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Systematic Review and Meta-Analysis A systematic review on endoscopic ultrasound in gastric neuroendocrine neoplasms: guidelines outpacing evidence
Matteo Marasco1,2orcid, Gianluca Esposito1,2,3orcid, Marianna Signoretti1orcid, Maria Rinzivillo1orcid, Francesco Panzuto1,2,3orcid

DOI: https://doi.org/10.5946/ce.2024.343
Published online: April 24, 2025

1Digestive Disease Unit, Sant' Andrea University Hospital, ENETS Center of Excellence, Rome, Italy

2PhD School in Translational Medicine and Oncology, Department of Medical and Surgical Sciences and Translational Medicine, Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy

3Department of Medical Surgical Sciences and Translational Medicine, Sapienza University of Rome, Rome, Italy

Correspondence: Francesco Panzuto Digestive Disease Unit, Department of Medical Surgical Sciences and Translational Medicine, Sant' Andrea University Hospital, ENETS Center of Excellence, Sapienza University of Rome, Via di Grottarossa 1035, 11089 Rome, Italy E-mail: francesco.panzuto@uniroma1.it
• Received: December 15, 2024   • Revised: February 6, 2025   • Accepted: March 5, 2025

© 2025 Korean Society of Gastrointestinal Endoscopy

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Background/Aims:
    Gastric neuroendocrine neoplasms (g-NENs), though rare, have shown a rise in incidence due to increased endoscopic screening and improved diagnostic awareness. International guidelines recommend the use of endoscopic ultrasound (EUS) in managing g-NENs to evaluate subepithelial lesion size, depth, and lymph node involvement before endoscopic resection. However, the supporting evidence for EUS’s role in g-NENs is scarce and limited.
  • Methods:
    According to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines, a comprehensive literature search was conducted on PubMed to identify studies about the role of EUS in g-NENs, including both retrospective and prospective human studies.
  • Results:
    A total of 355 studies were considered; however, only seven were included, highlighting EUS’s diagnostic utility in g-NENs, with only 44 specific cases. EUS showed promise in assessing tumor characteristics critical for endoscopic resection. Nevertheless, its diagnostic accuracy remained variable across lesion types, and its impact on clinical decision-making in g-NENs lacked robust evidence. EUS contributed to subepithelial lesion staging but was underrepresented in neuroendocrine tumor-specific studies, creating a knowledge gap.
  • Conclusions:
    This review underscores the need for larger multicenter studies to validate EUS’s efficacy and reliability in g-NEN management. Prospective trials are crucial to strengthen guidelines and provide clearer clinical guidance for managing these tumors.
  • Keywords: Endoscopy; Neoplasm staging; Stomach neoplasms
Although considered rare, neuroendocrine neoplasms (NENs) of the stomach have shown a continuous epidemiological rise, with a steadily increasing incidence over recent decades.1 This trend is likely associated with the expanded use of endoscopic procedures, such as gastroscopy, now also performed for screening purposes, leading to a more significant incidental detection of these often-small lesions. Additionally, a heightened awareness and understanding of these neoplasms have undoubtedly facilitated their diagnosis.2 Like all NENs of the digestive tract, they are primarily classified histopathologically according to the 2022 World Health Organization classification based on differentiation and proliferative activity: well-differentiated neuroendocrine tumors (NETs) graded 1 to 3 according to the Ki-67 index—grade 1 (Ki-67 <3%), grade 2 (Ki-67 3%–20%), and grade 3 (Ki-67 >20%)—and poorly differentiated neuroendocrine carcinomas, which are inherently high-grade with a Ki-67 index over 20% and exhibit aggressive behavior.3
Gastric NENs (g-NENs) are further classified based on clinical presentation: type 1, associated with chronic atrophic gastritis; type 2, arising in the context of multiple endocrine neoplasia type 1 syndrome; and type 3, sporadic with no underlying associated pathology.4 The international guidelines by the European Neuroendocrine Tumor Society (ENETS) recommend an endoscopic management approach primarily based on tumor size and other specific characteristics, as detailed in Table 1.5 The optimal resection method to achieve complete removal of g-NENs has not been fully established. Similar outcomes have been reported with endoscopic mucosal resection and endoscopic submucosal dissection techniques6; both are suitable options and generally preferred over simple snare polypectomy, as this latter approach carries a high likelihood of yielding an R1 histological result, indicating incomplete resection. The same guidelines advocate for the use of endoscopic ultrasound (EUS) for local staging (depth of infiltration or lymph node involvement) before planning an endoscopic resection, with recommendations mainly determined by tumor size (Table 1).
