Author Affiliations: Department of Gastroenterology (Dr Kao) and Center for Minimally Invasive Surgery (Dr Abbas), Kaiser Permanente, Los Angeles, California; and Department of Gastroenterology, Kaiser Permanente, Anaheim, California (Dr Giap).
Colorectal carcinoma remains a major cause of cancer-related death in the United States.1 Endoscopic removal of colon adenomas is an essential strategy in the prevention of colorectal cancer.2,3 Most small colorectal polyps are easily amenable to endoscopic polypectomy, but larger polyps (>2 cm) or lesions located in a difficult anatomic position often require surgical resection.
Several endoscopic techniques are available to remove large colorectal polyps, including piecemeal polypectomy, endoscopic mucosal resection, and endoscopic submucosal resection.4- 7 Recent technological advances have yielded a large armamentarium of endoscopic tools that have widened the spectrum of lesions potentially removable endoscopically to include early carcinoma.6- 12 Most of the data available on the endoscopic management of large colorectal polyps address technical issues, such as the procedural success rate, complications, and short-term outcome. However, as these endoscopic interventions gain wider acceptance, it is important to critically appraise them from a global perspective, taking into account the long-term outcome. From a surgeon's standpoint, it is essential when considering endoscopic removal of a large colorectal polyp not only to understand the immediate technical outcome but to gain an appreciation for the long-term results in terms of recurrence and the need for subsequent intervention, whether endoscopic or surgical.
The aim of this study was to review our experience with endoscopic excision of large colorectal polyps in a subgroup of patients initially referred for surgical resection.
The study was approved by the institutional review board of Kaiser Permanente Southern California. A retrospective review was conducted of all patients who underwent endoscopic excision of large colorectal lesions during a 4-year period. All patients had a lesion deemed not amenable to endoscopic excision at initial colonoscopy and were initially referred for surgical resection. At initial colonoscopy, histologic sampling of the lesion was performed. In a few patients, an attempt to excise the lesion was undertaken but not completed by the referring endoscopist because of technical difficulties or concerns about an increased risk of perforation.
All procedures were performed by 2 experienced endoscopists proficient in advanced therapeutic colorectal interventions (A.Q.G., a gastroenterologist, and M.A.A., a colorectal surgeon). Referred cases were reviewed by both endoscopists, who used subjective criteria based on the endoscopic pictures taken during the index colonoscopy to determine whether the lesion could be removed endoscopically. The size, location, and morphological (pedunculated vs sessile) and histologic (invasive vs not) features of the lesion were considered, but no case was excluded on the basis of any of these factors unless the lesion was difficult to visualize behind a fold or at an angulated flexure or if deep ulceration was present. All procedures were performed in the outpatient endoscopy suite with the patient under intravenous sedation using a combination of midazolam hydrochloride (Hospira, Inc, Lake Forest, Illinois), meperidine hydrochloride (Baxter Healthcare Corporation, Deerfield, Illinois), and fentanyl citrate (Hospira, Inc). A standard adult colonoscope (EC3830FK and EC3890Li; Pentax Medical Company, Montvale, New Jersey) or a pediatric colonoscope (EC3490Li; Pentax Medical Company) was used in most of the cases. A double-channel therapeutic gastroscope (GIF-2T160; Olympus, Center Valley, Pennsylvania) was used in some cases.
The “inject-and-cut” or “inject-lift-and-cut” endoscopic mucosal resection technique was used at the discretion of the endoscopist. Various tools were used, including endoscopic injection needles (Carr Locke needles; US Endoscopy, Mentor, Ohio) and a needle knife (MicroKnife; Boston Scientific Corp, Natick, Massachusetts). If an en bloc resection was not technically feasible, the lesion was removed in a piecemeal fashion. We used 27-mm and 33-mm snares (Sensation and Captivator snares, respectively; Boston Scientific Corp). Submucosal infiltration with normal saline solution was used selectively depending on the size and location of the lesion. Photographic documentation of the lesion before and after excision was obtained, and the endoscopist noted in the procedural report whether a complete or partial excision was achieved at the index intervention (Figure 1A and B and Figure 2A and B). Histopathologic assessment of all specimens was performed using standard hematoxylin-eosin stains. All patients were observed in the postprocedural recovery unit and released once discharge criteria were met. Follow-up endoscopic evaluation was typically conducted at 3 to 6 months, and additional photographic documentation was obtained (Figures 1C and 2C). The frequency of additional endoscopic surveillance was based on the histologic features of the lesion and completeness of resection.
