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DOI: 10.1055/a-1811-7025
Endoscopic submucosal dissection for superficial gastrointestinal lesions: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2022
- Main recommendations
- 1 Introduction
- 2 Methods
- 3 Pretreatment evaluation
- 4 Therapeutic options
- 5 Management after endoscopic resection
- 6 Surveillance after endoscopic resection
- 7 Pathological aspects
- Disclaimer
- References
Main recommendations
ESGE recommends that the evaluation of superficial gastrointestinal (GI) lesions should be made by an experienced endoscopist, using high definition white-light and chromoendoscopy (virtual or dye-based).
ESGE does not recommend routine performance of endoscopic ultrasonography (EUS), computed tomography (CT), magnetic resonance imaging (MRI), or positron emission tomography (PET)-CT prior to endoscopic resection.
ESGE recommends endoscopic submucosal dissection (ESD) as the treatment of choice for most superficial esophageal squamous cell and superficial gastric lesions.
For Barrett’s esophagus (BE)-associated lesions, ESGE suggests the use of ESD for lesions suspicious of submucosal invasion (Paris type 0-Is, 0-IIc), for malignant lesions > 20 mm, and for lesions in scarred/fibrotic areas.
ESGE does not recommend routine use of ESD for duodenal or small-bowel lesions.
ESGE suggests that ESD should be considered for en bloc resection of colorectal (but particularly rectal) lesions with suspicion of limited submucosal invasion (demarcated depressed area with irregular surface pattern or a large protruding or bulky component, particularly if the lesions are larger than 20 mm) or for lesions that otherwise cannot be completely removed by snare-based techniques.
ESGE recommends that an en bloc R0 resection of a superficial GI lesion with histology no more advanced than intramucosal cancer (no more than m2 in esophageal squamous cell carcinoma), well to moderately differentiated, with no lymphovascular invasion or ulceration, should be considered a very low risk (curative) resection, and no further staging procedure or treatment is generally recommended.
ESGE recommends that the following should be considered to be a low risk (curative) resection and no further treatment is generally recommended: an en bloc R0 resection of a superficial GI lesion with superficial submucosal invasion (sm1), that is well to moderately differentiated, with no lymphovascular invasion, of size ≤ 20 mm for an esophageal squamous cell carcinoma or ≤ 30 mm for a stomach lesion or of any size for a BE-related or colorectal lesion, and with no lymphovascular invasion, and no budding grade 2 or 3 for colorectal lesions.
ESGE recommends that, after an endoscopically complete resection, if there is a positive horizontal margin or if resection is piecemeal, but there is no submucosal invasion and no other high risk criteria are met, this should be considered a local-risk resection and endoscopic surveillance or re-treatment is recommended rather than surgery or other additional treatment.
ESGE recommends that when there is a diagnosis of lymphovascular invasion, or deeper infiltration than sm1, or positive vertical margins, or undifferentiated tumor, or, for colorectal lesions, budding grade 2 or 3, this should be considered a high risk (noncurative) resection, and complete staging and strong consideration for additional treatments should be considered on an individual basis in a multidisciplinary discussion.
ESGE recommends scheduled endoscopic surveillance with high definition white-light and chromoendoscopy (virtual or dye-based) with biopsies of only the suspicious areas after a curative ESD.
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This Guideline is an official statement of the European Society of Gastrointestinal Endoscopy (ESGE). It is an update of the previous 2015 Guideline addressing the role of endoscopic submucosal dissection (ESD) for superficial gastrointestinal lesions.
Abbreviations
1 Introduction
This Guideline represents an update of the Guideline on the role of endoscopic submucosal dissection (ESD) for superficial gastrointestinal (GI) lesions, published by the European Society of Gastrointestinal Endoscopy (ESGE) in 2015 [1].
This evidence-based Guideline was commissioned by ESGE. It addresses major issues concerning ESD, that is, evaluation before ESD, comparison with other therapeutic strategies, namely endoscopic mucosal resection (EMR) and surgery, and management after ESD, to inform and underpin the use of this fundamental technique for the treatment of superficial GI lesions.
