Abstract
Background and study aims
Endoscopic full-thickness resection (EFTR) can be used to treat recurrent or residual colorectal adenomas. No data are available on treatment of recurrences after EFTR, especially on feasibility and safety of repeat EFTR (re-EFTR)
Patients and methods
This single-center retrospective study included patients who underwent device-assisted non-exposed re-EFTR in the colorectum. Technical success, adverse events (AEs), and recurrences were analyzed and compared to patients with primary EFTR.
Results
Twenty-seven patients who underwent re-EFTR were included. Median age was 75 years (range: 54–85 years) and nine patients were female (33.3%). The indication for re-EFTR was recurrent adenoma in 24 patients (88.9%) and most lesions were in the right-sided colon (n = 22; 81.5%). Technical success was achieved in 22 patients (81.5%). Reasons for failure were failure to reach the lesion in one case and inability to fully mobilize the lesion into the cap in four cases. Follow-up after 2 to 6 months revealed recurrent lesion in four of 24 cases (16.7%) and four more occurred during further follow-up. Surgery was necessary in two cases. AEs occurred in two cases (7.4%). Comparison with primary EFTR showed a trend toward lower technical success (81.5% vs. 100.0%, P = .051), but no differences in recurrence or AEs.
Conclusions
Repeat EFTR for recurrence after a previous EFTR is feasible in most patients and only a few patients require surgical resection. The rate of recurrence might be higher than that after primary EFTR, yet there are no differences in AEs.
Keywords: Endoscopy Lower GI Tract; Polyps / adenomas / ...; Endoscopic resection (polypectomy, ESD, EMRc, ...); Colorectal cancer
Introduction
Endoscopic resection is the mainstay of treatment for colorectal adenomas. Several resection techniques are available for different sizes and types of lesions. For large lesions, endoscopic mucosal resection (EMR) has long been the most widely used resection technique. However, with an increase in size and use of piecemeal resection, the rate of recurrence increases. In an Australian study of 1000 patients treated with wide-field EMR for large non-pedunculated colorectal polyps, recurrence after 4 months was 16% 1 . Tumor size, intraprocedural bleeding, and high-grade dysplasia have been identified as risk factors for recurrence after piecemeal resection 2 , whereas piecemeal resection is the strongest risk factor for recurrence after EMR 3 . Use of margin ablation has recently demonstrated to reduce risk of recurrence to 3% after 6 months, and its use is now recommended in international guidelines 4 5 . Use of endoscopic submucosal dissection (ESD) reduces risk of recurrence compared with piecemeal EMR, but at the costs of a higher adverse event (AE) rate 6 .
Treatment of a recurrent or residual lesion (RRL) is technically more challenging because of scarring from the previous resection. Endoscopic full-thickness resection (EFTR) with the Full-Thickness Resection Device (FTRD, Ovesco Endoscopy AG, Tübingen, Germany) allows for device-assisted, non-exposure EFTR in the colon and has successfully been evaluated for treatment of RRLs 7 8 9 . The prospective WALL RESECT study included 127 patients with difficult adenomas and benign histology 8 . In these cases, R0 resection was achieved in 77.7% and recurrence occurred in 18 of 117 patients (15.3%). Meta-analyses support data on R0 resection rate and also show high technical success of colonic EFTR 10 11 . This is further supported by a large registry study, which also provided data on recurrence during follow-up: Recurrence was detected in 13.5% of the cases, irrespective of indication for EFTR 12 . EFTR can be combined with EMR – so-called hybrid-EMR-EFTR – for which recurrence rates were reported to be 0% and 11.4% in two studies 13 14 . In the aforementioned studies, a wide variety of treatment modalities (e.g., forceps excision, snare resection, and EFTR) have been used to treat recurrent lesions after EFTR. However, no detailed analysis of how to treat RRL after previous EFTR is available, especially if repeated EFTR is feasible in these cases. Thus, the aim of this study was to evaluate repeat EFTR (re-EFTR) for RRL after the first EFTR.