A large carcinoma in situ of the middle and distal rectum. A, Preoperative view. B, Retroflexion view of complete excision. C, Scar at 4 months after the excision.
A hemicircumferential serrated adenoma of the sigmoid colon. A, Preoperative view. B, View of complete excision. C, Small focal recurrence at 6 months after the excision.
A registry of all patients undergoing therapeutic endoscopy was prospectively maintained by the 2 endoscopists and was used to identify the patients who met the study criteria. The outpatient and inpatient electronic medical records were reviewed, and the abstracted data included demographics, American Society of Anesthesiologists class, indication for initial colonoscopy, and the lesion characteristics (location, size, and histologic features). The outcome measures analyzed were the completeness of excision, procedure-related morbidity or mortality, number of interventions to achieve complete excision, recurrent disease, endoscopic reintervention rate, surgical intervention rate, and endoscopic success rate. Complete excision was defined as removal of the lesion in its entirety, and incomplete excision was defined as residual disease still present at the end of the procedure. Recurrence was defined as the reappearance of the lesion at the original site after documentation of complete resolution during a previous endoscopic follow-up. Procedure-related morbidity was defined as gastrointestinal tract bleeding or perforation that occurred at the time of intervention or within 30 days and that required an emergency department visit, hospital readmission, and/or endoscopic or operative intervention.Endoscopic success rate was defined as the ability to completely eradicate the original lesion (whether this was achieved at the index procedure or at reintervention) or any subsequent recurrence endoscopically without the need for surgical intervention.
To determine the impact of variables such as patient or lesion characteristics on outcome measures, the data were analyzed using the Pearson χ2 test. P < .05 was considered statistically significant. This retrospective study was underpowered for multivariate analysis.
From October 1, 2005, through December 31, 2009, 104 patients were referred for surgical resection of colorectal lesions deemed not amenable to endoscopic excision at initial colonoscopy. Table 1 summarizes the patients' characteristics. The sex distribution was 54% women and 46% men, with a mean age of 67 (range, 29-92) years. Most of the patients (62%) were considered American Society of Anesthesiologists class II. The most common indications for the initial colonoscopy were screening (51%) and positive fecal occult blood test results (24%). The polyps were located in the colon in 68% of the patients and in the rectum in 32% (Table 2). The ascending colon was the most commonly involved location (32%). Tubullovillous or villous adenoma was the most common histologic finding (30%). Carcinoma in situ or invasive carcinoma was diagnosed in 38% of the cases. Most of the lesions were sessile. The mean size of the lesions was 3.3 cm, with a median size of 3.0 (range, 1-9) cm.
Of the 104 patients who were taken to the endoscopy suite with the intent of endoscopic excision, 98 (94%) underwent the intervention and 6 (6%) were deemed not amenable to endoscopic excision and were referred back for surgical evaluation (Figure 3). One patient had excision of the lesion but sustained a perforation and underwent emergency surgical resection. The reasons for technical inability in the subgroup of 6 patients were incomplete visualization of the lesion at a difficult angle or behind a fold or suspected deep invasion with significant involvement of a large area of the bowel wall. Of the 97 patients who underwent excision (excluding the 1 perforation), 77 had complete excision of the lesion and 20 had incomplete excision with residual disease. Of these 20 patients, 5 were referred for and underwent elective surgical resection for in situ or invasive carcinoma. Of the remaining 15 patients, 9 underwent additional endoscopic excision successfully, 2 died of medical comorbidities without additional intervention, 1 received chemotherapy for invasive carcinoma after declining colectomy, and 3 underwent unsuccessful endoscopic reexcision and were eventually referred for and underwent elective surgical resection for residual disease.
The short- and long-term outcomes of endoscopic resection of a cohort of 104 patients with large colorectal lesions deemed not amenable to endoscopic resection at initial colonoscopy.
