Topic Highlight Open Access
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Endosc. Nov 25, 2015; 7(17): 1238-1242
Published online Nov 25, 2015. doi: 10.4253/wjge.v7.i17.1238
Endoscopic resection of tumors in the lower digestive tract
Shi-Lun Cai, Qiang Shi, Tao Chen, Yun-Shi Zhong, Li-Qing Yao, Endoscopic Center, Zhongshan Hospital of Fudan University, Shanghai 200032, China
Author contributions: Cai SL and Shi Q contributed equally to this work; Cai SL, Zhong YS and Yao LQ designed the research; Cai SL and Chen T performed the research; Cai SL, Shi Q and Zhong YS wrote the paper.
Supported by Doctoral Fund Project in 2012, No. 20120071110061; Youth Foundation of National Natural Science Foundation of China, No. 81101566; Scientific Funds of Shanghai Government, Nos. 12QA1400600, XYQ2011017, 11411950501, 13411951600, 2013SY045, 2013SY054, and 201305; and Youth Foundation of Zhongshan Hospital Natural Science Foundation, No. 2013ZSQN17.
Conflict-of-interest statement: None.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Li-Qing Yao, MD, Endoscopic Center, Zhongshan Hospital of Fudan University, 180 Fenglin Road, Shanghai 200032, China. yaoliqingfd@126.com
Telephone: +86-21-64041990 Fax: +86-21-64041990
Received: April 26, 2015
Peer-review started: April 27, 2015
First decision: June 2, 2015
Revised: June 22, 2015
Accepted: August 6, 2014
Article in press: September 7, 2015
Published online: November 25, 2015

Abstract

As endoscopic technology has developed and matured, the endoscopic resection of gastrointestinal tract polyps has become a widely used treatment. Colorectal polyps are the most common type of polyp, which are best managed by early resection before the polyp undergoes malignant transformation. Methods for treating colorectal tumors are numerous, including argon plasma coagulation, endoscopic mucosal resection, endoscopic submucosal dissection, and laparoscopic-endoscopic cooperative surgery. In this review, we will highlight several currently used clinical endoscopic resection methods and how they are selected based on the characteristics of the targeted tumor. Specifically, we will focus on laparoscopic-endoscopic cooperative surgery.

Key Words: Colorectal tumor, Endoscopic resection

Core tip: The best case scenario for patients with lower digestive tract tumors is to detect and resect the tumor before it undergoes malignant transformation. However, modern technologies for tumor resection are numerous and there may be specific indications for the implementation of one technology over another. Therefore, we will discuss the current clinical endoscopic resection methods and the process for selecting specific interventions. We wish to highlight laparoscopic-endoscopic cooperative surgery, because it may be of assistance in endoscopic treatment and could remarkably decrease the rate of later surgical repair.



INTRODUCTION

Colorectal tumors are common in modern society and although numerous new technologies have become available to locate, identify, and treat these tumors, early detection and removal (e.g., during the polyp stage before malignant transformation) are still the key to long term survival and a favorable overall prognosis[1,2]. As a result, endoscopic methods have steadily developed to better meet these requirements. A study by Winawer et al[3] showed that endoscopic removal of colorectal adenomas can reduce the incidence rate of colorectal cancer by about 76%-90%. The current clinical endoscopic polypectomy methods are numerous and varied. Through careful observation of the distribution, size, morphology, and pathological features of colorectal polyps, clinicians/endoscopists can select the appropriate endoscopic resection treatment to avoid repeated unsuccessful procedures and improve the quality of life of the patient[2].