This Guideline does not address the skills and knowledge that the endoscopist should have to perform ESD, or the specific management of antithrombotic or other medications in the periprocedural setting, or quality measurements, as these are addressed in separate guidelines [2] [3]. A companion Technical Review will be published separately, that will cover prevention strategies regarding ESD complications and detailed technical issues.
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2 Methods
ESGE commissioned this Guideline and appointed a guideline leader (P.P.N.) who invited the listed authors to participate in its development. The key PICO (patients, interventions, controls, outcomes) questions were prepared by the coordinating team (P.P.N., J.v.H., M.D.R.) and then approved by the other members. The coordinating team formed organ-based task force subgroups, each with its own leader, and divided the key topics (pretreatment evaluation, treatment, management after treatment) among these task forces (see Appendix 1 s, available online-only in Supplementary Material).
Each task force performed a systematic literature search to prepare evidence-based and well-balanced statements on their assigned key questions, with a focus on articles published from January 2015 until January 2021, after the literature review of the previous ESD guideline. Searches were performed in PubMed. Articles were first selected by title; their relevance was then confirmed by review of the corresponding manuscripts, and articles with content that was considered irrelevant were excluded. All selected important articles were individually assessed and graded by the level of evidence and strength of recommendation, according to the GRADE system [4] [5].
Each task force proposed statements on their assigned key questions which were discussed and voted on at a virtual meeting in February 2021. In August 2021, new relevant articles published up till that date were considered and reviewed, and a draft prepared by the leaders and coordinating team was sent to all group members. Statements were only approved when the consensus was greater than 80 %. [Table 1] gives a complete list of statements.
The manuscript was also reviewed by two members of the ESGE Governing Board and sent for further comments to the national societies and individual members. After agreement on a final version, the manuscript was submitted to the journal Endoscopy for publication. All authors agreed on the final revised manuscript.
Evidence tables created from the literature review are presented in the Supplementary Material of this Guideline (Table 1 s, Esophageal squamous cell carcinoma (SCC); Table 2 s, Barrett’s esophagus (BE); Table 3 s, Stomach; Table 4 s, Duodenum; Table 5 s, Colorectum).
Organ-specific decision algorithms are presented in [Figs. 1–4].
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This Guideline was issued in 2022 and will be considered for review and update in 2027 or sooner if new and relevant evidence becomes available. Any updates to the Guideline in the interim will be noted on the ESGE website: http://www.esge.com/esge-guidelines.html.
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3 Pretreatment evaluation
3.1 Endoscopic evaluation
1 ESGE recommends that the evaluation of superficial gastrointestinal lesions should be done by an experienced endoscopist, using high definition white-light and chromoendoscopy (virtual or dye-based), and validated classifications when available.
Strong recommendation, high quality evidence.
Successful curative resection of a superficial GI lesion can only be achieved by precise characterization of the lesion, optimal delineation of tumor margins, and estimation of depth of invasion, and this can only be correctly assessed by experienced endoscopists. The morphology of all visible lesions should be described using the Paris classification since this gives an indication of the likelihood of invasive cancer [6].
Considering the increased availability of virtual chromoendoscopy (CE) techniques, the absence of side effects, shorter duration of the procedure, and similar or better accuracy in detecting and delineating the resection margins of lesions, as compared to dye-based CE, virtual CE (complementing high resolution white-light endoscopy [WLE]) should be the standard of care for pretreatment evaluation of superficial GI lesions [7].
3.1.1 Esophageal squamous cell carcinoma (SCC) lesions
The 2015 ESGE guideline recommended virtual CE (narrow-band imaging [NBI], blue-light imaging [BLI]) as an alternative to Lugol CE (LCE) for the detection of superficial esophageal SCC. Both methods have been proven to be more accurate than WLE alone [1]. CE provides a high diagnostic rate in evaluating the esophagus to diagnose SCC. A meta-analysis showed that NBI has comparable sensitivity to that of LCE (88 % vs. 92 %), but superior specificity (88 % vs. 82 %, P < 0.001) [8]. The higher specificity was confirmed in a prospective randomized trial, even when the technique was used by nonexperts [9]. A recent study compared LCE with NBI for delineation of tumor mucosal margins before endoscopic resection of SCC, and found no difference in the complete lateral resection rate [10]. Thus, virtual CE appears to be the optimal method for detection and delineation of esophageal SCC, with the more cumbersome LCE remaining as an option.
