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Using Endoscopic Submucosal Dissection as a Routine Component of the Standard Treatment Strategy for Large and Complex Colorectal Lesions in a Western Tertiary Referral Unit

Emmanuel, Andrew, M.B.Ch.B., M.S., M.R.C.S.; Gulati, Shraddha, M.B.B.S., M.R.C.P.; Burt, Margaret, R.N.; Hayee, Bu’Hussain, B.Sc., M.B.B.S., Ph.D., F.R.C.P.; Haji, Amyn, M.A., M.B.B.Chir., M.Sc., M.D., F.R.C.S.

Diseases of the Colon & Rectum: June 2018 - Volume 61 - Issue 6 - p 743–750
doi: 10.1097/DCR.0000000000001081
Original Contributions: Endoscopy
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BACKGROUND: Colorectal endoscopic submucosal dissection results in high rates of en bloc resection, few recurrences, and accurate diagnosis, and it is useful in lesions with significant fibrosis. However, endoscopic submucosal dissection has not been widely adopted by Western endoscopists and the published experience from Western centers is very limited.

OBJECTIVES: This study aims to report the outcomes from a UK tertiary center using colorectal endoscopic submucosal dissection as part of a standard lesion specific treatment approach.

DESIGN: This was a retrospective study.

SETTING: The study was conducted in a tertiary referral unit for interventional endoscopy in the United Kingdom.

PATIENTS: A total of 116 colorectal lesions were resected using endoscopic submucosal dissection or hybrid endoscopic submucosal dissection in 107 patients.

MAIN OUTCOME MEASURES: Outcomes included complications, recurrence, requirement for surgery, en bloc and R0 resection.

RESULTS: One hundred sixteen lesions (mean size 58.8mm) were resected using endoscopic submucosal dissection (n = 58) and hybrid endoscopic submucosal dissection (n = 58). Eighty-two (70.7%) had failed attempts at resection (n = 58) or extensive sampling before referral. Twelve contained invasive adenocarcinoma; endoscopic resection was curative in 6. Only 2 of 6 patients with noncurative endoscopic resection agreed to surgery, and none had lymph node metastases. Six of 7 perforations were successfully treated with endoscopic clips. Where endoscopic submucosal dissection was used alone, en bloc resection was achieved in 93% and R0 resection was achieved in 91%. Two patients experienced recurrence; both were managed with endoscopic resection.

LIMITATIONS: This was a retrospective study. Procedures were planned as endoscopic submucosal dissection, but some may have been converted to hybrid endoscopic submucosal dissection and not recorded.

CONCLUSION: Colorectal endoscopic submucosal dissection can be used in a Western center as part of a standard lesion-specific approach to deliver effective organ-conserving treatment to patients with large challenging lesions. Lesion assessment in Western practice should be improved to reduce the incidence of prior heavy manipulation and to guide appropriate referral. See Video Abstract at http://links.lww.com/DCR/A601.

King’s Institute of Therapeutic Endoscopy, King’s College Hospital NHS Foundation Trust, London, United Kingdom

Funding/Support: None reported.

Financial Disclosures: None reported.

Correspondence to: Amyn Haji, M.A., M.B.B.Chir., M.Sc., M.D., F.R.C.S., King’s Institute of Therapeutic Endoscopy, King’s College Hospital NHS Foundation Trust, London, UK. E-mail: amynhaji@nhs.net

Endoscopic submucosal dissection (ESD) allows organ-preserving, en bloc, curative resection of large superficial neoplastic lesions and cancers with early submucosal invasion in the colon and rectum. Colorectal ESD is more technically challenging than upper-GI ESD because of difficulties in scope stability and manipulation and a higher risk of perforation because of the thin colonic wall.1 Nevertheless, there has been a proliferation in its use. In large series it has been shown to achieve high rates of en bloc resection of large lesions with low recurrence rates compared with endoscopic mucosal resection (EMR) and is thought to have the added advantage of providing more accurate pathological diagnosis and reducing the need for additional surgery.2–7

