Abstract
Duodenal neuroendocrine tumors are relatively rare subepithelial tumors that arise from cells of the neuroendocrine system. Small duodenal neuroendocrine tumors can be treated endoscopically because of their low potential for metastasis. This study aimed to evaluate the clinical outcomes of conventional and underwater endoscopic mucosal resection for duodenal neuroendocrine tumors. Between March 2009 and March 2023, 15 patients with duodenal neuroendocrine tumors resected using conventional (n = 7) and underwater (n = 8) endoscopic mucosal resections were retrospectively enrolled. The median specimen size and median tumor size were 1.0 cm (interquartile range: 0.8–1.2 cm) and 0.6 cm (interquartile range: 0.4–0.6 cm), respectively. More than half of duodenal neuroendocrine tumors were located in the duodenal bulb (9/15, 60%). The en bloc and complete resection rates of both conventional and underwater endoscopic mucosal resections were 100%. Only one perforation event occurred in the conventional endoscopic mucosal resection group (14.3%). The patient with the perforation was treated with endoscopic clipping. The median follow-up period was 39.5 months (interquartile range: 19.5–57.3 months). There was no local recurrence or distant metastasis during the follow-up period. Underwater endoscopic mucosal resection is a safe and effective treatment option for small duodenal neuroendocrine tumors and is the preferred treatment option for flat-type duodenal neuroendocrine tumors.
Keywords: duodenal neuroendocrine tumor, underwater endoscopic mucosal resection
1. Introduction
Gastrointestinal (GI) neuroendocrine tumors (NETs) are rare neoplasms derived from cells of the neuroendocrine system beneath the epithelial layer.[1] Due to the widespread use of screening endoscopy, the detection of GI NETs is steadily increasing.[2] Most GI NETs are asymptomatic and are usually discovered incidentally during endoscopy for unrelated conditions.[3] The most frequent site for NETs is the rectum, followed by the stomach.[4] Rectal and gastric NETs <10 mm in size and confined to the submucosa have a low risk of lymph node metastasis.[5] For these lesions, endoscopic resection may be the optimal treatment modality because of the improved quality of life due to organ preservation compared to surgical resection.
Duodenal NETs are found less frequently than rectal and gastric NETs, accounting for <5% of all GI NETs.[4] The risk of lymph node metastasis from duodenal NETs is also known to be low.[6,7] The rich peripheral blood flow and thin duodenal wall compared to the rectum and stomach increase the difficulty of endoscopic resection.[8] Consequently, surgical resection is the preferred treatment option over endoscopic resection.[9] Recent advances in endoscopic techniques and equipment have improved the ability to perform endoscopic resection of small duodenal NETs.[10,11] Although the optimal treatment for duodenal NETs remains controversial due to their rarity, several studies on endoscopic resection for duodenal NETs <10 mm in size and confined to the submucosa have reported good long-term prognosis.[2,7,12]
Modified endoscopic mucosal resection (EMR), such as ligation-assisted, cap-assisted, and precut methods, and conventional EMR (C-EMR) are considered for the treatment of small duodenal NETs.[2] Modification of C-EMR enhances treatment performance for GI subepithelial tumors (SET).[13] However, injection of fluid into the submucosa during the procedure can cause SET to sink deeper under the epithelium. Snare capture of tumors with submucosal fibrosis can be disturbed by dam formation around the lesion after submucosal injection, which can lead to a failure of capturing the tumor. In contrast, underwater EMR (U-EMR) fills the lumen with water to lift the lesion, thereby avoiding the difficulties that occur after submucosal injection in flat lesions. U-EMR without submucosal injection showed a similar R0 resection rate and shorter procedure time than endoscopic submucosal dissection (ESD) for rectal NETs.[14] Notably, there have been case reports of successful U-EMR for duodenal NETs.[15–17] Hence, this study aimed to compare the clinical outcomes of C-EMR and U-EMR for duodenal NETs.
