article
Ligation-assisted endoscopic enucleation for the treatment of colorectal submucosal tumours originating in the muscularis propria J. Guo*, S. Wang*, Z. Liu†, S. Sun*, X. Liu*, S. Wang*, N. Ge* and G. Wang* *Endoscopic Center, Shengjing Hospital of China Medical University, Shenyang, China and †Ultrasound Department, Shengjing Hospital of China Medical University, Shenyang, China Received 27 August 2014; accepted 3 December 2014; Accepted Article online 20 January 2015
Abstract Aim A ligation-assisted endoscopic enucleation (EE-L) technique was developed and was evaluated to determine its efficacy and safety for treating colorectal submucosal tumours (< 10 mm) originating in the muscularis propria. Method EE-L was used to treat 13 patients between January 2011 and January 2014. The tumour was sucked into a transparent cap and ligated at its base by a rubber band ligature attached to the tip of the endoscope. With the creation of a pseudo-stalk, the tumour was then enucleated using endoscopic dissection and the wound was closed with clips. Results All tumours [median diameter 6.8 (4–10) mm] were successfully enucleated [procedure time 19 (11–27) min]. Histopathological examination identified 11 (84.6%) to be leiomyoma and 2 (15.4%) low-risk
Introduction There has been a rapidly increasing incidence worldwide of colorectal submucosal tumours (SMTs), possibly because of a significant increase in endoscopic screening for colorectal cancer [1]. Endoscopic ultrasonography (EUS) is often used to investigate them, but it is not sufficient to provide an accurate pathological diagnosis of a submucosal tumour originating from the muscularis propria layer; endosonic biopsy is also difficult with small lesions. Several endoscopic resection techniques have been demonstrated to be feasible and safe for the treatment of tumours originating in the muscularis propria, including ligation [2–4], submucosal dissection (ESD) Correspondence to: Siyu Sun, Endoscopic Center, Shengjing Hospital of China Medical University, 36 Sanhao Street, Shenyang, Liaoning Province 110004, China. E-mails: [email protected]; [email protected]
gastrointestinal stromal tumours. No perforations or massive haemorrhage occurred and there were no recurrences during a follow-up of 3–39 months. Conclusion EE-L is a successful technique for the removal of small colorectal tumours in the muscularis propria with few complications and enables a histopathological diagnosis. In this study, all the resected lesions had a benign pathology. Keywords Ligation, enucleation, submucosal tumour, muscularis propria, colorectal What does this paper add to the literature? This study has demonstrated that ligation-assisted endoscopic enucleation is a safe, effective and uncomplicated technique for the diagnosis and resection of small colorectal submucosal tumours originating in the muscularis propria.
[5,6], enucleation [7,8] and full-thickness resection [9], but these techniques have some disadvantages. By combining endoscopic band ligation and endoscopic enucleation, a new ligation-assisted endoscopic enucleation (EE-L) technique was developed to combine the advantages of both techniques. In a preliminary study, EE-L was demonstrated to be a safe, effective and simple method that could be used for the histological diagnosis and excision of small tumours originating in the muscularis propria in the oesophagus [10,11], but is is unclear whether it can be used to treat submucosal colorectal tumours originating in the muscularis propria.