Patients and methods
Study design
This retrospective, single-center study was conducted at RKH Hospital Ludwigsburg, Germany. The study included patients who underwent a second EFTR procedure in the colorectum using the FTRD. Patients were retrospectively identified from a database containing all device-assisted, non-exposed colorectal EFTR procedures performed with the FTRD since January 2015. All patients treated with primary EFTR between January 2015 and December 2022 who underwent re-EFTR were included in the study; no additional inclusion or exclusion criteria were applied. For the included patients, a retrospective chart review was conducted to gather data regarding baseline demographic and health characteristics, procedure details, and follow-up information.
Patients who underwent a single colorectal EFTR procedure were included in the control group after propensity score matching (PSM), as described below.
Outcome parameters
The outcome parameter was technical success, which was defined as reaching the target lesion with the FTRD mounted on the tip of the endoscope and successfully performing the resection. Further outcomes were resection status on histopathology, procedure-related AEs, recurrence at the first follow-up (after 2 to 6 months), and overall recurrence. Recurrence must be confirmed histopathologically. AE severity was graded according to the AGREE classification 15 .
Re-EFTR
Repeat EFTR procedure in the ascending colon. Histologically proven recurrent lesion in the ascending colon 15 months after first EFTR. This video clearly underscores the technical challenge in a case of re-EFTR. That is mainly related to pulling the lesion into the cap. Inadequate mobilization into the cap increases likelihood of the lesion slipping out of the cap during clip release and, thus, finally results in smaller resection specimens. In this case, the recurrent lesion was most likely already removed by forceps biopsy because no lesion could macroscopically be identified at time of re-EFTR and histopathology was negative as well.
Video 1
Re-EFTR was performed with the FTRD (Ovesco Endoscopy AG, Tübingen, Germany) in all cases. Technique for re-EFTR did not differ from primary FTRD resection in the colon and consisted of the following steps: 7 1) marking of the lesion’s borders; 2) introducing the endoscope with the mounted FTRD; 3) pulling the lesion into the cap using a grasping forceps or a tissue anchor; 4) deployment of the preloaded clip; and 5) resecting the lesion with the preloaded snare using electrocautery (High Cut, Effect 4.0, VIO 3 or VIO 300, ERBE Elektromedizin GmbH, Tübingen, Germany). Notably, if the clip from previous FTRD resection was still in place, this was removed using the remove System (Ovesco Endoscopy AG, Tübingen, Germany) during a first session and those patients underwent re-EFTR in a separate session. Because it is standard of care in our hospital to perform biopsies at the resection side and, if still in place, remove the clip during first follow-up colonoscopy, patients do not require additional colonoscopy for clip removal prior to re-EFTR in our institution ( Video 1 ).
Hybrid-EMR-EFTR: Technical aspects and criteria for usage
Hybrid-EMR-EFTR combines EMR with EFTR in a single-session procedure 16 . It is indicated for lesions with either a non-lifting part or suspicious area that are too large, i.e. > 20–25 mm for EFTR with the FTRD alone. Non-lifting parts are usually encountered during EMR but can be expected in large recurrent lesions due to scaring. The procedure starts with performing EMR of the lifting or non-suspicious parts. Once EMR is completed and only the non-lifting or suspicious area remains, the endoscope is withdrawn, the FTRD is mounted, and EFTR of that area is performed during the same session as described above.
Ethical considerations
This study was approved by the Ethics Committee of the Medical Faculty of Heidelberg University, Germany (study ID: S-624/2024, October 6, 2024) and conducted in accordance with the current version of the Declaration of Helsinki.
Statistical analysis
Categorical variables were reported as numbers (with relative frequencies) and compared using chi-square test or Fisher’s exact test, as appropriate. Continuous variables were reported as means (with range) and were compared using the Mann-Whitney test.
PSM was performed to balance distribution of the following baseline characteristics (i.e., the matched variables) in the two study cohorts: lesion size (maximum diameter in mm), location of the lesion within the colon, and indication for EFTR (e.g., recurrent adenoma). All analyses were performed using SPSS version 30.0 (IBM Corp., Armonk, New York, United States). Statistical significance was defined as P < 0.05.
Results
Study cohort and lesion characteristics
Between January 2015 and December 2022, we identified 234 primary EFTR procedures performed in the colorectum. Of these, re-EFTR was performed in 27 cases, all of which were included in the present study. Patient median age was 75 years (range: 54–85 years) and nine were female (33.3%). Of the 234 patients identified with primary EFTR, seven were referred for surgery for treatment of recurrence and one patient underwent ESD for recurrence of a rectal lesion after EFTR. Among the patients undergoing surgery were five with histopathologically confirmed carcinoma in the recurrent lesions.