For determining depth of invasion also, WLE appears to be suboptimal when compared to virtual CE [11]. The Japan Esophageal Society (JES) proposed a new simplified magnifying endoscopy (ME)-CE classification for estimating the depth of invasion of superficial esophageal SCC [12]. The JES classification categorized the lesions according to the type of microvessels: type A microvessels without severe irregularity correspond to noncancerous/low grade dysplastic lesions; type B microvessels with severe irregularity are suggestive of cancerous lesions. Type B is further divided into three categories: B1 corresponds to high grade intraepithelial neoplasia or intramucosal carcinoma m1 or m2; B2 to carcinoma invading the muscularis mucosae/m3 or sm1; and B3 to at least sm2 tumors. The overall accuracy of type B microvessels for predicting tumor invasion depth was 90.5 % [12]. Most studies using this classification show an overall accuracy exceeding 80 %–90 %, and excellent interobserver agreement (over 0.85). Performance is excellent with type B1 tumors (88.6 %; sensitivity 71.4 %, specificity of 100 %), and type B3 tumors (90.0 %; sensitivity 75 %, specificity 97.8 %) [13] [14]. All these studies used ME-NBI, but a recent trial reported similar accuracies with ME-blue-light imaging (BLI) with concordance between ME-NBI and ME-BLI of 91.2 % [15]. Based on these studies we propose that the newly developed JES classification is useful in estimating the invasion depth of superficial SCC and, even though no study has been reported in the West, it can be considered in clinical practice.
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3.1.2 Barrett’s esophagus (BE)-associated lesions
Although early esophageal neoplasia in BE generally presents as subtle flat lesions that may be difficult to detect, most procedures performed with high resolution endoscopes do reveal these abnormalities to the experienced eye [16] [17]. Both virtual CE and acetic acid dye-based CE are easy to learn and interpret. Criteria have been developed in the new PREDICT classification to diagnose Barrett’s neoplasia according to focal loss of acetowhitening and surface patterns of Barrett’s mucosa [18]. Concerning acetic acid, a recent meta-analysis showed that pooled sensitivity, specificity, and positive and negative likelihood ratios (with 95 % confidence intervals [95 %CIs] shown in parentheses), for the diagnosis of high grade dysplasia (HGD) and Barrett’s adenocarcinoma for all the included studies (9 studies, 1379 patients) were 0.92 (0.83–0.97), 0.96 (0.85–0.99), 25.0 (5.9–105.3), and 0.08 (0.04–0.18), respectively [19].
The BING working group developed a simple, internally validated system to identify dysplasia and esophageal adenocarcinoma (EAC) in patients with BE, based on NBI results. When images are assessed with a high degree of confidence, the system can classify neoplasia within Barrett’s with > 90 % accuracy and a high level of interobserver agreement [20]. However, a recent study showed that its sensitivity and positive predictive value for the diagnosis of dysplasia may be low in daily practice [21].
These studies suggest that both CE methods are valuable tools with excellent performance when used by experienced observers and should be used for evaluation of Barrett’s dysplasia, alone or simultaneously.
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3.1.3 Stomach lesions
Diagnosis and evaluation of early gastric cancer (EGC) lesions is clearly improved by CE when compared to WLE [22]. Virtual CE with ME has high accuracy in delineating horizontal margins before ESD and performs equally well as or better than dye-based CE [23] [24] [25]. CE has also the potential for predicting EGC differentiation [26] [27]. Several studies also suggest that CE can be used for prediction of depth of invasion, with a blurry mucosal and irregular mesh pattern suggesting submucosal invasion, with a global accuracy superior to 80 % [27] [28] [29] [30]. However, no validated classification exists nor is there any study suggesting that CE is better than standard high resolution WLE for this purpose, and the decision not to endoscopically resect the lesion is still based mainly on macroscopic features of the lesion ([Fig. 3]).