ENDOSCOPIC DIAGNOSIS BEFORE RESECTION

Before endoscopic resection, a comprehensive evaluation of the lesion is required. Ordinary endoscopy, magnifying endoscopy, or narrow-banding imaging (NBI) can be used to make a preliminary observation[4]. If the pathology confirms that the lesion is an adenoma, endoscopic resection can be performed. Pedunculated adenomas can be removed easily by endoscopic resection, regardless of the size of tumor; if the adenoma is sessile, the resection will be based on relevant patient parameters (age, body condition, and the patient’s wishes)[5]. If pathological examination shows that the lesion is malignant, a “lifting sign” should be judged by injecting normal saline and indigo dye at the basal submucosal layer of the lesion. If the “lifting sign” is negative, the tumor has invaded and extended into the submucosa or even below[6]. Research has confirmed that for lesions confined to the mucosal layer, lymph node metastasis generally does not occur. Tumors that extend deeper into the submucosal layer can be divided into categories SM1-SM3. SM1 tumors (submucosal invasion < 1000 μm) have a low risk of lymph node metastasis, while the SM2 and SM3 tumors (submucosal invasion more than 1000 μm) have a higher lymphatic metastasis risk-up to 12.5%[7-9]. Tumors with a negative “lifting sign” should be surgically removed, rather than removed endoscopically.

ENDOSCOPIC RESECTION METHODS
Argon plasma coagulation

The principle of argon plasma coagulation (APC) is to use a specialized device to deliver ionization energy from argon; this high frequency energy can be implemented to solidify the tissue surface. Presently, APC plays an important role in maintaining hemostasis and cauterizing lesions during surgical and endoscopic procedures taking place in the human gastrointestinal tract[10]. The advantages of APC for treating colorectal lesions are that it is a rapid and efficient procedure that produces only a small vulnus and is generally well-tolerated by patients[11]. Some studies show that the most outstanding advantage of APC is its self-limited solidification depth. The damage of solidification generally does not extend more than 3 mm, minimizing the risk of perforation[12]. Based on the characteristics of the laser and the high frequency electric knife, APC can effectively be used to stop bleeding during a gastrointestinal procedure. Furthermore, during the operation, the probe does not need to contact the tissue, reducing the risk for adhesions or hemorrhages[13]. However, APC does have some limitations. Mainly, it is difficult to obtain pathological specimens with this technique, making it nearly impossible to determine the invasion depth, such that the cutting edge of the polyps is unclear.

Endoscopic mucosal resection

Endoscopic mucosal resection (EMR) has become a routine method for the treatment of early gastrointestinal mucosal lesions[14]. The general method of EMR is adapted to the submucosal injection of liquid saline to separate the lesions from the underlying muscle layer, after which lesions can be completely removed with a snare. The method is simple, safe, produces a small vulnus, is easily adaptable, and fairly easier to master, even for less experienced endoscopists[15,16]. However, there is the risk for rare and serious complications, such as intestinal perforation and bleeding, although these can be remedied by endoscopy or surgery. The incidence of perforation is very low (0.7%-1.3%), and the risk for bleeding is also fairly low (5.0%-8.1%)[17,18]. Some studies show that effective/optimized submucosal injection can help to prevent complications and ensure the safety of EMR[19]. Compared to APC, EMR has some advantages. Namely, EMR allows for pathological examination of the lesion after EMR to determine invasion depth and the cutting edge. However, due to the likelihood for electrocoagulation through snaring, EMR is only suitable for the complete resection of tumors with diameters that are less than 20 mm. Here, the complete resection rate is 64.3%-77.4%, and the recurrence rate is very low (0%-3.6%)[20,21]. If the tumor is larger than 20 mm, the complete resection rate drops significantly to 48.1%-32.9%, while the recurrence increases to 16%-25.7%[22,23]. Therefore, EMR is not an appropriate choice for the treatment of particularly large (greater than 20 mm) gastrointestinal tumors.