However, almost all these results are obtained from expert centers in Asia, primarily Japan.5 The adoption of ESD in Western practice has been limited because of its technical difficulty, steep learning curve, and the difference in training opportunities compared with Japan.8–10 There are concerns about the differences in outcomes and adverse events in Western compared with Japanese series,5,11–13 leading many Western endoscopists to favor EMR as a safer, technically less demanding, and more feasible strategy for treating most lesions.8,9,14

Endoscopic submucosal dissection, however, provides several advantages over EMR for appropriately selected patients. It allows en bloc resection of lesions at high risk of containing submucosal invasion and is a valuable technique in resecting lesions with profound submucosal fibrosis from previous resection or heavy manipulation, which is common in Western practice.15,16 It is likely that the use of ESD will increase in Western practice, but the patient population, referral patterns, case load for the few endoscopists performing ESD, and lesion characteristics are likely to be substantially different than in Eastern practice. It is therefore important to establish the safety and efficacy of incorporating ESD into the standard practice of a tertiary referral unit in the West. There are few published studies on colorectal ESD from Western centers, mostly involving small numbers of patients,17–20 and the larger prospective series include only rectal or rectosigmoid lesions.11,21,22 Nevertheless, the emerging trend is that excellent results can be achieved for ESD in the colorectum in Western centers.21–24

In this study, we report the outcomes from a UK tertiary referral center using colorectal ESD as an essential component of a pragmatic lesion and patient-specific treatment approach.

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METHODS

This was an observational study of consecutive patients undergoing colorectal ESD for any type of lesion at a tertiary referral center. Retrospective analysis of prospectively collected data was performed.

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Patients

Our interventional endoscopy unit is one of few such tertiary centers in the United Kingdom and receives patients from a wide geographical area. Endoscopic mucosal resection is practiced in the region, but all patients were referred from outside our service because the referring endoscopist decided the lesion was beyond the capabilities or resources of the referring institution. Patients who had ESD used as part of the resection strategy for colorectal lesions between July 1, 2010, and March 31, 2017, were included.

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Lesion assessment and selection

All lesions were evaluated using a standardized assessment process with magnification chromoendoscopy with indigo carmine and narrow band imaging using Olympus CF-H260AZL (Olympus, Tokyo, Japan) and Fuji EC-600Z (Fujifilm, Düsseldorf, Germany) colonoscopes. The assessment was supplemented with variable high-frequency miniprobe ultrasound (Fujifilm) to evaluate for deep invasion in cases where adenocarcinoma was suspected, for example, where Kudo pit pattern type V was identified, laterally spreading tumor (LST) nongranular type, and some LST granular mixed-nodular type lesions. All lesions were considered for endoscopic resection, with the exception of those with obvious deep invasion.

Figure 1 shows the decision-making process for selecting the resection technique appropriate to the lesion.

FIGURE 1

FIGURE 1

In general, ESD to achieve en bloc resection was considered mandatory for LST nongranular lesions and those with type Vi pit as a result of the high incidence of invasive elements in these lesions. Laterally spreading tumor granular mixed nodular lesions also have a significant incidence of adenocarcinoma that is almost always located under dominant nodular components or in depressed areas.25,26 En bloc resection using ESD was considered preferable for these lesions, and, at a minimum, ESD was used as part of a hybrid technique to ensure resection of the dominant nodules in 1 piece to avoid sectioning an area of adenocarcinoma, in keeping with recommendations from Japanese experts.27,28 Endoscopic submucosal dissection was also used to aid resection of recurrent or residual lesions, or lesions subjected to previous heavy manipulation. Figure 2 shows examples of lesion-specific selection of the resection technique.