Method Consecutive patients with a submucosal tumour detected on routine colonoscopy between January 2011 and January 2014 were identified. They were included
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in the study if: (1) the colorectal lesion originated from the muscularis propria, as indicated by endorectal ultrasound (EUS), (2) the tumour was < 10 mm in diameter, (3) the patient had a normal complete blood count and prothrombin time for at least 1 week before the procedure, and (4) the patient was not taking warfarin, clopidogrel, aspirin or any other nonsteroidal antiinflammatory drug. The study was approved by the institutional review board at the China Medical University, and all enrolled patients provided informed consent. A physician experienced in endoscopic ligation and endoscopic submucosal dissection techniques conducted EE-L on the patients. Devices
A linear-array scanning echo-endoscope (Pentax, Tokyo, Japan, EG3870UT equipped with a Hitachi, Tokyo, Japan, 6500 EUB ultrasonography machine) or a radial scanning echo-endoscope (UM-2R; Olympus Corporation, Tokyo, Japan) was used for EUS. For endoscopic ligation, a standard endoscope (EPK-i, Pentax) with a 10-mm air-driven ligator cap (Sumibe, Akita, Japan) was used. The cap had a small tube used to control the band that was released after air (2 ml) had been injected into the tube. For enucleation, a hook knife (Olympus Corporation), forceps, electrocautery snare (SD-9L-1; Olympus), haemostatic forceps (FD-410LR; Olympus) and high-frequency generator (ICC 200; Erbe, T€ ubingen, Germany) were used. Metallic clips (Olympus Corporation) were used for wound closure.
Procedure EUS was performed to determine the origin of any hypoechoic mass and particularly whether it originated from the muscularis propria,. A linear-array scanning echoendoscope was used to observe lesions located in the rectum; a radial scanning echo-endoscope was used to observe lesions in the colon. The procedure for a ligation-assisted endoscopic enucleation is illustrated in Fig. 1. First the lesion is aspirated into a transparent cap attached to the tip of an endoscope with an elastic band (Fig. 1b) followed by release of the band at its base to force the lesion to assume a polypoid form (Fig. 1c). If the lesion is not completely ligated, the band is removed with a foreign body forceps and the lesion ligated again. Several metal clips are placed around the elastic band to help closure of the wound. A hook knife was then used to open the mucosal and submucosal layers overlying the tumour to enable it to be dissected from the muscularis propria (Fig. 1d). Once
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the tumour has been completely dissected, an electrocautery snare is used for the final excision (Fig. 1e,f). The wound is carefully evaluated for any residual tumour and, if satisfactory, the wound is closed by metal clips (Fig. 1g,h). Colonoscopy was repeated at 6 and 12 months after resection. If no residual tumour was seen patients with a leiomyoma did not require further surveillance. In contrast, patients with a gastrointestinal stromal tumour (GIST) were recommended to have a 2-yearly colonoscopy. Histopathological examination of the resected specimen recorded the cell type, cellularity, nuclear atypia and mitotic index. To differentiate mesenchymal and epithelial tumours, an immunohistochemical analysis was conducted for CD117 (c-kit), CD34, smooth muscle actin, desmin, S-100, DOG-1 and Ki-67.
Results The patients’ demographic characteristics, features of the lesion, pathological diagnosis and clinical outcome are shown in Table 1. Of the 34 patients with a tumour originating from the muscularis propria as demonstrated by EUS, seven with a tumour > 10 mm in diameter were excluded. Fourteen patients chose to have colonoscopic follow-up. The remaining 13 patients (8 male), mean age 57.1 (36–72) years, had a colorectal tumour of median diameter 6.8 (4–10) mm originating in the muscularis propria and were selected for EE-L. Nine tumours were in the colon and four were in the rectum. The en bloc resection rate was 100% (13/13). Histopathological examination of the 13 specimens showed 11 (84.6%) to be an leiomyoma and 2 (15.4%) a GIST. All were benign. In all cases EUS could not differentiate leiomyoma from GIST. The mean duration of the EE-L procedure was 19.2 (11–27) min. There was no case of perforation or massive haemorrhage. No recurrence occurred during a follow-up of 3–39 months.