Endoscopic submucosal dissection

Endoscopic submucosal dissection (ESD) was developed based on EMR techniques and was named after it was approved as a new resection method in 2003. In this procedure, an insulation tipped knife (knife IT) is instrumental for performing ESD. Compared to EMR, ESD can not only provide complete specimens for more reliable pathological examination, but it can also be used to fully resect the tumor with a low rate of recurrence[24]. For tumors less than 20 mm, the complete resection rate is 82.6%-97.7% and the recurrence rate is nearly 0%[21,25,26]. However, if the tumor is larger than 20 mm, the complete resection rate drops a little to 74%-91.8%, but the recurrence rate remains 0%-1%[17,22,23,25]. During the ESD procedure, the operator should pay attention to the “lifting sign” after submucosal injection, which can be used to determine the lesion depth. If the lesion is located in the mucous layer with a proper boundary to the muscularis propria and has a positive “lifting sign,” it can be removed by ESD[27,28]. However, the rate of perforation in ESD is higher than that for EMR, because the submucosal layer is nearer to the muscularis. For this procedure, which is more complicated than EMR, the incidence of complications also correlates with the operator’s technical proficiency[29]. Nonetheless, in some studies, the bleeding rate of ESD remains low (0.4%-2.5%), although the risk of perforation is slightly higher (2.9%-5.3%)[30,31].

Laparoscopic-endoscopic cooperative surgery

At present, endoscopic therapy is not only applied to resecting colorectal polyps, but also to the treatment of early colorectal cancers that are located in the mucosal layer. Through endoscopic resection, patients can avoid laparotomy, sustain lesser injury, and recover quickly[32]. However, the colonoscopy field of vision is limited in the intestinal lumen, such that the condition of the bowel wall or abdominal cavity is unclear. Some lesions located in the splenic or hepatic flexure can make endoscopic resection difficult. Laparoscopic-endoscopic cooperative surgery (LECS) takes advantage of characteristics of both laparoscopic and colonoscopic procedures. LECS is often implemented when the lesion is difficult to be removed or cannot be completely resected by endoscopic methods alone[33]. Under the guide of a colonscope, the laparoscope can look for and identify the intestinal site where the lesion is located and dissociate it from this site if necessary. By pulling and pushing the laparoscope upward, the lesion may be exposed so that endoscopists can use EMR or ESD to remove the lesion. During this process, the operator can focus on the complete excision of the lesion and does not need to be concerned with possibility of perforation. If perforation or bleeding occurs, laparoscopy can be used to repair the perforation and return to hemostasis immediately. However, no randomized controlled trials have been performed to evaluate LECS in the treatment of lower digestive tract tumors. Nonetheless, select published LECS cases suggest that it is a feasible procedure for the en bloc resection of some colonic lateral spreading tumors that would be otherwise difficult to resect using exclusively endoscopic methods[34-36].

CHOOSING THE ENDOSCOPIC TREATMENT
Tumors with a diameter less than 3 mm

For small tumors less than 3 mm in diameter, APC can be used for solidification of the lesion. However, as this technique cannot be used to collect pathological specimens, long-term endoscopic follow-up is required[37].

Tumors with a diameter less than 20 mm

For lesions in this size category, according to a study by Lee et al[26], there are no significant differences in the complete resection rate between EMR (82.6%) and ESD (64.3%) techniques. Although EMR has a recurrence rate of 3.6%, the risk of cancer progression for small tumors is minimal and the main pathological type for this size tumor is adenoma; therefore, EMR is suitable for the removal of small lesions and is a fairly easy technique to master, even for less experienced endoscopists. The risk of perforation with EMR is lower than that with ESD, and it is regarded as a quicker and safer choice for lesions with a relatively smooth surface without signs of bleeding and erosion[18,38]. However, there are some exceptions. If the endoscopic diagnosis (NBI or magnifying endoscope) strongly indicates that the lesion is malignant and the pathological examination shows the same results, the tumor must be excised by ESD and the patients should undergo close follow-up in the future.