FIGURE 2

FIGURE 2

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Procedure

Endoscopic submucosal dissection was performed by 3 experienced interventional endoscopists with prior training in ESD. Procedures were performed using PCF Q260JL (Olympus) with ST distal hood (Fujifilm), the ERBE electrosurgery device (Erbe Elekromedezin, Tübingen, Germany), and the FlushKnife (Fujifilm). Succinylated gelatine (Gelofusine; B. Braun, Crissier, Switzerland) with adrenaline and dyed with methylene blue was used for submucosal injection. A limited mucosal incision and trimming was performed followed by submucosal dissection under the lesion. The mucosal incision was then completed around the lesion. Depending on the size and location of the lesion and the presence of submucosal fibrosis, different strategies were used, including tunneling technique, pocket creation method, or clip with line to assist traction, which have been described elsewhere.29–31

Hybrid ESD involved submucosal dissection, usually to ensure resection of nodular components in 1 piece or to assist in the resection of scarred areas, followed by completion of the procedure by EMR. The resection bed was routinely examined after the procedure using magnification chromoendoscopy for any residual lesion.

Procedures were performed by using conscious sedation and analgesia with intravenous midazolam and fentanyl administered by the endoscopist. General anesthesia was only used if the patient was unable to tolerate the procedure under conscious sedation. Most patients were discharged home on the same day as the procedure.

Patients underwent surveillance endoscopy at 3 months (SC1) and 12 months (SC2), and thereafter were placed on a surveillance program as per national guidelines for adenoma surveillance if appropriate.

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Data and Statistics

Data collected included patient demographics, lesion location, size, morphology, Kudo pit pattern, type of resection, previous intervention, en bloc resection, complications, histopathology findings, recurrence, and requirement for surgery.

En bloc resection was defined as removal of the lesion in 1 piece. The resection was classified as R0 if histological examination confirmed complete resection of all margins, R1 if either vertical or lateral margins were involved, and Rx if the margins were uncertain. Prior heavy manipulation was defined as previous attempts at resection, extensive sampling (≥6 biopises), or tattoo placed into the base of the lesion.

Results are reported using means and standard deviation for continuous variables and frequencies for categorical variables. For comparisons between groups, categorical data were analyzed using the χ2 test, and means of continuous data were analyzed using the t test. Ethical approval for this study was granted by the National Research Ethics Committee.

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RESULTS

A total of 116 colorectal lesions were resected using ESD (n = 58) or hybrid ESD (n = 58) in 107 patients with a mean age of 72 years. The median procedure time was 125 minutes (range 30–360 minutes). Resection could not be completed in 2 other patients after an initial attempt. One patient had a known adenocarcinoma initially assessed as at least massive submucosal invasion, but the patient was not fit for surgery and wanted an attempt at endoscopic resection. The other lesion was deeply scarred from a previous failed transanal resection, and ESD was initially undertaken under general anesthetic so that conversion to transanal endoscopic microsurgery (TEM) could be undertaken if necessary. The procedure was successfully completed by TEM in the same sitting.

Table 1 shows the characteristics of the resected lesions. The mean size of resected lesions was 58.8 mm. Over 70% of lesions had prior failed attempts at resection or heavy manipulation. Only 11 lesions had not been biopsied or had a previous attempt at resection.

TABLE 1

TABLE 1

There were 12 cases of invasive adenocarcinoma. Six had minimal submucosal invasion, R0 resection margins, and no adverse histopathological features (lymphovascular invasion or tumor budding), and ESD was considered curative. Six resections were considered noncurative: 1 lesion had minimal submucosal invasion with R0 resection but tumor budding was evident; 5 lesions had massive submucosal invasion (2 with positive vertical margins (1 had vascular invasion) and 3 had R0 resections with no other adverse histopathological features). One patient was considered unfit for surgery and the remaining 5 patients were counseled to consider surgery. Only 2 agreed, and there were no residual tumor or lymph node metastases in either resection specimen. Of the 12 patients with invasive adenocarcinoma, 2 have subsequently died of unrelated causes, 3 returned to their referring institution and have not been followed by our unit, and 2 underwent surgery. The remaining 5 are to be followed up for the first 2 years with 6 monthly magnification chromoendoscopy, colonoscopic ultrasound of the scar, CT to assess for systemic recurrence, and MRI for rectal lesions. After this period they will have endoscopic surveillance at 3 years, then every 5 years, and CT every 6 months for 5 years. There have been no cases of local or distant recurrence of adenocarcinoma to date after a mean follow-up of 13 months (range 7–21 months).