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3.1.4 Duodenal lesions
Data are scarce on the pretherapeutic evaluation of duodenal neoplasia. In a single-center trial the ability of virtual CE to distinguish adenoma from intramucosal cancers was evaluated, with a mixed or absent pattern having 72 % accuracy with moderate interobserver agreement (kappa 0.59) [31]. Endoscopic prediction of invasion depth of early duodenal neoplasia has never been compared with that of EUS, CT, or other imaging modalities, and therefore pre-ESD staging is still based on endoscopic evaluation [32].
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3.1.5 Colorectal lesions
In patients with large colorectal laterally spreading tumors (LSTs) resected endoscopically, the risk of pathological T1 cancer can be predicted on the basis of the laterally spreading tumor (LST) subclassification and tumor diameter [33]. To determine the indication for ESD or EMR, overall judgment based on the subclassification of LST, vessel, surface, and pit pattern diagnosed by means of CE observation is useful. Distinction between adenoma and adenocarcinoma can be achieved with high accuracy using high resolution endoscopy and CE observation [34] [35]. For this purpose, NICE (NBI International Colorectal Endoscopic) and JNET (Japan NBI Expert Team) classifications have been associated with high accuracy in determining the histology of the lesion [36] [37]. Thus, the indication for EMR, ESD or surgery will be made on macroscopic morphological features and on more detailed features assessed by advanced imaging techniques (see [Fig. 4]) [38] [39]. The latter were recently addressed in an ESGE guideline [40].
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3.2 Endoscopic ultrasonography and other modalities
2 ESGE does not recommend routine performance of endoscopic ultrasonography (EUS), computed tomography (CT), magnetic resonance imaging (MRI), or positron emission tomography CT (PET-CT) prior to endoscopic resection (ER).
Strong recommendation, moderate quality evidence.
3 ESGE suggests that when suspicious features for deep submucosal invasion are present, complete staging should be considered in order to exclude stage T2/T3 or lymph node metastasis (LNM).
Weak recommendation, low quality evidence.
3.2.1 Esophageal SCC lesions
Given the results shown with endoscopy, particularly when complemented with virtual magnifying endoscopy with chromoendoscopy (ME-CE), the role of other staging modalities, including EUS, CT, MRI, or PET-CT, is doubtful in lesions with estimated depth of invasion of T1 m3–sm1 or less.
A meta-analysis performed in 2016 confirmed the limitations of EUS in detecting submucosal invasion, with pooled sensitivity and specificity for T1 versus T2–4 tumors of 77 % (95 %CI 73 %–80 %) and 95 % (95 %CI 94 %–96 %), respectively. Among the T1 tumors, EUS had a pooled sensitivity in distinguishing between T1a and T1b of 83 %–84 % (95 %CI 80 %–88 %), and a specificity of 89 % (95 %CI 86 %–92 %) [41]. In the largest retrospective study focusing on EUS overstaging, the rate of overstaged pTis–T1a was 39.5 % [42].
Several reports and a meta-analysis compared accuracy outcomes between EUS and ME-NBI, showing comparable results [43] [44]. In one of these reports, the sensitivity and accuracy of ME-NBI in distinguishing m1–m2 from m3 /sm1 and from more deeply invasive SCCs was significantly higher than that of EUS (P = 0.048 and P = 0.017, respectively) [44]. Recent studies have emphasized the relevance of MRI and PET-CT with regard to T1 lesions, showing a high accuracy of MRI compared to EUS and CT [45] [46], and a possible role for PET-CT in identifying T1a lesions when no uptake can be seen in the esophageal wall [47], but these studies need further validation. Nevertheless, since PET-CT is a standard staging method for advanced SCC, the combined use of PET-CT and high resolution CE, especially with microvascular findings of types B2 and B3, may be useful to determine whether ER is indicated for the lesion [48]. When the lesion is visible on PET, a therapeutic modality other than ER should be considered [47].