Among the 27 included patients, the indication for Re-EFTR was recurrent adenoma in 24 patients (88.9%), residual adenoma in two patients (7.4%), and the last patient (3.7%) underwent re-EFTR for previously Rx resected T1 colorectal cancer. Median lesion size was 12 mm (range: 0–40 mm). It was in the right-sided colon in 22 (81.5%), left-sided colon in three (11.1%), and rectum in two patients (7.4%). The additional lesions and patient characteristics are summarized in Table 1 .
Table 1 Baseline demographic and health as well as procedure characteristics.
| A summary of all patient-related and lesion-related characteristics of the 27 patients included in the analysis who underwent re-EFTR is presented. CRC, colorectal cancer; EFTR, endoscopic full-thickness resection; EMR, endoscopic mucosal resection; HGD, high-grade dysplasia; LGD, low-grade dysplasia. | |
| Sex, female | 9 (33.3) |
| Age, years | 74 (54–85) |
| Comorbidities | |
| Coronary artery disease, n | 4 (14.8) |
| Diabetes, n | 3 (11.1) |
| Obesity (body mass index > 35 kg/m 2 ), n | 4 (14.8) |
| Immunosuppression, n | 2 (7.4) |
| Chronic kidney disease, n | 0 |
| Liver cirrhosis, n | 2 (7.4) |
| Medication | |
| Aspirin | |
| Discontinued, n | 2 (7.4) |
| Not discontinued, n | 6 (22.2) |
| Anticoagulant therapy | |
| Discontinued, n | 3 (11.1) |
| Lesion characteristics | |
| Indication for Re-EFTR | |
| Recurrent adenoma, n | 24 (88.9) |
| Residual adenoma, n | 2 (7.4) |
| Re-resection of CRC, n | 1 (3.7) |
| Lesion size, mm | 12 (0–40) |
| Location of lesion | |
| Coecum, n | 9 (33.3) |
| Ascending colon, n | 10 (37.0) |
| Transverse colon, n | 3 (11.1) |
| Descending colon, n | 1 (3.7) |
| Sigmoid, n | 2 (7.4) |
| Rectum, n | 2 (7.4) |
| Primary EFTR characteristics | |
| Time since first EFTR, months | 6 (1–70) |
| Indication for first EFTR | |
| Recurrent adenoma, n | 20 (74.1) |
| Residual adenoma, n | 6 (22.2) |
| CRC, n | 1 (3.7) |
| Use of hybrid-EMR-EFTR, n | 14 (51.9) |
| Lesion size, mm | 30 (5–100) |
| Resection status (R status) | |
| R0, n | 6 (22.2) |
| R1/R2, n | 4 (14.8) |
| Rx, n | 17 (63.0) |
| Histology | |
| No adenoma, n | 3 (11.1) |
| Adenoma with LGD, n | 13 (48.1) |
| Adenoma with HGD, n | 11 (40.7) |
Repeat EFTR procedure
Re-EFTR was technically successful in 22 of 27 cases (81.5%, Fig. 1 ). In one case, the lesion could not be reached with the mounted FTRD. This was due to a stenosis caused by the previous EFTR. The lesion was in the transverse colon. The patient underwent surgery and histopathology revealed invasive carcinoma, whereas biopsies prior to re-EFTR only showed high-grade dysplasia. In four cases scarring limited the ability to pull the lesions into the cap. Upon releasing the clip, the lesions slipped out of the cap and the preloaded snare slipped over the lesions. In these four cases, resection was completed using a separate snare. Thus, resection was completed in 26 of 27 cases (96.3%) and was macroscopically complete in all 26 cases. In nine cases (33.3%), a hybrid-EMR-EFTR procedure was performed. Median procedure time for all 27 patients was 71 min (range: 37–130 min).
Fig. 1.
Repeat EFTR procedure in two patients. a-d Use of the FTRD to perform re-EFTR in a patient with a recurrent lesion in the coecum. e-h Re-EFTR performed for recurrence after first EFTR in the ascending colon.