Additionally, the European Society of Gastrointestinal Endoscopy (ESGE) recommends the use of EUS for g-NENs to characterize subepithelial lesions (SELs) in terms of size, location, originating layer, and other features.7 Finally, the American Society for Gastrointestinal Endoscopy (ASGE) guidelines recommend the use of EUS for local staging of g-NENs and a preliminary assessment prior to endoscopic resection without providing further specific details or more detailed guidance.8 The quality of evidence supporting this recommendation is reported as “moderate” (level 3 out of 4), although the literature supporting this recommendation is extremely weak, consisting of small retrospective series.
Clinical studies specifically focusing on EUS usage in the setting of g-NENs are generally lacking. Most scientific studies on EUS in NENs pertain to pancreatic NENs, with very limited data available on NENs originating from the stomach.
This systematic review aims to investigate and analyze the available scientific literature on the use of EUS in g-NENs to better understand the strength and robustness of guideline recommendations.
Search strategy
A systematic literature search was conducted on PubMed and Web of Science to identify studies relevant to the role of EUS in g-NENs. The search was performed using the following string: (“Endoscopic Ultrasound” OR “Endosonography” OR “EUS”) AND (“Neuroendocrine Tumors” OR “Neuroendocrine Neoplasms” OR “Carcinoid Tumor”) AND (“Stomach” OR “Gastric”). The search was conducted on January 27, 2025. The review followed the PRISMA guidelines9 and included both retrospective and prospective human studies, but was limited to articles written in English, with no restrictions on publication date or patient demographics.
After obtaining the search results, two authors (F.P. and M.M.) independently reviewed the records and excluded meeting abstracts, case reports or series, editorials, and review articles. The selection focused on identifying prospective or retrospective clinical studies specifically addressing the use of EUS in NENs of the stomach.
The literature search conducted according to the aforementioned criteria returned 355 records overall (140 from PubMed and 215 from Web of Science; Fig. 1). After carefully evaluating titles and abstracts, the vast majority were excluded because they consisted of reviews, articles outside the scope of the present study, meeting abstracts, case reports, or articles written in language other than English. This left a total of seven articles, for which the full texts were subsequently analyzed (Fig. 1). The main characteristics of the seven studies included in the final analysis are presented in Table 2.10-16
The study by He et al.10 examined the diagnostic accuracy of EUS in assessing small gastric SELs, comparing EUS-based presumptive diagnoses to definitive histological findings after resection. In a retrospective cohort of 224 patients, the analysis revealed that EUS allowed for detailed characterization of SELs by size, echogenicity, and layer of origin; EUS had an overall accuracy of 82.6% for determining the layer of origin of submucosal tumors, with accuracy rates of 72.4%, 82.6%, and 74.6% for tumors originating in the muscularis mucosae, submucosa, and muscularis propria, respectively. However, its diagnostic accuracy was limited. EUS achieved an accuracy of 45.5% when matched against histological outcomes, underscoring limitations in differentiating benign from malignant pathologies. The accuracy of EUS varied across lesion types, with correct diagnoses in 50% of pancreatic rests and leiomyomas and 100% of lipomas and NENs. However, the NEN subset included only three cases, limiting specific insights into EUS’s performance in these cases.
Varas et al.11 further explored the utility of EUS in identifying gastrointestinal NENs, specifically within gastroduodenal and colorectal regions, as candidates for endoscopic resection. Among 18 patients with 23 NENs (2–20 mm; mean, 8 mm), EUS showed high sensitivity (94%) in assessing tumor size, depth, and surrounding structures, thereby selecting suitable cases for minimally invasive resection. In cases where lesions were confined to the superficial layers without muscularis propria or nodal involvement, EUS-guided resection achieved complete resection in 90.5% of cases. In g-NENs, specifically, 13 cases demonstrated similar utility, in which EUS helped in identifying lesions appropriate for endoscopic resection based on depth and other features.
Costa et al.12 analyzed the role of EUS in staging and selecting treatment options for gastrointestinal NENs, focusing on 16 gastric cases in a cohort of 27 patients. EUS was helpful in assessing tumor depth, layer of origin, size, and perilesional lymph nodes, all critical factors in determining eligibility for endoscopic resection. In g-NEN cases, EUS identified well-demarcated, hypoechoic, homogeneous lesions primarily from the mucosal layer in 80% of cases and from the submucosa in 70%. The average tumor size was 7.6 mm, with tumors confined to the mucosal and submucosal layers deemed suitable for endoscopic resection.