Discussion A GIST is derived from the interstitial cells of Cajal or their precursors. A GIST tumour can arise at any location in the gastrointestinal tract, particularly the stomach (60–70%) and small intestine (25–35%), but it is rare in the large bowel (5%) and oesophagus (2–3%) [12]. As confirmed in the present study the accuracy of EUS can be unsatisfactory [13–16]. Although EUSguided fine needle aspiration might help to establish the histological diagnosis, insufficient tissue might be obtained, rendering it difficult to provide an accurate histopathological assessment of the benign or malignant
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(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
Figure 1 Procedure for ligation-assisted endoscopic enucleation. (a) Endoscopic ultrasonography and an endoscopic image of the tumour before banding. (b) An image of the tumour aspirated into a transparent cap. (c) The tumour ligated with an elastic band. (d) The tumour after exposure. (e), (f) The resected tumour. (g), (h) Metallic clips were used to close the wound surface.
Table 1 Demographic and clinicopathological characteristics of the study 13 patients included in the study.
Patient
Gender/age (years)
Location
Tumour size (mm)
Operation time (min)
Enucleation time (min)
Pathological diagnosis
Complications
1 2 3 4 5 6 7 8 9 10 11 12 13
Male/52 Female/49 Male/54 Male/62 Male/70 Female/69 Male/57 Male/42 Male/36 Female/55 Female/57 Female/67 Male/72
Rectum Colon Colon Colon Colon Colon Colon Rectum Rectum Colon Colon Rectum Colon
5 4 10 9 9 6 7 7 6 5 4 6 10
31 46 52 58 35 46 41 26 29 43 49 32 48
19 22 21 27 16 25 19 16 11 20 17 14 23
Leiomyoma Leiomyoma GIST GIST Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma
None None None None None None None None None None None None None
nature of a tumour [17]. As these tumours are small, surgical resection might be deemed excessively invasive. The National Comprehensive Cancer Network (NCCN) and European Society for Medical Oncology (ESMO) guidelines state that nodules measuring more than 2 cm should be excised and biopsied, whereas the Canadian guidelines indicate that even small GISTs of < 1 cm should be excised because of the risk of metastasis [14–16,18]. The NCCN guidelines do state that the 2-cm cut-off is somewhat arbitrary, although reasonable, and suggest that the proper management of small GISTs (< 2 cm) discovered incidentally remains controversial [14–16,18–22]. For smaller nodules
(< 2 cm), the ESMO recognizes that performing a biopsy could be difficult and recommends EUS and follow-up, reserving excision only for oesophageal, gastric and duodenal nodules that increase in size [15]. In contrast, the standard approach for rectal nodules is biopsy and excision after ultrasound assessment, regardless of tumour size, because the risk of rectal nodule increasing in size is higher [15]. In contrast follow-up may be an option with a small lesion if discussed with the patient [15]. Because a small tumour may increase in size and may not always be benign, some patients with a small SMT will chose resection. If the tumour can be safely resected and its pathological characteristics obtained
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using a mini-invasive technique, this approach would be rational. Endoscopic submucosal resection with band ligation (ESMR-L) has been previously demonstrated to be useful for treating rectal carcinoid tumours [23]. Ono et al. [23] reported that this was technically simple, minimally invasive and safe for small rectal carcinoid tumours confined to the mucosa. ESMR-L provides a deeper resection margin than conventional endoscopic mucosal resection or polypectomy. In the study by Niimi et al. [24], all 24 consecutive rectal carcinoid tumours in the submucosa were successfully treated with an endoscopic ligation device with an en bloc resection rate of 100% (11/11 tumours). The mean procedure time was longer in the ESD (28.8 16.2 min) than the EMR-L group (17.4 4.4 min). Perforation is a recognized complication of endoscopic resection, even if performed by an expert endoscopist [5–9,25]. The EE-L technique may substantially decrease this risk. First, the base below the tumour is firmly ligated with an elastic band. Secondly, precutting the overlying mucosa and submucosa above the tumour and then gradually enucleating it maintains most of the overlying mucosa, facilitating wound closure [25]. Thirdly, closing the wound with clips and an elastic band could prevent perforation as used in other circumstances in the gastrointestinal tract [26]. This study had some limitations. Using EE-L, complete enucleation is defined solely by endoscopic observation, similar to other endoscopic resection techniques for tumours originating in the muscular propria. With endoscopic resection it is difficult to obtain an adequate margin around the tumour. For these reasons long-term follow-up is required to ensure complete excision of GISTs. The present study has demonstrated that EE-L is a safe, effective and relatively uncomplicated technique for diagnosing and resecting small colorectal tumours originating in the muscularis propria.