Tumors with a diameter more than 20 mm

Some studies report that the proportion of adenocarcinomas significantly increases in tumors larger than 20 mm in diameter, since the degree of tumor malignancy is often associated with the relative tumor size[39]. Other studies report that the size of the tumor can be at least partly used as an index to predict the degree of malignancy. The possibility of recurrence for tumors greater than 10 mm diameter is relatively high[26]. Early adenocarcinomas have characteristics of invasion, recurrence, and metastasis, and due to a lower complete resection rate and high recurrence rate, EMR is not suitable for these kinds of tumors. Fortunately, ESD can be used to remove larger tumors with much higher complete resection rates and lower recurrence rates. However, ESD still has some limitations, especially for larger laterally spreading tumors. Here the excised area is often too large, translating to an extremely high risk of perforation[40]. Once a perforation occurs, a surgical repair or intestinal resection is needed to repair the large defect left by ESD. Therefore, LECS may be a better choice to ensure a complete resection, while minimizing the risk of serious complications. Based on the assistance of a laparoscope, the visibility of lesion is greatly enhanced and the operator can focus on the complete excision of the lesion while not worrying about the possibility of perforation, which can easily and rapidly be repaired using the laparoscope to stitch the perforated area. Rapid detection and repair of any perforations greatly reduce the risk of abdominal infection. Therefore, in certain situations, LECS can not only be minimally invasive, but also offers better and safer therapeutic effects[41,42].

CONCLUSION

Endoscopic resection presents a great technological leap in the diagnosis and treatment of colorectal tumors, as well as an important preventive measure to remove polyps in their premalignant stages. In recent years, some new technologies, such as magnifying endoscopy and NBI have improved the detection rate of early colorectal cancers, which improves long term survival and the resulting quality of life. At the same time, with the continuous development of endoscopic treatment equipment and the introduction of new technologies, most colorectal polyps and early cancers can now be resected by minimally invasive EMR, ESD, or LECS techniques, which can now achieve the same effects as surgery. However, when endoscopic treatment is to be used, the indications should be carefully considered following evaluation of the relevant patient and pathological parameters, along with the likelihood of complete resection and risk for complications. Therefore, initial colonscopy examination is crucial. Although minimally invasive and often successful in full resection, endoscopic resections do have some limitations. If the cancer invades deep into the submucosal layer, belongs to the lower differentiation, or contains a lymphatic or venous tumor thrombus, additional radical surgical operation will still be required.