De Angelis et al.13 investigated the application of EUS in diagnosing and managing gastrointestinal NENs in a cohort of 50 patients, specifically analyzing five g-NEN cases from a total of nine g-NENs included. EUS was employed to evaluate lesion depth, adjacent structure involvement, and lymph node metastasis. It demonstrated an accuracy of 75% in staging gastric NETs (g-NETs), accurately identifying confinement to the mucosa or submucosa, which was essential for determining suitability for endoscopic resection. EUS significantly impacted clinical management, altering treatment strategies in 63.6% of patients with NENs, such as by excluding residual disease after resection or identifying deeper tissue involvement requiring surgery. Despite these findings, the sample size of g-NENs remained limited, making it challenging to generalize EUS’s diagnostic and prognostic utility specifically for g-NENs.
Karaca et al.14 assessed the accuracy of EUS in diagnosing small gastric SELs, including NENs, in a retrospective analysis of 22 patients. Among SELs evaluated, only two were identified as gastric carcinoid tumors, limiting NEN-specific conclusions. EUS characterized lesion size, echogenicity, and layer of origin before resection, achieving a moderate accuracy of 45.5% overall. EUS performed better in identifying non-neoplastic lesions (66.7%) than neoplastic ones, such as NENs (30.8%).
Korkut et al.15 retrospectively investigated the contribution of EUS to the diagnosis of gastrointestinal SELs in 170 patients. The most common localization of SELs was in the stomach (67.1%), mainly in the gastric corpus and antrum. Most SELs were leiomyomas (51.2%), and NENs represented only 5.8% of cases with ten patients. Among patients with pathological biopsy samples (34.1%), 71.1% were accurately diagnosed using EUS (including only four cases of NENs). Particularly, the percentage of accurate diagnosis was 75% for NETs. Although the majority of lesions were localized in the stomach, the study lacked specific data and distinctions about g-NENs.
Finally, another older study by Zimmer et al.16 reported the sensitivity of diagnostic methods, mainly EUS, in localizing upper gastrointestinal NENs in 18 prospectively enrolled patients, with a total of 25 primary tumoral lesions histologically proven. Only one case corresponded to g-NEN; however, most were pancreatic NENs (n=17). This study described that EUS had the highest sensitivity (88%) for tumor detection compared to somatostatin receptor scintigraphy, computed tomography, transabdominal ultrasonography, and magnetic resonance imaging. Moreover, EUS proved to be particularly sensitive to lesions smaller than 2 cm in diameter. Considering that the majority of included NENs were pancreatic lesions, this last result could not be particularly extended and generalized to g-NENs.
Adding together the cases reported in each of the seven aforementioned studies, the total number of patients with g-NENs in whom the diagnostic accuracy of EUS was specifically assessed was 44, a very low figure derived from heterogeneous and consistently retrospective studies.
This study represents an attempt to consolidate the available data in the literature regarding the diagnostic accuracy of EUS in g-NENs. The need to conduct this review arose from the evident difficulty in identifying sufficiently robust scientific evidence to support the recommendations made by the ENETS,5 ESGE,7 and ASGE8 guidelines for EUS in this clinical context. Guidelines hold particular value for clinicians in a field such as NENs, on which clinical research is generally limited. NENs are rare, highly heterogeneous diseases, and there is a widely acknowledged need for multidisciplinary management that should ideally be referred to specialized centers.17 Thus, guidelines have added significance in influencing clinical decisions for managing these patients and are also often the foundation upon which scientific societies base their recommendations within position papers.18
Creating guidelines for rare adult solid cancers is complex due to the diversity of subtypes. EURACAN has advanced this effort by adopting and developing guidelines across multiple domains (including NENs) and extending their utility to international projects.19 Future priorities include regularly updating these guidelines and assessing their implementation, requiring extensive resources and data collection from patient registries. Patients with rare cancers face difficulties in diagnosis, treatment access, and participation in clinical trials due to their rarity and complexity.20