Acknowledgements This study was supported by the National Natural Science Foundation of China (grant no. 81071798), the Medical Peak Project Foundation of Liaoning Province (grant no. [2010]696), and the Shengjing Free Researcher Project Foundation. We thank all of the doctors, nurses and pathologists who participated in this study.
Author contributions JG: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of
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the article for important intellectual content; Final approval of the article. SW: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. ZL: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. SS: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. XL: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. SW: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. NG: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. GW: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article.
Disclosures JG, SW, ZL, SS, XL, SW, NG, GW declare that they have no competing interests.
References 1 Scherubl H. Rectal carcinoids are on the rise: early detection by screening endoscopy. Endoscopy 2009; 41: 162–5. 2 Sun S, Jin Y, Chang G, Wang C, Li X, Wang Z. Endoscopic band ligation without electrosurgery: a new technique for excision of small upper-GI leiomyoma. Gastrointest Endosc 2004; 60: 218–22. 3 Sun S, Ge N, Wang C, Wang M, L€ u Q. Endoscopic band ligation of small gastric stromal tumors and follow-up by endoscopic ultrasonography. Surg Endosc 2007; 21: 574–8. 4 Sun S, Ge N, Wang S, Liu X, L€ u Q. EUS-assisted band ligation of small duodenal stromal tumors and follow-up by EUS. Gastrointest Endosc 2009; 69(3 Pt 1): 492–6. 5 Lee IL, Lin PY, Tung SY, Shen CH, Wei KL, Wu CS. Endoscopic submucosal dissection for the treatment of intraluminal gastric subepithelial tumors originating from the muscularis propria layer. Endoscopy 2006; 38: 1024–8. 6 Białek A, Wiechowska-Kozłowska A, Huk J. Endoscopic submucosal dissection of large gastric stromal tumor arising from muscularis propria. Clin Gastroenterol Hepatol 2010; 8: 119–20.
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7 Jeong ID, Jung SW, Bang SJ, Shin JW, Park NH, Kim DH. Endoscopic enucleation for gastric subepithelial tumors originating in the muscularis propria layer. Surg Endosc 2011; 25: 468–74. 8 Park YS, Park SW, Kim TI et al. Endoscopic enucleation of upper-GI submucosal tumors by using an insulated-tip electrosurgical knife. Gastrointest Endosc 2004; 59: 409– 15. 9 Wang L, Ren W, Fan CQ et al. Full-thickness endoscopic resection of nonintracavitary gastric stromal tumors: a novel approach. Surg Endosc 2011; 25: 641–7. 10 Guo J, Liu Z, Sun S, Liu X, Wang S, Ge N. Ligationassisted endoscopic enucleation for treatment of esophageal subepithelial lesions originating from the muscularis propria: a preliminary study. Dis Esophagus 2014, doi: 10.1111/dote.12192. [Epub ahead of print]. 11 Guo J, Liu Z, Sun S et al. Ligation-assisted endoscopic enucleation for the diagnosis and resection of small gastrointestinal tumors originating from the muscularis propria: a preliminary study. BMC Gastroenterol 2013; 13: 88. 12 Miettinen M, Lasota J. Gastrointestinal stromal tumors (GISTs): definition, occurrence, pathology, differential diagnosis and molecular genetics. Pol J Pathol 2003; 54: 3–24. 13 Karaca C, Turner BG, Cizginer S, Forcione D, Brugge W. Accuracy of EUS in the evaluation of small gastric subepithelial lesions. Gastrointest Endosc 2010; 71: 722–7. 14 Blay JY, von Mehren M, Blackstein ME. Perspective on updated treatment guidelines for patients with gastrointestinal stromal tumors. Cancer 2010; 116: 5126–37. 15 Casali PG, Jost L, Reichardt P, Schlemmer M, Blay JY. Gastrointestinal stromal tumours: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 2009; 20(Suppl 4): 64–7. 16 Blackstein ME, Blay JY, Corless C et al. Gastrointestinal stromal tumours: consensus statement on diagnosis and treatment. Can J Gastroenterol 2006; 20: 157–63.