Footnotes

P- Reviewer: Zaky A S- Editor: Ma YJ L- Editor: Wang TQ E- Editor: Jiao XK

References
1.  Yamasaki Y, Uedo N, Ishihara R, Tomita Y. Endoscopic mucosal resection of early stage colon neuroendocrine carcinoma. BMJ Case Rep. 2015;2015.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 3]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
2.  Santos CE, Malaman D, Carvalho Tdos S, Lopes CV, Pereira-Lima JC. Malignancy in large colorectal lesions. Arq Gastroenterol. 2014;51:235-239.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Winawer SJ, Zauber AG. Incidence reduction following colonoscopic polypectomy. Am J Gastroenterol. 2011;106:370.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 6]  [Cited by in F6Publishing: 7]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
4.  Goto N, Kusaka T, Tomita Y, Tanaka H, Itokawa Y, Koshikawa Y, Yamaguchi D, Nakai Y, Fujii S, Kokuryu H. Magnifying narrow-band imaging with acetic acid to diagnose early colorectal cancer. World J Gastroenterol. 2014;20:16306-16310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 6]  [Cited by in F6Publishing: 8]  [Article Influence: 0.8]  [Reference Citation Analysis (0)]
5.  Seo JY, Chun J, Lee C, Hong KS, Im JP, Kim SG, Jung HC, Kim JS. Novel risk stratification for recurrence after endoscopic resection of advanced colorectal adenoma. Gastrointest Endosc. 2015;81:655-664.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 32]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
6.  Ishiguro A, Uno Y, Ishiguro Y, Munakata A, Morita T. Correlation of lifting versus non-lifting and microscopic depth of invasion in early colorectal cancer. Gastrointest Endosc. 1999;50:329-333.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Kitajima K, Fujimori T, Fujii S, Takeda J, Ohkura Y, Kawamata H, Kumamoto T, Ishiguro S, Kato Y, Shimoda T. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol. 2004;39:534-543.  [PubMed]  [DOI]  [Cited in This Article: ]
8.  Di Gregorio C, Bonetti LR, de Gaetani C, Pedroni M, Kaleci S, Ponz de Leon M. Clinical outcome of low- and high-risk malignant colorectal polyps: results of a population-based study and meta-analysis of the available literature. Intern Emerg Med. 2014;9:151-160.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 22]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
9.  Ueno H, Mochizuki H, Hashiguchi Y, Shimazaki H, Aida S, Hase K, Matsukuma S, Kanai T, Kurihara H, Ozawa K. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004;127:385-394.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  Neneman B, Gasiorowska A, Małecka-Panas E. The efficacy and safety of argon plasma coagulation (APC) in the management of polyp remnants in stomach and colon. Adv Med Sci. 2006;51:88-93.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Oxenberg J, Hochwald SN, Nurkin S. Ablative therapies for colorectal polyps and malignancy. Biomed Res Int. 2014;2014:986352.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 3]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
12.  East JE, Toyonaga T, Suzuki N. Endoscopic management of nonpolypoid colorectal lesions in colonic IBD. Gastrointest Endosc Clin N Am. 2014;24:435-445.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 23]  [Cited by in F6Publishing: 24]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]
13.  Panos MZ, Koumi A. Argon plasma coagulation in the right and left colon: safety-risk profile of the 60W-1.2 l/min setting. Scand J Gastroenterol. 2014;49:632-641.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 6]  [Cited by in F6Publishing: 7]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
14.  Sakamoto T, Matsuda T, Nakajima T, Saito Y. Efficacy of endoscopic mucosal resection with circumferential incision for patients with large colorectal tumors. Clin Gastroenterol Hepatol. 2012;10:22-26.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 44]  [Cited by in F6Publishing: 48]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
15.  Consolo P, Luigiano C, Strangio G, Scaffidi MG, Giacobbe G, Di Giuseppe G, Zirilli A, Familiari L. Efficacy, risk factors and complications of endoscopic polypectomy: ten year experience at a single center. World J Gastroenterol. 2008;14:2364-2369.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Kaimakliotis PZ, Chandrasekhara V. Endoscopic mucosal resection and endoscopic submucosal dissection of epithelial neoplasia of the colon. Expert Rev Gastroenterol Hepatol. 2014;8:521-531.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 9]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