In summary, ME-CE is superior to WLE alone in estimating depth of invasion for esophageal SCC, and has at least a similar overall staging accuracy compared with EUS, without the limitations of EUS such as the risk of overstaging early endoscopically curable disease. JES type B2–B3 lesions or lesions with distinct features, such as nodular protrusion, ulceration, and depressed areas, should be considered to have the risk of submucosal invasion and are most likely to benefit from additional staging procedures such as EUS and PET-CT.
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3.2.2 Barrett’s esophagus (BE)-associated lesions
A meta-analysis of EUS staging of superficial esophageal adenocarcinoma (EAC) showed favorable pooled values for mucosal cancer staging, but unsatisfactory diagnostic results for EAC at the esophagogastric junction [49]. Even in lesions suspicious for malignancy (nodular or depressed lesions), resection of the lesion with histological examination had greater utility than staging by EUS [50]. Hence, EUS appears to be of limited utility in accurate staging of BE patients with high grade dysplasia (HGD) or early EAC [51]. Nevertheless, if deep submucosal invasion is suspected endoscopically, then complete staging should be performed with EUS, CT, and/or PET-CT.
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3.2.3 Stomach lesions
The use of abdominal CT or PET-CT in the staging of endoscopically resectable early gastric cancer (EGC) does not have an established role because of the very low risk of distant metastasis. Moreover, perigastric adenopathy may be a nonpathological finding that can jeopardize ER. Regarding the use of these techniques in order to assess the feasibility of ESD in EGC, in recent years only a few studies have tried to use CT or PET-CT to predict the curability of EGC by ER; they have shown differing results, with an accuracy for CT scan of 60 % [52] whilst PET-CT showed sensitivity, specificity, PPV, and NPV of 79 %, 91 %, 81 %, and 89 %, respectively [53].
The role of EUS in the staging of EGC is also debatable. In a recent meta-analysis, for invasion depth EUS showed sensitivity and specificity of 0.87 (95 %CI 0.86–0.88) and 0.67 (95 %CI 0.65–0.70), respectively. The overall overstaging rates for m1–3 and sm1 tumors by EUS were 13.3 % and 32.8 %, respectively, while the overall understaging rate for sm tumors was 29.7 %. The total misdiagnosis rates for EUS were 30.4 % for lesions ≥ 2 cm and 20.9 % for lesions < 2 cm, 27.7 % for ulcerative lesions and 21.4 % for nonulcerative lesions, and 22 % for differentiated lesions and 26.9 % for undifferentiated lesions [54]. Globally, the overall accuracy varied from 71.5 % [55] to 95 % [56].
It should be noted that endoscopy alone (even without CE) has almost 80 % accuracy in determining curability by ER, with several prediction models described to decide between ESD or surgery, with good results published in the literature [57] [58] [59]. Moreover, ESD does not preclude the possibility of subsequent surgery and should be seen as the most definitive T-staging modality.
To conclude, EUS, CT, or PET do not add to endoscopic evaluation alone, they have significant rates of over- and understaging, and cannot be recommended routinely, particularly for lesions that are considered endoscopically resectable.
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3.2.4 Colorectal lesions
A subset analysis of a multicenter randomized controlled trial (RCT) comparing CE with EUS for staging of early colorectal cancer (CRC) showed no advantage of EUS over CE, with a global accuracy of 78 % for both techniques [60]. Since the 2015 guideline, four new meta-analyses have been published that address the diagnostic accuracy of EUS, CT, and MRI. Overall, with indirect comparison, no significant differences in T or N staging could be found between CT, MRI, or EUS, in the setting of a newly diagnosed rectal lesion that is being considered for endoscopic therapy. Accuracy in distinguishing T1 from T2 cancers is limited for both EUS and MRI, with a serious risk for overstaging [61] [62] [63] [64].
Based on those studies we recommend that all colorectal lesions should be described according to laterally spreading tumor (LST) type, CE features, and location, in order to predict the risk of submucosal invasion and, hence, choose the best therapeutic option. EUS and/or MRI may have a role in the rectum when suspicious features of submucosal invasion are present. As ER might create inflammatory lymph nodes around the rectum, in these cases staging should preferably be done before any eventual resection; however, in cases with T-stage discrepancy between optical evaluation and EUS/MRI, the endoscopic evaluation should carry greater weight. Complete staging is recommended in lesions with optical features for deep submucosal invasion.