2. Materials and methods
This retrospective study was approved by the ethics committee of the Pusan National University Yangsan Hospital Institutional Review Board and performed in accordance with the Declaration of Helsinki. Obtaining written consents was waived because of the retrospective aspect of this study. We retrospectively reviewed electronic medical records from March 2009 to March 2023, and enrolled patients who underwent resection of duodenal NETs using either C-EMR or U-EMR. The procedure was performed between March 2009 and August 2018 in the C-EMR group, and between January 2019 and September 2022 in the U-EMR group (Fig. 1). C-EMR and U-EMR were performed by experienced endoscopists with >5 years of experience performing upper endoscopy.
Figure 1.
Flow chart of patients included in the study. EMR, endoscopic mucosal resection; NET, neuroendocrine tumors.
In the U-EMR group, a 15 mm polypectomy snare through an endoscope (Olympus GIF-290 or GIF260, Tokyo, Japan) using an Endo Cut Q current (effect: 3, cut duration: 2, cut interval: 3) generated using a VIO 300D electrosurgical unit (Erbe Elektromedizin GmbH, Tübingen, Germany) was used. The amount of water instilled in the U-EMR was based on the endoscopist’s experience; however, enough water is usually infused to allow the lesion to float.
Duodenal NETs were grossly classified according to the Paris classification: those larger than the closed cup of the biopsy forceps (2.5 mm) were classified as Ip, Is, or Isp according to the presence or absence of a neck or in-between; and lesions smaller than the closed cup of the biopsy forceps (2.5 mm) were classified as IIa, IIb, or IIc according to whether they were elevated, flat, or depressed, respectively.[18,19] Procedure time was defined as the time from the start of endoscopic injector insertion to the completion of resection in the C-EMR group, and the time from the infusion of water into the lumen to the completion of resection in the U-EMR group.
2.1. Statistical analysis
The Mann–Whitney U test and Fisher exact test were used to analyze the data. The median values were used to represent the statistical central tendency, and the interquartile range was used to express the statistical distribution. The statistical analysis was performed using the IBM SPSS software for Windows, version 21.0 (IBM Corp., Armonk).
3. Results
The baseline patient characteristics are shown in Table 1. A total of 15 patients (C-EMR, n = 7 patients; U-EMR, n = 8 patients) were included in the study. The average age was 51.9 years, and the median age was 55.0 years. Regarding the location of the lesions, over half were found in the bulb, 9 in the first part of the duodenum (60.0%), and 6 in the second part (40.0%). The morphological features were classified as type I (2/15, 13.3%), Isp (7/15, 46.7%), IIa (5/15, 33.3%), and IIb (1/15, 6.7%). In relation to surface changes, erosions and depressions were found in 7 and 11 cases, respectively, and there were no ulcerations observed. Forceps biopsy was performed before resection in 14 patients. Histological biopsy results before endoscopic resection indicated NET in 9 cases, suspicion of NET in 1 case, and inflammation in 4 cases. One patient underwent endoscopic resection for diagnosis and treatment without a biopsy. Endoscopic ultrasonography was performed in 13 patients (86.7%), and all cases revealed a hypoechoic submucosal tumor originating from the second or third layer. No cases of lymph node metastases were observed on abdominal computed tomography. Only one patient in the C-EMR group was taking antiplatelet medications (acetylsalicylic acid). The mean follow-up period was 43.5 months (median, 39.5 months).
Table 1.
Baseline characteristics of patients with duodenal neuroendocrine tumor.