Complications were noted in 7 patients (7%) after the index intervention. One patient sustained a perforation in the ascending colon and underwent emergent exploration and right-sided hemicolectomy. Two patients had active bleeding during the intervention. The hemorrhage was controlled with a clip device (Resolution clips; Boston Scientific Corp) without the need for transfusion. Four patients had delayed bleeding and presented from 5 to 12 days after the procedure. Three of these patients underwent a second endoscopy with control of the bleeding. One patient was observed for 48 hours and was discharged without the need for endoscopic intervention. All complications were noted within the colon (ascending colon), and none occurred in the rectum, but this trend did not reach statistical significance (P = .06). No procedure-related death was noted. No complications were noted during subsequent endoscopic procedures for surveillance or to treat residual or recurrent disease (Table 3).
During a mean follow-up of 14 (median, 12; range, 3-48) months, recurrent disease at the original site of endoscopic excision was noted in 10 of the 86 patients (12%) who had undergone complete excision previously. All recurrences were small (Figure 2C) and were managed successfully with endoscopic intervention; none required surgical resection. Rectal lesions had a higher risk for recurrence compared with those in the colon (P = .002). The patient's sex and the size or histologic features of the lesion had no influence on recurrence (Table 4).
During the study period, 15 of the 104 patients (14%) underwent surgical resection (Figure 3). After the index endoscopic intervention, 6 patients underwent elective resection for disease not amenable to endoscopic excision, 5 patients for incomplete excision of carcinoma, and 1 patient for acute perforation. An additional 3 patients underwent elective resection for persistent disease after additional endoscopic attempts to eradicate the disease. The operations performed included right-sided hemicolectomy in 7 patients, proctectomy with coloanal anastomosis in 3, anterior resection of the rectum in 2, transanal excision in 2, and subtotal colectomy in 1.
Successful endoscopic management was achieved in 86 patients (83%), with most of the lesions completely excised at the index intervention (Table 3). Endoscopic reintervention occurred in 25 of 92 patients (27%). The reasons for reintervention included residual disease in 12 patients and recurrence in 10 patients. Carcinoma was associated with a lower endoscopic success rate (P < .001) (Table 4).
Endoscopic screening and early removal of colorectal polyps remains one of the most effective interventions for colorectal cancer prevention. In particular, the larger polyps represent a subgroup of lesions with a higher risk for being malignant.13,14 Furthermore, lesions larger than 2 cm can pose a significant challenge even to an experienced endoscopist and are often referred for surgical resection because of the risk of perforation and bleeding or because of the inability to completely eradicate the lesion. Perforation rates have been reported at 0% to 10.4%, and procedure-related bleeding can occur in 1% to 45% of patients.6,15- 17 Such wide variation in morbidity is most likely owing to patient selection in terms of lesion size and location and is influenced by the skills and experience of the endoscopist. Several factors have been previously implicated as representing a higher risk for complications: right-sided lesions, sessile polyps larger than 1 cm, and polyps with a thick stalk.6,11,16,17 In our study, we found a statistically insignificant trend toward an increased risk of complications for right-sided lesions, consistent with previous observations. No complication was observed in the rectum. However, the complication rate of 7% was very favorable considering the well-established risks of surgical resection.18,19 Furthermore, most of the encountered complications were managed nonoperatively. Whether prophylactic endoscopic clipping of the polypectomy site would have eliminated some of the observed complications is unclear. However, in view of recent literature suggesting a potential benefit,20 we now consider clipping a large polypectomy site in the ascending colon.