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17 Philipper M, Hollerbach S, Gabbert HE et al. Prospective comparison of endoscopic ultrasound-guided fine-needle aspiration and surgical histology in upper gastrointestinal submucosal tumors. Endoscopy 2010; 42: 300–5. 18 Demetri GD, Benjamin RS, Blanke CD et al. NCCN Task Forcereport: management of patients with gastroin-testinal stromal tumor (GIST)—update of the NCCN clinical practice guidelines. J Natl Compr Canc Netw 2007; 5(Suppl 2): S1–29. 19 American Gastroenterological Association Institute. American Gastroenterological Association Institute medical position statement on the management of gastric subepithelial masses. Gastroenterology 2006; 130: 2215–6. 20 National Comprehensive Cancer Network. Clinical Practice Guidelinesin Oncology for Soft Tissue Sarcoma. Version 2. Fort Washington, PA: National Comprehensive Cancer Net-work, 2009. 21 Montemurro M, Dirnhofer S, Borner M, Burkhard R, Demar-tines N, Furrer M. Diagnosis and treatment of GIST in Switzer-land [guidelines]. Schwiz Med Forum 2008; 8: 416–30. 22 Nishida T, Hirota S, Yanagisawa A et al. Clinical practice guidelines for gastrointestinal stromal tumor (GIST) in Japan: English version. Int J Clin Oncol 2008; 13: 416–30. 23 Ono A, Saito Y, Matsuda T et al. Endoscopic submucosal resection of rectal carcinoid tumors with a ligation device. Gastrointest Endosc 2003; 57: 583–7. 24 Niimi K, Goto O, Fujishiro M et al. Endoscopic mucosal resection with a ligation device or endoscopic submucosal dissection for rectal carcinoid tumors: an analysis of 24 consecutive cases. Dig Endosc 2012; 24: 443–7. 25 Liu BR, Song JT, Qu B, Wen JF, Yin JB, Liu W. Endoscopic muscularis dissection for upper gastrointestinal subepithelial tumors originating from the muscularis propria. Surg Endosc 2012; 13: 3141–8. 26 Raju GS, Gajula L. Endoclips for GI endoscopy. Gastrointest Endosc 2004; 13: 267–79.