Table 2 shows outcomes for resection using ESD. Eighty-five of 116 (73%) patients were successfully treated with day case procedures and did not require hospital admission. Sixty-seven percent of patients requiring admission were elective admissions for reasons such as assistance with bowel preparation in elderly frail patients, or general anaesthesia, and they were generally discharged the following day.

TABLE 2

TABLE 2

Postprocedure bleeding occurred in 5 patients (4.3%) with 2 requiring endoscopic reintervention. Only 1 patient required surgery for a perforation. This patient underwent en bloc resection of a LST nongranular pseudodepressed type lesion. Fibrotic tissue was encountered in the deep submucosa and a resection plane deep to this was undertaken in case it represented invasive adenocarcinoma. The ESD specimen showed a T1 SM3 lesion with a clear margin. There were no residual tumor or lymph node metastases in the surgical resection specimen.

A total of 17 patients were discharged from follow-up as a result of having surgery, extreme age or frailty, death, or declining follow-up. A further 5 patients had resection of recurrent lesions. Of the remaining patients, 85% had received at least 1 surveillance endoscopy. Recurrence occurred in 2 patients treated with ESD alone, and 10 patients treated with hybrid ESD after a mean follow-up of 12.4 months. All cases were managed endoscopically.

Table 3 shows outcomes in patients treated with ESD alone. En bloc resection was achieved in 93% with R0 resection confirmed on histological examination in 91%. Recurrence occurred in 2 (4.7%), one of which had been a piecemeal resection. Both were successfully treated with further endoscopic resection.

TABLE 3

TABLE 3

There were no significant differences in overall complications, perforation, surgery for any reason, en bloc resection rates, or R0 resection rates between lesions smaller than 50 mm and larger lesions ≥50 mm (Table 4).

TABLE 4

TABLE 4

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DISCUSSION

Several studies have shown that ESD to resect colorectal lesions results in high rates of en bloc resection, few recurrences, and potentially curative treatment of early submucosal cancers.2–5,7 However, these results are reported almost exclusively from Japanese or a few other Asian expert centers.5 Although EMR is widely used in Western practice,32,33 the adoption of ESD has been much slower and it is not commonly used in Western endoscopy units. Endoscopic submucosal dissection is a technically challenging procedure with significant potential risks, and some early Western series reporting high complication rates and lower en bloc resection rates compared with Japanese experts discouraged many from adopting the technique.12,34 However, the efficacy of ESD in achieving high rates of en bloc resection, providing good-quality histopathological specimens for accurate diagnosis, performing potential curative resection of early cancers, and resecting challenging lesions with submucosal fibrosis cannot be ignored. Evidence that colorectal ESD can be effectively incorporated into Western practice is slowly emerging, although to date there has only been 1 study involving a large number of patients.21 In the United Kingdom, for example, there has only been 1 small study, which was published over a decade ago, on the use of colorectal ESD.35

We have shown that colorectal ESD, for appropriately selected lesions and patients, can be safely and effectively incorporated into the standard practice of a Western interventional endoscopy unit. Where ESD was used alone, en bloc resection rates of 93% were achieved with a high rate of confirmed R0 resection and very few recurrences. Overall, there were few complications and only 1 patient (who had a deeply invasive submucosal cancer) required surgery for a perforation.

These results, particularly the low rate of surgical intervention, should be considered in the context of the lesion characteristics that may present substantial and unique challenges compared with those encountered in Eastern centers. In common with other Western countries, expertise in endoscopic diagnosis, the use of magnification, and knowledge regarding lesion classification and appropriate referral are lacking compared with Japan.9 These factors may have contributed to 2 important characteristics of the cohort in this study. First, there was a large mean lesion size of 5.8 cm, possibly because lesions are either detected later or referral is delayed. Second, over 70% of lesions had been subjected to previous failed attempts at resection or heavy manipulation. The resulting submucosal fibrosis in large lesions makes an already technically challenging procedure more difficult. This is in stark contrast to Japan where guidelines explicitly state the importance of avoiding even biopsy of lesions and stress the value of assessment using magnification for appropriate lesion selection.27