| Age, yr, median (IQR) | 55.0 (45.0–60.0) |
| Gender, male/female, n (%) | 10/5 (66.7/33.3) |
| Characteristics of lesions | |
| Location of lesions, n (%) | |
| 1st portion | 9 (60.0) |
| 2nd portion | 6 (40.0) |
| Lesion size, cm (IQR) | 0.6 (0.4–0.6) |
| Specimen size, cm (IQR) | 1.0 (0.8–1.2) |
| Morphology of lesions, n (%) | |
| Is | 2 (13.3) |
| Isp | 7 (46.7) |
| IIa | 5 (33.3) |
| IIb | 1 (6.7) |
| Features of the surface of NET, n (%) | |
| Erosion | 7 (46.7) |
| Depression | 11 (73.3) |
| Ulceration | 0 (0) |
| Previous biopsy result, n (%) | |
| NET | 9 (60.0) |
| Suspicious of NET | 1 (6.7) |
| Inflammation | 4 (26.7) |
| Biopsy, not performed | 1 (6.7) |
| Percentage of patients taking antiplatelet or anticoagulation agents, n (%) | |
| Antiplatelet agents | 1 (6.7) |
| Follow-up period, median mo, (IQR) | 39.5 (19.5–57.3) |
Abbreviations: IQR, interquartile range; NET, neuroendocrine tumor.
In the comparison of the gross morphology, the Isp type was the most prevalent morphology in the C-EMR group (5/7, 71.4%), followed by IIa (2/7, 28.6%). In the U-EMR group, there were 2 Isp types (25.0%), 2 Is types (25.0%), 3 IIa types (37.5%), and 1 IIb type (12.5%). When comparing the locations of the lesions, the C-EMR group had 2 lesions (28.6%) in the first part of the duodenum and 5 (71.4%) in the second part, whereas the U-EMR group had 7 lesions (87.5%) in the first part and 1 (12.5%) in the second part.
A comparison of treatment outcomes between the C-EMR and U-EMR groups is presented in Table 2. The procedure time in the C-EMR group was significantly longer than in the U-EMR group (15.8 min vs 3.6 min, P = .013). The tumor size and resected specimen size were 0.7 cm and 1.1 cm, respectively, in the C-EMR group and 0.5 cm and 1.0 cm, respectively, in the U-EMR group (P = .232 and P = .613, respectively). En bloc resection and complete endoscopic resection was achieved in all cases in both C-EMR and U-EMR groups. The pathologic complete resection rates were 57.1% in the C-EMR group (4/7) and 62.5% in the U-EMR group (5/8) (P = 1.000). For pathologically incomplete resections, both the C-EMR and U-EMR groups consisted of 2 vertical margin positives and 1 indeterminate margin involvement each (3/7, 42.9% and 3/8, 37.5%, respectively). Regarding NET grade, in the C-EMR group, 5 cases were grade 1 (71.4%), and 1 was grade 2 (14.3%). In the U-EMR group, all 8 cases were grade 1 (100%). No lymphovascular or perineural invasions were observed in either group.
Table 2.
Treatment outcomes of conventional endoscopic mucosal resection and underwater endoscopic mucosal resection for duodenal neuroendocrine tumors.
| C-EMR (n = 7) | U-EMR (n = 8) | P-value | |
|---|---|---|---|
| Procedural time, min (IQR) | 15.8 (10.3–20.0) | 3.6 (2.2–5.8) | .013 |
| Lesion size, cm (IQR) | 0.7 (0.5–0.8) | 0.5 (0.4–0.8) | .232 |
| Specimen size, cm (IQR) | 1.1 (1.0–1.2) | 1.0 (0.7–1.3) | .613 |
| En bloc resection, n (%) | 7 (100) | 8 (100) | 1.000 |
| Endoscopically complete resection, n (%) | 7 (100) | 8 (100) | 1.000 |
| Pathologically complete resection, n (%) | 4 (57.1) | 5 (62.5) | 1.000 |
| Margin involvement or indeterminate, n (%) | 3 (42.9) | 3 (37.5) | .833 |
| Grade, n (%) | |||
| Grade 1 | 5 (71.4) | 8 (100) | .429 |
| Grade 2 | 1 (14.3) | 0 (0) | |
| Mitosis, n (%) | |||
| 0/10 HPF | 2 (28.6) | 7 (87.5) | .054 |
| 1/10 HPF | 5 (71.4) | 1 (12.5) | |
| Ki67, n (%) | |||
| 1% | 3 (42.9) | 6 (75.0) | .281 |
| 2% | 3 (42.9) | 2 (25.0) | |
| >2% | 1 (14.3) | 0 (0) | |
| Lymphovascular invasion, n (%) | 0 (0) | 0 (0) | − |
| Perineural invasion, n (%) | 0 (0) | 0 (0) | − |
| Perforation, n (%) | 1 (14.3) | 0 (0) | .467 |
| Bleeding, n (%) | 0 (0) | 0 (0) | − |
Abbreviations: C-EMR, conventional endoscopic mucosal resection; U-EMR, underwater endoscopic mucosal resection; IQR, interquartile range; HPF, high-power field; −, not available.