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Original article
Ligation-assisted endoscopic enucleation for the treatment of colorectal submucosal tumours originating in the muscularis propria J. Guo*, S. Wang*, Z. Liu†, S. Sun*, X. Liu*, S. Wang*, N. Ge* and G. Wang* *Endoscopic Center, Shengjing Hospital of China Medical University, Shenyang, China and †Ultrasound Department, Shengjing Hospital of China Medical University, Shenyang, China Received 27 August 2014; accepted 3 December 2014; Accepted Article online 20 January 2015
Abstract Aim A ligation-assisted endoscopic enucleation (EE-L) technique was developed and was evaluated to determine its efficacy and safety for treating colorectal submucosal tumours (< 10 mm) originating in the muscularis propria. Method EE-L was used to treat 13 patients between January 2011 and January 2014. The tumour was sucked into a transparent cap and ligated at its base by a rubber band ligature attached to the tip of the endoscope. With the creation of a pseudo-stalk, the tumour was then enucleated using endoscopic dissection and the wound was closed with clips. Results All tumours [median diameter 6.8 (4–10) mm] were successfully enucleated [procedure time 19 (11–27) min]. Histopathological examination identified 11 (84.6%) to be leiomyoma and 2 (15.4%) low-risk
Introduction There has been a rapidly increasing incidence worldwide of colorectal submucosal tumours (SMTs), possibly because of a significant increase in endoscopic screening for colorectal cancer [1]. Endoscopic ultrasonography (EUS) is often used to investigate them, but it is not sufficient to provide an accurate pathological diagnosis of a submucosal tumour originating from the muscularis propria layer; endosonic biopsy is also difficult with small lesions. Several endoscopic resection techniques have been demonstrated to be feasible and safe for the treatment of tumours originating in the muscularis propria, including ligation [2–4], submucosal dissection (ESD) Correspondence to: Siyu Sun, Endoscopic Center, Shengjing Hospital of China Medical University, 36 Sanhao Street, Shenyang, Liaoning Province 110004, China. E-mails: [email protected]; [email protected]
gastrointestinal stromal tumours. No perforations or massive haemorrhage occurred and there were no recurrences during a follow-up of 3–39 months. Conclusion EE-L is a successful technique for the removal of small colorectal tumours in the muscularis propria with few complications and enables a histopathological diagnosis. In this study, all the resected lesions had a benign pathology. Keywords Ligation, enucleation, submucosal tumour, muscularis propria, colorectal What does this paper add to the literature? This study has demonstrated that ligation-assisted endoscopic enucleation is a safe, effective and uncomplicated technique for the diagnosis and resection of small colorectal submucosal tumours originating in the muscularis propria.
[5,6], enucleation [7,8] and full-thickness resection [9], but these techniques have some disadvantages. By combining endoscopic band ligation and endoscopic enucleation, a new ligation-assisted endoscopic enucleation (EE-L) technique was developed to combine the advantages of both techniques. In a preliminary study, EE-L was demonstrated to be a safe, effective and simple method that could be used for the histological diagnosis and excision of small tumours originating in the muscularis propria in the oesophagus [10,11], but is is unclear whether it can be used to treat submucosal colorectal tumours originating in the muscularis propria.
Method Consecutive patients with a submucosal tumour detected on routine colonoscopy between January 2011 and January 2014 were identified. They were included
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in the study if: (1) the colorectal lesion originated from the muscularis propria, as indicated by endorectal ultrasound (EUS), (2) the tumour was < 10 mm in diameter, (3) the patient had a normal complete blood count and prothrombin time for at least 1 week before the procedure, and (4) the patient was not taking warfarin, clopidogrel, aspirin or any other nonsteroidal antiinflammatory drug. The study was approved by the institutional review board at the China Medical University, and all enrolled patients provided informed consent. A physician experienced in endoscopic ligation and endoscopic submucosal dissection techniques conducted EE-L on the patients. Devices
A linear-array scanning echo-endoscope (Pentax, Tokyo, Japan, EG3870UT equipped with a Hitachi, Tokyo, Japan, 6500 EUB ultrasonography machine) or a radial scanning echo-endoscope (UM-2R; Olympus Corporation, Tokyo, Japan) was used for EUS. For endoscopic ligation, a standard endoscope (EPK-i, Pentax) with a 10-mm air-driven ligator cap (Sumibe, Akita, Japan) was used. The cap had a small tube used to control the band that was released after air (2 ml) had been injected into the tube. For enucleation, a hook knife (Olympus Corporation), forceps, electrocautery snare (SD-9L-1; Olympus), haemostatic forceps (FD-410LR; Olympus) and high-frequency generator (ICC 200; Erbe, T€ ubingen, Germany) were used. Metallic clips (Olympus Corporation) were used for wound closure.