Since the original description of endoscopic excision of colorectal polyps,21 various techniques have been developed to remove large lesions, including piecemeal polypectomy, endoscopic mucosal resection, and endoscopic submucosal resection.4- 12,22- 26 The short-term success rate has been encouraging. The purpose of reviewing our experience with endoscopic excision of large colorectal lesions was not only to determine immediate outcome measures, such as technical success and the complication rate, but to conduct a comprehensive assessment of its impact beyond the index intervention. We found that most patients (83%) could be successfully treated endoscopically, with only a small number of patients (14%) requiring operative resection to treat complications, incomplete excision after index intervention, or long-term residual disease that could not be eradicated endoscopically. Furthermore, complete excision of the lesion was achieved at the index intervention, with only a few patients requiring more than 1 excision to completely eradicate the lesion. Overall, 27% of the patients required more than 1 endoscopic intervention to treat postprocedural bleeding, to remove residual disease, or to treat recurrence at the original site. We noted a 12% recurrence rate, which is within the range of 0% to 46% reported in the literature.12,22,27 Several factors have an influence on recurrence rate, including patient selection and length of follow-up. We were able to excise recurrent disease endoscopically without the need for surgical intervention. Although larger studies with longer follow-up are needed to stratify risk factors for recurrent disease, there is a lack of guidelines for the best endoscopic surveillance regimen in this heterogeneous group of large lesions. Therefore, a surveillance timeline needs to be individualized to each patient. In our practice, we currently recommend a second endoscopy at 3 to 6 months after complete excision, and we tailor the timing of additional studies according to the histologic findings and location of the lesion. Based on our results, the risk of recurrence was higher in rectal lesions, which would require a more frequent follow-up.
Despite a high overall endoscopic success rate in our group of patients, a diagnosis of carcinoma in situ or invasive carcinoma was associated with a lower success rate. Most of the lesions in our study were sessile. Although endoscopic polypectomy may be a suitable option for many pedunculated malignant polyps, its role may be limited in sessile lesions.28 This may be owing to technical factors, such as inability to safely obtain a deep margin, or because of the limitation of endoscopy in addressing the lymphatic spread in case of invasion. In our experience, the reasons for failure of endoscopic management of some of the cases harboring carcinoma were incomplete excision, long-term residual disease, and concern about the suitability of endoscopic excision in the setting of poor histologic features, such as lymphovascular invasion, or poor differentiation.
Finally, we would like to acknowledge several limitations of our study. First, ours was a retrospective study, and the follow-up period for each patient varied. Furthermore, the mean follow-up period for the entire group was 14 months and may not be sufficient to draw firm conclusions about the long-term effectiveness of endoscopic excision. Most colorectal polyps may take years to develop, and a longitudinal assessment for a longer period would be preferable and is necessary to stratify the risk of recurrence. Therefore, long-term control of invasive lesions by endoscopic resection can be addressed only by a larger study with long-term follow-up, such as a multi-institutional study or a national registry with a larger number of patients. In addition, the selection criteria for including patients in this study were subjective and based on the referring surgeon's perception of the endoscopic resectability of the lesion.
Although most large colorectal neoplasms require surgical resection, this study demonstrates that endoscopic excision of large colorectal polyps is technically feasible and safe. For a select group of patients, endoscopic excision is a viable alternative to colorectal resection. Surgeons' involvement in interventional endoscopy is critical to determine which patients can benefit from endoscopic excision vs those who need surgical resection. It is essential to gain an appreciation for the value of endoscopic excision but to also understand its limitations. When counseling patients who may benefit from endoscopic excision, keep in mind that endoscopic reintervention or surgical resection is needed in approximately one-third of patients. Prophylactic clipping of the polypectomy site of lesions in the ascending colon should be considered, and the effect on decreasing procedural complications, such as bleeding and perforation, should be further investigated. Long-term surveillance is warranted for all lesions in view of the risk of recurrence, especially for lesions located in the rectum.
Correspondence: Maher A. Abbas, MD, Center for Minimally Invasive Surgery, Kaiser Permanente, 4760 Sunset Blvd, Third Floor, Los Angeles, CA 90027 (email@example.com).
Accepted for Publication: April 27, 2010.
Author Contributions:Study concept and design: Kao, Giap, and Abbas. Acquisition of data: Kao, Giap, and Abbas. Analysis and interpretation of data: Kao, Giap, and Abbas. Drafting of manuscript: Kao and Abbas. Critical revision of the manuscript for important intellectual content: Giap and Abbas. Statistical analysis: Abbas. Administrative, technical, and material support: Kao and Giap. Study supervision: Giap and Abbas.
Financial Disclosure: None reported.
Previous Presentation: This paper was presented at the 81st Annual Meeting of the Pacific Coast Surgical Association; February 14, 2010; Maui, Hawaii.
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