One complication occurred in the C-EMR group, which was a microperforation treated with endoscopic clipping. There was no significant difference in the perforation rate between the 2 groups (14.3% vs 0%, P = .467). No bleeding-related complications were observed in either group. No recurrences were observed during the follow-up period.
4. Discussion
Due to the high likelihood of perforation, ESD of duodenal NET is not as utilized, while EMR is usually adopted to resect duodenal NET.[20–23] Modified EMR methods have been introduced to increase the complete resection rate and the safety of the procedure. Herein, we evaluated a novel technique, U-EMR, for resecting duodenal NET and compared it to C-EMR.
U-EMR was first introduced in 2012 as a novel technique for the resection of colorectal polyps.[24] Submucosal injection in C-EMR provides a safety margin,[25] which often makes capturing lesions with a snare difficult. On the other hand, U-EMR floats the submucosal layer using the buoyancy of water immersion without submucosal injection. If the lesion floats while submerged, a conventional snare grabs it and transmits electricity to the cut. Many studies have reported the usefulness and safety of U-EMR.[26–28] In this study, we demonstrated the benefits of U-EMR for duodenal NET resection. The main difficulty in duodenal EMR is due to the thin duodenal wall, which many surgeons are reluctant to resect deep enough to avoid perforation, eventually resulting in incomplete resection. With the buoyancy in U-EMR, resection with sufficient submucosal capture can be achieved without submucosal injection. The U-EMR group had a statistically significant shorter procedure time compared to the C-EMR group in this study (median procedural time, 3.6 min vs 15.8 min, respectively, P = .013). Theoretically, skipping the submucosal injection and easy snare capture of the tumor could reduce the total procedure time, leading to a reduction in the workload of endoscopists.
No local recurrence or distant metastasis was observed during the follow-up period after U-EMR. According to previous studies related to GI NET, the recurrence rates after endoscopic complete resection, although pathological margins are involved, are allowable if the degree of NET grade is favorable.[29–31] The absence of recurrence, even in cases with unclear or indeterminate resection margins, is most likely related to the nature of duodenal NETs. U-EMR has advantages over other EMR methods, especially flat-type SET or SET with fibrosis. Submucosal injection could hide flat-type SET (Fig. 2A–C) and SET with fibrosis (Fig. 3A–C), which makes it difficult to capture the lesion using a snare. In our center, we have 2 cases of perforation when resection duodenal NET by modified EMR. Initially, we attempted to perform C-EMR, but encountered difficulties in snaring the lesion after submucosal injection. Despite the switching to modified EMR (ligation and precut EMR), the surrounding submucosal injection impeded the adequate capture of the lesion, resulting in excessive capturing and subsequent perforation occurred. U-EMR can overcome the difficulties induced by submucosal injection, especially for flat lesions (see Video S1, Supplemental Digital Content, http://links.lww.com/MD/N981, which demonstrates the technique of using U-EMR for the flat lesion). With the help of buoyancy, U-EMR could increase visibility during the process of capturing the lesion compared to C-EMR (Fig. 4). Although there have been some case reports of successful U-EMR for duodenal NETs, the strength of this study is that it is the first comparison between C-EMR and U-EMR.
Figure 2.
The effect of submucosal injection for a flat duodenal neuroendocrine tumor. (A) A duodenal neuroendocrine tumor was observed in the bulb. (B) The tumor sunk after submucosal injection. (C) The schematic descriptions show the difficulties in resecting a flat neuroendocrine tumor after submucosal injection, which could hinder the capture of the subepithelial tumor by sinking the tumor during conventional endoscopic mucosal resection.