Procedure EUS was performed to determine the origin of any hypoechoic mass and particularly whether it originated from the muscularis propria,. A linear-array scanning echoendoscope was used to observe lesions located in the rectum; a radial scanning echo-endoscope was used to observe lesions in the colon. The procedure for a ligation-assisted endoscopic enucleation is illustrated in Fig. 1. First the lesion is aspirated into a transparent cap attached to the tip of an endoscope with an elastic band (Fig. 1b) followed by release of the band at its base to force the lesion to assume a polypoid form (Fig. 1c). If the lesion is not completely ligated, the band is removed with a foreign body forceps and the lesion ligated again. Several metal clips are placed around the elastic band to help closure of the wound. A hook knife was then used to open the mucosal and submucosal layers overlying the tumour to enable it to be dissected from the muscularis propria (Fig. 1d). Once
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the tumour has been completely dissected, an electrocautery snare is used for the final excision (Fig. 1e,f). The wound is carefully evaluated for any residual tumour and, if satisfactory, the wound is closed by metal clips (Fig. 1g,h). Colonoscopy was repeated at 6 and 12 months after resection. If no residual tumour was seen patients with a leiomyoma did not require further surveillance. In contrast, patients with a gastrointestinal stromal tumour (GIST) were recommended to have a 2-yearly colonoscopy. Histopathological examination of the resected specimen recorded the cell type, cellularity, nuclear atypia and mitotic index. To differentiate mesenchymal and epithelial tumours, an immunohistochemical analysis was conducted for CD117 (c-kit), CD34, smooth muscle actin, desmin, S-100, DOG-1 and Ki-67.
Results The patients’ demographic characteristics, features of the lesion, pathological diagnosis and clinical outcome are shown in Table 1. Of the 34 patients with a tumour originating from the muscularis propria as demonstrated by EUS, seven with a tumour > 10 mm in diameter were excluded. Fourteen patients chose to have colonoscopic follow-up. The remaining 13 patients (8 male), mean age 57.1 (36–72) years, had a colorectal tumour of median diameter 6.8 (4–10) mm originating in the muscularis propria and were selected for EE-L. Nine tumours were in the colon and four were in the rectum. The en bloc resection rate was 100% (13/13). Histopathological examination of the 13 specimens showed 11 (84.6%) to be an leiomyoma and 2 (15.4%) a GIST. All were benign. In all cases EUS could not differentiate leiomyoma from GIST. The mean duration of the EE-L procedure was 19.2 (11–27) min. There was no case of perforation or massive haemorrhage. No recurrence occurred during a follow-up of 3–39 months.
Discussion A GIST is derived from the interstitial cells of Cajal or their precursors. A GIST tumour can arise at any location in the gastrointestinal tract, particularly the stomach (60–70%) and small intestine (25–35%), but it is rare in the large bowel (5%) and oesophagus (2–3%) [12]. As confirmed in the present study the accuracy of EUS can be unsatisfactory [13–16]. Although EUSguided fine needle aspiration might help to establish the histological diagnosis, insufficient tissue might be obtained, rendering it difficult to provide an accurate histopathological assessment of the benign or malignant
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(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
Figure 1 Procedure for ligation-assisted endoscopic enucleation. (a) Endoscopic ultrasonography and an endoscopic image of the tumour before banding. (b) An image of the tumour aspirated into a transparent cap. (c) The tumour ligated with an elastic band. (d) The tumour after exposure. (e), (f) The resected tumour. (g), (h) Metallic clips were used to close the wound surface.
Table 1 Demographic and clinicopathological characteristics of the study 13 patients included in the study.