Histopathological outcomes
Histopathological examination of the 26 cases in which resection was performed revealed adenomas with low-grade dysplasia in 11 cases (42.3%) and adenomas with high-grade dysplasia in six cases (22.2%). In nine cases (34.6%), there was no residual adenoma within the resection specimen, despite histopathological proof of recurrence prior to re-EFTR in eight of these cases.
Resection status among the 17 patients with histopathological proof of adenoma was R0 and R1 in one case (5.9%) each and Rx in 15 cases (88.2%). Among the 15 cases with Rx resection, hybrid-EMR-EFTR was performed in seven patients, and in four patients, a second snare had to be used for resection because the preloaded snare slipped over the lesion (see above).
Adverse events
AEs occurred in two of 27 cases (7.4%). In one patient, postprocedural bleeding occurred the following day. The patient was successfully treated endoscopically using through-the-scope clips. This AE was classified as Grade 3a, according to the AGREE classification. One patient experienced pain on the day after resection which was treated with analgesics and this was classified as Grade 1. There were no intraprocedural AEs.
Follow-up
Follow-up colonoscopy within 2 to 6 months after resection was available for 24 patients (88.9%). Among the three cases with missing follow-up colonoscopy was the one patient who underwent surgery after failed re-EFTR. The FTRD clip spontaneously dropped off in 17 cases (70.8%) and was still in situ in seven cases (29.2%). There was a histopathologically confirmed recurrent adenoma in four of 24 cases (16.7%), whereas the remaining 20 cases (83.3%) did not show recurrence. Treatment was endoscopic in three cases and surgical resection in one. Endoscopic treatment was biopsy forceps excision in two with no further recurrence and EFTR in the last. This patient underwent multiple further endoscopic resections, including a fourth EFTR and EMR with hot avulsion, but finally was recurrence free. Of note, that patient already underwent hemicolectomy before first EFTR.
Any follow-up colonoscopy was available for 25 patients and during further follow-up, there were four more cases with recurrence detected at 12, 17, 26, and 38 months after re-EFTR. Three of them were treated endoscopically and surgery was performed in one patient who developed carcinoma 2 years after re-EFTR. Endoscopic treatment was EFTR in all three cases. Of them, one patient finally was free of recurrence, whereas one encountered recurrence and underwent surgical resection and the last underwent surgical resection for appendicitis following the third EFTR procedure. Patient outcomes are summarized in Fig. 2 . The total recurrence rate was eight in 25 cases (32.0%). Median follow-up after re-EFTR among all 27 cases was 9 months (range: 2–72).
Fig. 2.
Follow-up after repeat EFTR. Shown is the follow-up for all 27 patients included in the study. This includes the number of patients with occurrence of a recurrent or residual lesion (RRL) and its subsequent treatment. Data on first follow-up after 2 to 6 months as well as for overall follow-up are presented. *Includes one patient who underwent surgery after failed re-EFTR.
Comparison of repeat EFTR with repeat EFTR combined with EMR
As stated previously, a hybrid approach combining EMR and EFTR was used in nine patients (33.3%). In that group, there was a trend toward larger median lesion size (25 mm vs. 12 mm, P = 0.087) and longer median procedure time (80 min. vs. 70 min., P = 0.100).
No difference was noted regarding technical success (7/9 [77.8%] vs. 15/17 [88.2%], P = 0.591), intraprocedural AEs (0/9 [0%] vs. 0/17 [0%]), or postprocedural AEs (0/9 [0%] vs. 2/17 [11.8%], P = 0.529). There was a trend toward a statistically higher recurrence rate at first follow-up (1/16 [6.3%] vs. 3/8 [37.5%], P = 0.91). Numerically overall recurrence was higher as well, yet not statistically significant (4/16 [25.0%] vs. 4/9 [44.4%], P = 0.394).
Comparison of repeat EFTR with primary EFTR
Characteristics of patients and lesions with primary EFTR and re-EFTR are summarized and compared in Table 2 . In patients who underwent primary EFTR, technical success was achieved in all 27 cases (100.0%) compared with 22 of 27 cases (81.5%) in the re-EFTR group ( P = 0.051). Although R0 resection was numerically lower and recurrence was numerically higher in the re-EFTR group than in the control group, the difference was not statistically significant. No difference in AE rates was observed ( Table 3 ).