17.  Terasaki M, Tanaka S, Oka S, Nakadoi K, Takata S, Kanao H, Yoshida S, Chayama K. Clinical outcomes of endoscopic submucosal dissection and endoscopic mucosal resection for laterally spreading tumors larger than 20 mm. J Gastroenterol Hepatol. 2012;27:734-740.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 123]  [Cited by in F6Publishing: 119]  [Article Influence: 9.9]  [Reference Citation Analysis (0)]
18.  Serrano M, Mão de Ferro S, Fidalgo P, Lage P, Chaves P, Dias Pereira A. Endoscopic mucosal resection of superficial colorectal neoplasms: review of 140 procedures. Acta Med Port. 2012;25:288-296.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Grgov S, Dugalić P, Tomasević R, Tasić T. Endoscopic mucosal resection of flat and sessile colorectal adenomas: our experience with long-term follow-ups. Vojnosanit Pregl. 2014;71:33-38.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Goto O, Fujishiro M, Kodashima S, Kakushima N, Ono S, Yahagi N, Omata M. Feasibility of electrocautery snaring as the final step of endoscopic submucosal dissection for stomach epithelial neoplasms. Dig Liver Dis. 2009;41:26-30.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 15]  [Cited by in F6Publishing: 15]  [Article Influence: 1.0]  [Reference Citation Analysis (0)]
21.  Kim KM, Eo SJ, Shim SG, Choi JH, Min BH, Lee JH, Chang DK, Kim YH, Rhee PL, Kim JJ. Treatment outcomes according to endoscopic treatment modalities for rectal carcinoid tumors. Clin Res Hepatol Gastroenterol. 2013;37:275-282.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 41]  [Cited by in F6Publishing: 51]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
22.  Lee EJ, Lee JB, Lee SH, Youk EG. Endoscopic treatment of large colorectal tumors: comparison of endoscopic mucosal resection, endoscopic mucosal resection-precutting, and endoscopic submucosal dissection. Surg Endosc. 2012;26:2220-2230.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 96]  [Cited by in F6Publishing: 92]  [Article Influence: 7.7]  [Reference Citation Analysis (0)]
23.  Tajika M, Niwa Y, Bhatia V, Kondo S, Tanaka T, Mizuno N, Hara K, Hijioka S, Imaoka H, Ogura T. Comparison of endoscopic submucosal dissection and endoscopic mucosal resection for large colorectal tumors. Eur J Gastroenterol Hepatol. 2011;23:1042-1049.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 68]  [Cited by in F6Publishing: 75]  [Article Influence: 5.8]  [Reference Citation Analysis (0)]
24.  Wang J, Zhang XH, Ge J, Yang CM, Liu JY, Zhao SL. Endoscopic submucosal dissection vs endoscopic mucosal resection for colorectal tumors: a meta-analysis. World J Gastroenterol. 2014;20:8282-8287.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 87]  [Cited by in F6Publishing: 81]  [Article Influence: 8.1]  [Reference Citation Analysis (0)]
25.  Kim YJ, Kim ES, Cho KB, Park KS, Jang BK, Chung WJ, Hwang JS. Comparison of clinical outcomes among different endoscopic resection methods for treating colorectal neoplasia. Dig Dis Sci. 2013;58:1727-1736.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 45]  [Cited by in F6Publishing: 45]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]
26.  Lee DS, Jeon SW, Park SY, Jung MK, Cho CM, Tak WY, Kweon YO, Kim SK. The feasibility of endoscopic submucosal dissection for rectal carcinoid tumors: comparison with endoscopic mucosal resection. Endoscopy. 2010;42:647-651.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 86]  [Cited by in F6Publishing: 100]  [Article Influence: 7.1]  [Reference Citation Analysis (0)]
27.  Saito Y, Otake Y, Sakamoto T, Nakajima T, Yamada M, Haruyama S, So E, Abe S, Matsuda T. Indications for and technical aspects of colorectal endoscopic submucosal dissection. Gut Liver. 2013;7:263-269.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 49]  [Cited by in F6Publishing: 62]  [Article Influence: 5.6]  [Reference Citation Analysis (0)]
28.  Lai LH, Chan FK. Endoscopic submucosal dissection for colonic lesions: why and how should we do it? J Dig Dis. 2011;12:229-233.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 6]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
29.  Sanchez-Yague A, Kaltenbach T, Raju G, Soetikno R. Advanced endoscopic resection of colorectal lesions. Gastroenterol Clin North Am. 2013;42:459-477.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 36]  [Cited by in F6Publishing: 42]  [Article Influence: 3.8]  [Reference Citation Analysis (0)]