This need is particularly pertinent within g-NENs, in which three distinct tumor types (types 1, 2, and 3) present unique clinical behaviors and require different therapeutic approaches.4 In such a complex setting, guidelines act as a guiding light for clinicians who may lack extensive experience in managing these challenging cases. Thus, it is surprising that, despite the anticipated importance of these guidelines, the scientific literature supporting the recommendations on the use of EUS for g-NENs remains limited and fragile.10-14 Nevertheless, EUS has clearly taken on a crucial role in SEL management. Indeed, on upper gastrointestinal endoscopy, g-NENs often appear as multifocal pale small lesions that are flat or sessile with central erosion and likely clear demarcation line.21 EUS provides other essential information about the characteristics of g-NENs before choosing the most appropriate treatment. First, it establishes the precise size and wall involvement (deeper mucosa or submucosa), margins (usually rounded and sharp), and echogenicity (usually iso/hypoechoic intramural structure). Complementary methods such as contrast-enhanced ultrasound (hypervascular contrast during the early phase) and elastography are additional tools for improving the possibility of differential diagnosis (Fig. 2).7,22 Additionally, EUS is a reliable method for lymph node locoregional staging before treatment decision, although the diagnostic accuracy in this context has been more studied in gastric adenocarcinoma.23 Finally, EUS aids simultaneous deep biopsies for diagnostic confirmation.
However, there are no prospective studies, no adequately powered multicenter retrospective studies, nor randomized trials that have investigated how EUS might alter the management of g-NEN patients who are candidates for either endoscopic or surgical resection. The recommendations are thus based almost exclusively on expert opinions, typically from prominent scholars responsible for drafting the guidelines, or on evidence extrapolated from other tumor types, primarily gastrointestinal stromal tumors (GISTs) in the case of NENs.6 Frequently, studies include heterogeneous groups of patients with subepithelial gastric tumors, where NENs and GISTs are grouped together—an entirely unsound approach methodologically, as these are fundamentally different pathologies. This blending of different tumor types raises questions about the interpretability of EUS staging results and the true clinical relevance of such information for the long-term management of patients. This is one of the reasons why data from the current literature cannot be fully generalized and applied to the field of g-NENs; designing exclusive EUS and g-NEN studies is desirable.
The currently available data supporting the guidelines for using EUS in g-NENs are, therefore, not only scarce but also highly heterogeneous, calling into question the robustness of these recommendations. The analyzed studies present significant variability in design, patient populations, and diagnostic approaches, contributing to a fragmented and fragile evidence base. Given these limitations, larger multicenter studies are needed to produce high-quality data and uphold the scientific rigor of guidelines affecting their applicability in clinical practice. Future research must establish clear evidence-based criteria for EUS in g-NEN management to strengthen guideline development. Dedicated studies should evaluate whether EUS can effectively guide therapeutic decisions, including choosing between various resection techniques or surgery, to ensure radical treatment without undue risk to patients. It is crucial to create patient cohorts that are as homogeneous as possible, including only g-NETs, and to expend efforts to detail the diagnostic accuracy of EUS (even with the use of complementary tools explained above) compared with other available radiological diagnostic methods. The scientific community, at a minimum, would benefit from a simple prospective observational study following current guidelines (for instance, performing EUS on all type 1 NENs larger than 1 cm and all type 3 NENs before endoscopic resection) or even from a retrospective multicenter collection of data from high-expertise centers specializing in NEN management.
Indeed, this would be a paradoxical case of implementing a recommendation before accumulating supportive evidence. Nevertheless, such studies would help in bridging the clear cultural and knowledge gap that persists in the absence of this critical data.
Fig. 1.
Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow diagram.
ce-2024-343f1.jpg
Fig. 2.
Endoscopic evaluation of multiple type 1 gastric neuroendocrine neoplasms: white-light (A) and blue-light (B) imaging at upper gastrointestinal endoscopy; B mode (C) and contrast-enhanced (D) endoscopic ultrasound images.
ce-2024-343f2.jpg
ce-2024-343f3.jpg
Table 1.
Indication for endoscopic resection and EUS in g-NETs
Endoscopic resection EUS
Type 1 g-NET, <1 cm Not mandatory. Endoscopic surveillance is appropriate. Not required
Type 1 g-NET, 1–2 cm Endoscopic resection is required. EMR (m-EMR) or ESD are the preferred options. Required for assessing gastric wall involvement and to plan the optimal endoscopic resection
Type 1 g-NET, >2 cm Not indicated unless the patient is unfit for surgery Required to perform local tumor staging (e.g., lymph node assessment)
Type 3 g-NET Endoscopic resection may be an option when size <1 cm and low Ki-67; otherwise, surgery is required. Required for assessing gastric wall involvement and excluding lymph node metastases before planning endoscopic resection