Patient
Gender/age (years)
Location
Tumour size (mm)
Operation time (min)
Enucleation time (min)
Pathological diagnosis
Complications
1 2 3 4 5 6 7 8 9 10 11 12 13
Male/52 Female/49 Male/54 Male/62 Male/70 Female/69 Male/57 Male/42 Male/36 Female/55 Female/57 Female/67 Male/72
Rectum Colon Colon Colon Colon Colon Colon Rectum Rectum Colon Colon Rectum Colon
5 4 10 9 9 6 7 7 6 5 4 6 10
31 46 52 58 35 46 41 26 29 43 49 32 48
19 22 21 27 16 25 19 16 11 20 17 14 23
Leiomyoma Leiomyoma GIST GIST Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma Leiomyoma
None None None None None None None None None None None None None
nature of a tumour [17]. As these tumours are small, surgical resection might be deemed excessively invasive. The National Comprehensive Cancer Network (NCCN) and European Society for Medical Oncology (ESMO) guidelines state that nodules measuring more than 2 cm should be excised and biopsied, whereas the Canadian guidelines indicate that even small GISTs of < 1 cm should be excised because of the risk of metastasis [14–16,18]. The NCCN guidelines do state that the 2-cm cut-off is somewhat arbitrary, although reasonable, and suggest that the proper management of small GISTs (< 2 cm) discovered incidentally remains controversial [14–16,18–22]. For smaller nodules
(< 2 cm), the ESMO recognizes that performing a biopsy could be difficult and recommends EUS and follow-up, reserving excision only for oesophageal, gastric and duodenal nodules that increase in size [15]. In contrast, the standard approach for rectal nodules is biopsy and excision after ultrasound assessment, regardless of tumour size, because the risk of rectal nodule increasing in size is higher [15]. In contrast follow-up may be an option with a small lesion if discussed with the patient [15]. Because a small tumour may increase in size and may not always be benign, some patients with a small SMT will chose resection. If the tumour can be safely resected and its pathological characteristics obtained
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using a mini-invasive technique, this approach would be rational. Endoscopic submucosal resection with band ligation (ESMR-L) has been previously demonstrated to be useful for treating rectal carcinoid tumours [23]. Ono et al. [23] reported that this was technically simple, minimally invasive and safe for small rectal carcinoid tumours confined to the mucosa. ESMR-L provides a deeper resection margin than conventional endoscopic mucosal resection or polypectomy. In the study by Niimi et al. [24], all 24 consecutive rectal carcinoid tumours in the submucosa were successfully treated with an endoscopic ligation device with an en bloc resection rate of 100% (11/11 tumours). The mean procedure time was longer in the ESD (28.8 16.2 min) than the EMR-L group (17.4 4.4 min). Perforation is a recognized complication of endoscopic resection, even if performed by an expert endoscopist [5–9,25]. The EE-L technique may substantially decrease this risk. First, the base below the tumour is firmly ligated with an elastic band. Secondly, precutting the overlying mucosa and submucosa above the tumour and then gradually enucleating it maintains most of the overlying mucosa, facilitating wound closure [25]. Thirdly, closing the wound with clips and an elastic band could prevent perforation as used in other circumstances in the gastrointestinal tract [26]. This study had some limitations. Using EE-L, complete enucleation is defined solely by endoscopic observation, similar to other endoscopic resection techniques for tumours originating in the muscular propria. With endoscopic resection it is difficult to obtain an adequate margin around the tumour. For these reasons long-term follow-up is required to ensure complete excision of GISTs. The present study has demonstrated that EE-L is a safe, effective and relatively uncomplicated technique for diagnosing and resecting small colorectal tumours originating in the muscularis propria.
Acknowledgements This study was supported by the National Natural Science Foundation of China (grant no. 81071798), the Medical Peak Project Foundation of Liaoning Province (grant no. [2010]696), and the Shengjing Free Researcher Project Foundation. We thank all of the doctors, nurses and pathologists who participated in this study.
Author contributions JG: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of
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the article for important intellectual content; Final approval of the article. SW: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. ZL: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. SS: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. XL: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. SW: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. NG: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article. GW: Conception and design; Analysis and interpretation of the data; Drafting of the article; Critical revision of the article for important intellectual content; Final approval of the article.
Disclosures JG, SW, ZL, SS, XL, SW, NG, GW declare that they have no competing interests.
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