Table 2 Comparison of patients in the Re-EFTR and control groups .
| Re-EFTR group | Primary EFTR group | P | |
| Comparison of baseline demographic and lesion characteristics between the two study cohorts after propensity score matching. CRC, colorectal cancer; EFTR, endoscopic full-thickness resection. | |||
| Age, years | 75 (54–85) | 68 (47–84) | 0.010 |
| Sex, female | 9/27(33.3) | 10 / 27 (37.0) | 0.776 |
| Indication for Re-EFTR | > 0.999 | ||
| Recurrent adenoma, n | 24/27 (88.9) | 25 / 27 (92.6) | |
| Residual adenoma, n | 2/27 (7.4) | 1 / 27 (3.7) | |
| Reresection of CRC, n | 1/27 (3.7) | 1 / 27 (3.7) | |
| Lesion size, mm | 12 (0–40) | 15 (0–40) | 0.402 |
| Site of lesion | > 0.999 | ||
| Coecum, n | 9/27 (33.3) | 9 / 27 (33.3) | |
| Ascending colon, n | 10/27 (37.0) | 9 / 27 (33.3) | |
| Transverse colon, n | 3/27 (11.1) | 3 / 27 (11.1) | |
| Descending colon, n | 1/27 (3.7) | 1 / 27 (3.7) | |
| Sigmoid, n | 2/27 (7.4) | 2 / 27 (7.4) | |
| Rectum, n | 2/27 (7.4) | 3 / 27 (11.1) | |
Table 3 Comparison of repeat EFTR with first EFTR in the colorectum.
| Re-EFTR group | Primary EFTR group | P | |
| Outcomes in patients with re-EFTR and those who underwent their first colorectal EFTR. The results are shown as absolute frequencies (relative frequencies) or medians (range). AE, adverse event; EFTR, endoscopic full-thickness resection. | |||
| Technical success, n | 22/27 (81.5) | 27/27 (100.0) | 0.051 |
| Lesion reached, n | 26/27 (96.3) | 27/27 (100.0) | > 0.999 |
| Recurrence at 2–6 months, n | 4/24 (16.7) | 1/20 (5.0) | 0.198 |
| Overall recurrence, n | 8/25 (32.0) | 2/20 (10.0) | 0.147 |
| Resection status (R status) | 0.275 | ||
| R0, n | 10/26 (38.5) | 15/27 (55.6) | |
| R1, n | 1/26 (3.8) | 0 | |
| Rx, n | 15/25 (57.7) | 12/27 (44.4) | |
| Total AEs, n | 2/27 (7.4) | 6/27 (22.2) | 0.250 |
Discussion
To the best of our knowledge, this is the first study to evaluate feasibility and safety of repeated EFTR with the FTRD. Our findings indicate that re-EFTR for RRL after previous EFTR is generally safe and feasible for most patients.
Re-EFTR was technically successful in 81.5% of patients, and including four cases in which a separate snare was used after the preloaded snare slipped over the lesion, macroscopic complete resection was achieved in 96.3% of cases.
Treatment of RRL is mostly hampered by development of submucosal fibrosis and scarring, which makes repeat endoscopic resection more challenging. Various techniques have been proposed for treatment of RRL. EFTR was prospectively evaluated in 181 patients in the WALL RESECT trial, among whom 72 patients had RRL. Overall technical success and R0 resection rates were 89.5% and 76.9%, respectively 8 . Cold-forceps avulsion combined with snare-tip soft coagulation (CAST) has been used adjacent to EMR for treatment of non-lifting parts. In 38 patients with RRL, this resulted in 15.2% recurrence at first surveillance colonoscopy 17 . Finally, ESD can be used to treat RRL, as shown in a recent Japanese prospective analysis of 54 cases, with a mean lesion size of 16 mm. R0 resection was achieved in 83.3% 18 . ESD was compared with EFTR for treatment of RRL in two retrospective analyses. The first study by Yzet et al. showed similar results for RRL up to 20 mm in size, whereas ESD was superior regarding R0 resection for lesions > 20 mm 19 . This, however, is not surprising, given the known size limitation for EFTR with the FTRD of approximately 20 mm 8 . The second study by Barbaro et al. did not show any differences regarding en bloc resection and R0 resection between both groups, but found less perforations in the EFTR group 9 .