EUS, endoscopic ultrasound; g-NET, gastric neuroendocrine tumor; EMR, endoscopic mucosal resection; ESD, endoscopic submucosal dissection.

Table 2.
Main characteristics of the seven studies included in the final analysis
Study Year Study design No. of patients (overall/g-NETs) Key finding
He et al.10 2016 Prospective 224/3 · EUS accuracy >80%
· Specific data for g-NETs are not assessable due to low patient numbers.
Varas et al.11 2010 Retrospective 18/13 · EUS is the preferred technique for selecting patients for endoscopic resection.
· Specific accuracy data for g-NETs are lacking.
Costa et al.12 2020 Not reported 27/16 · EUS diagnostic accuracy of 71% for gastrointestinal NETs
· No specific data on gastric NETs are reported.
De Angelis et al.13 1999 Retrospective 50/9 · EUS aids in the decision-making and management of GEP NETs.
· Limited and fragmented data on g-NETs are reported.
Karaca et al.14 2010 Retrospective 22/2 · EUS overall diagnostic accuracy of 45.5%
· No available data on g-NETs
Korkut et al.15 2022 Retrospective 170/10 · Overall EUS diagnostic accuracy of 71.1% in patients with histological samples of upper gastrointestinal SELs
· EUS diagnostic accuracy was 75% for neuroendocrine tumors (10 cases of NETs).
· No available specific data on g-NETs
Zimmer et al.16 1994 Prospective 18/1 · EUS sensitivity of 88% for tumor detection
· Most neuroendocrine lesions are pancreatic NETs.

g-NET, gastric neuroendocrine tumor; EUS, endoscopic ultrasound; NET, neuroendocrine tumor; GEP, gastroenteropancreatic; SEL, subepithelial lesion.

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      A systematic review on endoscopic ultrasound in gastric neuroendocrine neoplasms: guidelines outpacing evidence
      Image Image Image
      Fig. 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow diagram.
      Fig. 2. Endoscopic evaluation of multiple type 1 gastric neuroendocrine neoplasms: white-light (A) and blue-light (B) imaging at upper gastrointestinal endoscopy; B mode (C) and contrast-enhanced (D) endoscopic ultrasound images.
      Graphical abstract

      Fig. 1.

      Fig. 2.

      Graphical abstract

      A systematic review on endoscopic ultrasound in gastric neuroendocrine neoplasms: guidelines outpacing evidence
      Endoscopic resection EUS
      Type 1 g-NET, <1 cm Not mandatory. Endoscopic surveillance is appropriate. Not required
      Type 1 g-NET, 1–2 cm Endoscopic resection is required. EMR (m-EMR) or ESD are the preferred options. Required for assessing gastric wall involvement and to plan the optimal endoscopic resection
      Type 1 g-NET, >2 cm Not indicated unless the patient is unfit for surgery Required to perform local tumor staging (e.g., lymph node assessment)
      Type 3 g-NET Endoscopic resection may be an option when size <1 cm and low Ki-67; otherwise, surgery is required. Required for assessing gastric wall involvement and excluding lymph node metastases before planning endoscopic resection
      Study Year Study design No. of patients (overall/g-NETs) Key finding
      He et al.10 2016 Prospective 224/3 · EUS accuracy >80%
      · Specific data for g-NETs are not assessable due to low patient numbers.
      Varas et al.11 2010 Retrospective 18/13 · EUS is the preferred technique for selecting patients for endoscopic resection.
      · Specific accuracy data for g-NETs are lacking.
      Costa et al.12 2020 Not reported 27/16 · EUS diagnostic accuracy of 71% for gastrointestinal NETs
      · No specific data on gastric NETs are reported.
      De Angelis et al.13 1999 Retrospective 50/9 · EUS aids in the decision-making and management of GEP NETs.
      · Limited and fragmented data on g-NETs are reported.
      Karaca et al.14 2010 Retrospective 22/2 · EUS overall diagnostic accuracy of 45.5%
      · No available data on g-NETs
      Korkut et al.15 2022 Retrospective 170/10 · Overall EUS diagnostic accuracy of 71.1% in patients with histological samples of upper gastrointestinal SELs
      · EUS diagnostic accuracy was 75% for neuroendocrine tumors (10 cases of NETs).
      · No available specific data on g-NETs
      Zimmer et al.16 1994 Prospective 18/1 · EUS sensitivity of 88% for tumor detection
      · Most neuroendocrine lesions are pancreatic NETs.
      Table 1. Indication for endoscopic resection and EUS in g-NETs

      EUS, endoscopic ultrasound; g-NET, gastric neuroendocrine tumor; EMR, endoscopic mucosal resection; ESD, endoscopic submucosal dissection.

      Table 2. Main characteristics of the seven studies included in the final analysis

      g-NET, gastric neuroendocrine tumor; EUS, endoscopic ultrasound; NET, neuroendocrine tumor; GEP, gastroenteropancreatic; SEL, subepithelial lesion.

      Table 1.

      Table 2.

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