Figure 3.
The effect of submucosal injection for a duodenal neuroendocrine tumor with submucosal fibrosis. (A) A duodenal neuroendocrine tumor with submucosal fibrosis was located at the superior descending angle. (B) The tumor did not lift after the submucosal injection. (C) The schematic descriptions show the difficulties in resecting a tumor with submucosal fibrosis after submucosal injection, which could disturb the capture of the subepithelial tumor by dam formation around the tumor during conventional endoscopic mucosal resection.
Figure 4.
Underwater endoscopic mucosal resection for a duodenal neuroendocrine tumor. (A) During underwater endoscopic mucosal resection, buoyancy can help the lesion float. The duodenal neuroendocrine tumor was located next to the ampulla. (B) The tumor floated after the water was instilled. (C) Visibility was maintained during tumor capture using a snare. (D) The schematic diagrams show the underwater endoscopic mucosal resection of duodenal neuroendocrine tumors.
However, there are several limitations to this study, including its single-center retrospective design and small number of patients, due to endoscopists at our center being more likely to perform modified EMR than C-EMR for NET with a flat morphology until 2018. Modified EMR was considered when complete resection of the NET was expected to be difficult. This means that the successful resection and complication rates of C-EMR may have been overestimated. Subsequently, U-EMR was used for endoscopic resection in all duodenal NETs. The single-center design and rarity of duodenal NETs resulted in a small sample size, which limits the power of the conclusion of this study. The short follow-up period (median, 39.5 months) is an also limitation of the study. This is attributed to the fact that C-EMR was introduced at our center after 2018, and because the vast majority of patients were asymptomatic, follow-up losses were frequent. To draw definitive conclusions regarding the usefulness of U-EMR for the endoscopic treatment of duodenal NET, a large-scale multicenter study is needed.
In conclusion, U-EMR is effective, safe, and has a short procedure time for the resection of small duodenal NETs. U-EMR can be a preferred endoscopic resection technique over C-EMR for non-protruding NETs in the duodenum.
Acknowledgments
Statistical analysis was performed with the assistance of the Department of Medical Statistics, Institute of Biomedical Science and Technology Convergence, Pusan National University Yangsan Hospital.
Author contributions
Conceptualization: Tae Un Kim, Su Jin Kim.
Data curation: Jin Ook Jang, Cheol Woong Choi, Dae Gon Ryu, Su Bum Park, Jung Wook Lee.
Formal analysis: Jin Ook Jang, Cheol Woong Choi, Dae Gon Ryu, Su Bum Park, Jung Wook Lee.
Supervision: Tae Un Kim.
Writing – original draft: Jin Ook Jang, Su Jin Kim.
Writing – review & editing: Tae Un Kim, Su Jin Kim.
Supplementary Material
Abbreviations:
- C-EMR
- conventional endoscopic mucosal resection
- EMR
- endoscopic mucosal resection
- ESD
- endoscopic submucosal dissection
- GI
- gastrointestinal
- NET
- neuroendocrine tumor
- SET
- subepithelial tumors
- U-EMR
- underwater endoscopic mucosal resection
The authors have no funding and conflicts of interest to disclose.
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Supplemental Digital Content is available for this article.
How to cite this article: Jang JO, Kim TU, Choi CW, Ryu DG, Park SB, Lee JW, Kim SJ. Comparison of clinical outcomes between conventional and underwater endoscopic mucosal resection for duodenal neuroendocrine tumors. Medicine 2024;103:47(e39988).
Contributor Information
Jin Ook Jang, Email: lookingforhelpingpeoplelive@gmail.com.
Cheol Woong Choi, Email: drluckyace@pusan.ac.kr.
Dae Gon Ryu, Email: gon22gon@naver.com.
Su Bum Park, Email: psubumi@daum.net.
Jung Wook Lee, Email: teaterry@hanmail.net.
Su Jin Kim, Email: endoksj@gmail.com.
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