Although there are substantial data on RRL treatment in general, information regarding treatment of RRL following EFTR remains limited. Following EFTR, the recurrence rate was approximately 10% to 15% 8 12 20 . In a study reporting on long-term outcome, there were nine RRLs in 91 patients, of which six were treated endoscopically by either EMR or forceps polypectomy 20 .
Based on our experience, the most challenging aspect of treating recurrence after EFTR is scarring at the resection site. This makes re-EFTR technically more demanding, as reflected by the lower technical success rate for re-EFTR (81.5%) than for primary EFTR (100%). Technical failures were due to inability to pull the lesion into the cap and subsequent slipping of the preloaded snare. Scarring limits the extent to which the lesion can be mobilized into the cap, leading to smaller pseudopolyp formation above the clip and increasing risk of the preloaded snare slipping over the lesion (Supplementary video). Similar difficulties related to either snare resection or mobilization of the lesion into the cap have recently been described in detail in a large Italian retrospective analysis 21 . In our study, EFTR failure might have contributed to the higher recurrence rate in the re-EFTR group than in the control group, although this difference was not statistically significant. Despite the higher recurrence rate, only two patients required surgery.
Most importantly, there was no difference in the AE rate between re-EFTR and primary EFTR in this analysis. Further, the AE rate in the re-EFTR group was 7.4%, which is comparable to an AE rate of 11.3% shown in a large analysis on 1892 colorectal EFTR procedures with the FTRD 22 .
Interestingly, a hybrid-EMR-EFTR approach, combining EMR and EFTR, was used in one-third of cases (n = 9). This technique was first described by our group in a small series of 10 cases in 2017 16 . In 2023, our data on 75 cases were published, which demonstrated a technical success rate of 100% and macroscopically complete resection in 97.3% of the cases. Further, the AE rate was low (6.7%) and recurrence occurred in 11.4% of patients. Meanwhile, similar results were reported in three further studies, including some cases with a combination of EFTR and ESD 14 23 24 . In contrast, in this analysis, recurrence at first follow-up colonoscopy after hybrid-EMR-EFTR after a previous EFTR was as high as 37.5%.
This study was limited by its retrospective design as well as by its single-center design and small sample size. However, EFTR is a relatively new technique and no reports have focused on treatment of recurrences after EFTR. Further, it must be acknowledged that this study was conducted at a high-expertise center regarding colonic EFTR, and it is unclear to what degree the results can be transferred to non-expert centers. However, it should be noted that results from the German Colonic FTRD Registry, which included EFTR procedures from 65 hospitals throughout Germany, including mid-sized and smaller ones, showed similar results compared with the prospective WALL RESECT trial conducted at tertiary referral centers 8 12 . Nevertheless, recurrent lesions after EFTR warrant evaluation at a center with high expertise to decide whether repeat endoscopic resection is feasible.
Conclusions
In conclusion, repeat EFTR for recurrence after a previous colorectal EFTR is feasible in many patients. It is technically more challenging, and the recurrence rate might be higher, but there seems to be no difference in AE rate compared with primary EFTR, in this cohort. Further research should focus on treatment of recurrent or residual lesions after endoscopic resection.
Declaration of Generative AI and AI-assisted technologies in the writing process
During the preparation of this work the authors used Paperpal for grammar and language check. After using this tool, the authors reviewed and edited the content as needed and take full responsibility for the content of the publication.
Footnotes
Conflict of Interest AW recieved lecture fees and research grants from Ovesco Endoscopy AG and recieved lecture fees from Olympus. KC recieved lecture fees and research grants from Ovesco Endoscopy AG.
Contributorsʼ Statement Andreas Wannhoff: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Supervision, Writing - original draft. Khalid Takhgiriev: Conceptualization, Data curation, Formal analysis, Investigation, Writing - original draft. Remy Hosari: Data curation, Investigation, Validation, Writing - review & editing. Paul Hubbes: Data curation, Investigation, Validation, Writing - review & editing. Karel Caca: Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Validation, Writing - review & editing.
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