30.  Lee EJ, Lee JB, Lee SH, Kim do S, Lee DH, Lee DS, Youk EG. Endoscopic submucosal dissection for colorectal tumors--1,000 colorectal ESD cases: one specialized institute’s experiences. Surg Endosc. 2013;27:31-39.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 103]  [Cited by in F6Publishing: 94]  [Article Influence: 7.8]  [Reference Citation Analysis (0)]
31.  Hotta K, Yamaguchi Y, Saito Y, Takao T, Ono H. Current opinions for endoscopic submucosal dissection for colorectal tumors from our experiences: indications, technical aspects and complications. Dig Endosc. 2012;24 Suppl 1:110-116.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 36]  [Article Influence: 3.0]  [Reference Citation Analysis (0)]
32.  Hauenschild L, Bader FG, Laubert T, Czymek R, Hildebrand P, Roblick UJ, Bruch HP, Mirow L. Laparoscopic colorectal resection for benign polyps not suitable for endoscopic polypectomy. Int J Colorectal Dis. 2009;24:755-759.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18]  [Cited by in F6Publishing: 20]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
33.  Hiki N, Nunobe S, Matsuda T, Hirasawa T, Yamamoto Y, Yamaguchi T. Laparoscopic endoscopic cooperative surgery. Dig Endosc. 2015;27:197-204.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 69]  [Cited by in F6Publishing: 78]  [Article Influence: 8.7]  [Reference Citation Analysis (0)]
34.  Fukunaga Y, Tamegai Y, Chino A, Ueno M, Nagayama S, Fujimoto Y, Konishi T, Igarashi M. New technique of en bloc resection of colorectal tumor using laparoscopy and endoscopy cooperatively (laparoscopy and endoscopy cooperative surgery - colorectal). Dis Colon Rectum. 2014;57:267-271.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 26]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
35.  Shi Q, Xu MD, Zhong YS, Zhou PH, Wu HF, Yao LQ. The laparoscopic-endoscopic cooperative surgery for the colonic calcifying fibrous tumor: one case report. J Laparoendosc Adv Surg Tech A. 2012;22:996-998.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 8]  [Cited by in F6Publishing: 11]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
36.  Irino T, Nunobe S, Hiki N, Yamamoto Y, Hirasawa T, Ohashi M, Fujisaki J, Sano T, Yamaguchi T. Laparoscopic-endoscopic cooperative surgery for duodenal tumors: a unique procedure that helps ensure the safety of endoscopic submucosal dissection. Endoscopy. 2015;47:349-351.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 13]  [Cited by in F6Publishing: 29]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
37.  Friedland S, Banerjee S, Kochar R, Chen A, Shelton A. Outcomes of repeat colonoscopy in patients with polyps referred for surgery without biopsy-proven cancer. Gastrointest Endosc. 2014;79:101-107.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 38]  [Cited by in F6Publishing: 44]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
38.  Park JJ, Cheon JH, Kwon JE, Shin JK, Jeon SM, Bok HJ, Lee JH, Moon CM, Hong SP, Kim TI. Clinical outcomes and factors related to resectability and curability of EMR for early colorectal cancer. Gastrointest Endosc. 2011;74:1337-1346.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 28]  [Article Influence: 2.2]  [Reference Citation Analysis (0)]
39.  Noshirwani KC, van Stolk RU, Rybicki LA, Beck GJ. Adenoma size and number are predictive of adenoma recurrence: implications for surveillance colonoscopy. Gastrointest Endosc. 2000;51:433-437.  [PubMed]  [DOI]  [Cited in This Article: ]
40.  Repici A, Hassan C, Pagano N, Rando G, Romeo F, Spaggiari P, Roncalli M, Ferrara E, Malesci A. High efficacy of endoscopic submucosal dissection for rectal laterally spreading tumors larger than 3 cm. Gastrointest Endosc. 2013;77:96-101.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 60]  [Article Influence: 5.5]  [Reference Citation Analysis (0)]
41.  Ohi M, Yasuda H, Ishino Y, Katsurahara M, Saigusa S, Tanaka K, Tanaka K, Mohri Y, Inoue Y, Uchida K. Single-incision laparoscopic and endoscopic cooperative surgery for gastrointestinal stromal tumor arising from the duodenum. Asian J Endosc Surg. 2013;6:307-310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 8]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
42.  Sakon M, Takata M, Seki H, Hayashi K, Munakata Y, Tateiwa N. A novel combined laparoscopic-endoscopic cooperative approach for duodenal lesions. J Laparoendosc Adv Surg Tech A. 2010;20:555-558.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 23]  [Cited by in F6Publishing: 28]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]