Despite this, there were few significant complications. Submucosal fibrosis increases the technical difficulty of the procedure and increases the risk of perforation and recurrence.36,37 The recurrence rate should, therefore, also be considered in the context of these challenging lesions. Where ESD was used alone, there were few recurrences. However, the higher recurrence rate for hybrid ESD could be considered acceptable for lesions of this size with such a high incidence of prior heavy manipulation, and these were all managed endoscopically. To date, there have not been any patients requiring surgery as a result of recurrence.

Another often stated disadvantage with ESD is that it involves hospital admission, often for several days.9,38 However, the majority of cases in this study were safely performed as day case procedures. Most patients who required hospital admission were admitted electively for reasons such as assisting with bowel preparation in elderly frail patients, which would have been the case even if the patients had piecemeal EMR performed.

A significant limitation to our study is its retrospective design and inherent selection bias. Although the strategy for resection will generally be decided before resection, some patients may have had procedures converted from an intended full ESD to a hybrid procedure. However, this is true of most published series on ESD, almost all of which are retrospective series. The few Western prospective series are also subject to selection bias in that only lesions suitable for the study may be selected, for example, limiting ESD to rectal lesions, and it is not always clear how many lesions were excluded from treatment for ESD. We feel that, by reporting both the use of ESD alone and hybrid ESD, we reflect the reality of the challenges of clinical practice, particularly in a setting where assessment and intervention before referral differ significantly from those in other published series on ESD. A one-size-fits-all approach to the use of ESD is not appropriate in this setting, for example, hybrid ESD may be more appropriate than persisting with en bloc ESD in elderly frail patients with extensive scarred lesions. The patients in this series underwent the most appropriate treatment as determined by the lesion characteristics, their medical comorbidities, physiological status, and personal preferences.

Some Western authors question the overall value of ESD given the proven safety and efficacy of EMR,8,14 but nevertheless acknowledge that ESD has an important role in resection of high-risk lesions and for recurrent or scarred lesions. As such, it is important to develop the technique in Western centers and establish if it can safely be incorporated into standard practice.

This study contributes to the limited but expanding body of evidence that colorectal ESD is feasible, safe, and effective in a Western tertiary center setting. Furthermore, these results were achieved while offering ESD as a component of a standard lesion and patient-specific treatment approach. The limited opportunities for training in ESD are a challenge for Western units. We supported, and followed, a “Western” training concept shared by other authors that involves the acquisition of considerable experience in diagnostic and interventional endoscopy (EMR) to develop sufficient handling skills and tip control, followed by ESD training on animal models, and then a period of observation of Japanese or other experts. Further experience on animal models is useful, and then gradual progression with human cases, under the guidance of a mentor, beginning in the rectum and then advancing onto more proximal lesions.10,39 As a result, many of the resections reported in this series are rectal lesions, although a significant proportion were successfully resected elsewhere in the colon. Although our unit also performs TEM, our approach is to attempt endoscopic resection for all rectal lesions without clear features of massive submucosal invasion. As a result, only 3 patients over the past 5 years have had rectal adenomas without submucosal invasion removed by surgery (TEM in all 3 cases) and none have been subjected to major segmental resection.40

We have shown that colorectal ESD can be used alone, or as part of a hybrid procedure, to deliver organ-conserving treatment to patients with large and extremely challenging lesions. Where ESD was used alone, en bloc resection and complications were comparable to results from Asian expert centers. As a result of the challenges and potential risks, the use of ESD should be reserved for expert practitioners. Meticulous lesion assessment and selection are essential. It will be important to improve knowledge regarding lesion assessment and selection in Western practice to guide appropriate referral to expert endoscopists and reduce the incidence of attempts at resection or extensive sampling before referral.

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Keywords:

Colorectal adenoma; Colorectal endoscopic submucosal dissection; Endoscopic resection; Endoscopic submucosal dissection

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