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4 Therapeutic options
4.1 Esophageal SCC lesions
4 ESGE recommends ESD as the treatment of choice for most esophageal squamous cell and gastric (or junctional non-Barrett’s) superficial lesions, mainly to provide an en bloc potentially curative resection with accurate pathologic staging.
Strong recommendation, moderate quality evidence.
5 ESGE suggests that ESD might also be considered for en bloc resection of noncircumferential clinically staged T1a-m3/T1b-sm1 or for circumferential clinically staged T1a-m1/m2 esophageal squamous cell carcinoma (SCC).
Weak recommendation, moderate quality evidence.
Numerous studies evaluating long-term outcomes after ESD for superficial esophageal cancer have been published since the 2015 guideline [65] [66] [67]. Following ESD for lesions limited to the epithelium (m1) or the lamina propria (m2), the 5-year disease-specific survival (DSS) and 5-year overall survival (OS) rates were reported to be 98 %–100 %, and 85 %–95 %, respectively. Thus such lesions represent an absolute indication for ER [66].
Two issues are still debated regarding T1 tumors. The first concerns the role of ER as first-line treatment for noncircumferential esophageal SCC that has preoperatively been clinically staged as cT1a-m3/T1bsm1 (N0M0). The second concerns ESD for superficial SCC involving the entire circumference of the esophagus.
There are no available European data covering these two topics, but the most recent Japan Gastroenterological Endoscopy Society (JGES) guideline suggests that ESD is weakly recommended as first-line treatment for preoperatively clinically diagnosed cT1a-m3/T1b-sm1 noncircumferential esophageal SCC. It is also weakly recommended for clinically diagnosed cT1a superficial SCC with a major axis length ≤ 50 mm and involving the entire circumference of the esophagus, upon implementation of preventive measures for stenosis [68]. A recent study adds evidence to these recommendations, showing that almost 60 % of endoscopically predicted T1a-m3/T1b-sm1 tumors involving less than three-quarters of the circumference can be cured by ER alone but if the lesion is circumferential then the ESD curability rate drops to less than 20 % [69].
4.1.1 Comparison with endoscopic mucosal resection (EMR)
There is no randomized study comparing EMR with ESD for SCC, but several new European reports have confirmed the efficacy and the superiority of ESD compared to EMR already stated in the previous 2015 guideline [10] [67] [70] [71]. In a French trial, the complete resection rates for the ESD group and the EMR group were, respectively, 97.1 % versus 85 % (P < 0.01), and the 5-year disease-free survival rates were, respectively, 95.2 % versus 73.4 % (P < 0.01) [71]. In an older meta-analysis of retrospective studies, ESD had higher en bloc and curative resection rates than EMR regardless of lesion size [72]. Thus ESD seems superior to EMR in the treatment of SCC as evidenced by significantly higher en bloc and curative resection rates and by a notably lower local recurrence rate [73].
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4.1.2 Comparison with surgery
Three recent articles compared the outcomes of ESD and surgical resection for pT1 esophageal SCC, all of which were single-center, retrospective studies. A report from Shanghai [74]. found fewer treatment-related deaths in patients in the ESD compared with the surgery group, although the difference was not significant (0.3 % vs. 1.5 %, P < 0.186). Furthermore, there were significantly fewer severe complications in the ESD group than in the surgical resection group (15.2 % vs. 27.7 %, P < 0.001). Post-treatment stenosis was more common in the ESD group but the difference was not significant (13.4 % vs. 9.9 %, P < 0.203). However, in the ESD compared with the surgical resection group, treatment duration and length of hospital stay were significantly shorter (49 min vs. 240 min, P < 0.001, and 3 days vs. 11 days, P < 0.001, respectively) and the cost of hospitalization was significantly lower (median 2813 US dollars [USD] vs. 10 001 USD, P < 0.001). There was no significant difference between the two groups in terms of all deaths, disease-specific death rates, or metastasis rates, over a median observation period of 21 months, including in the patients with T1b tumors. Similarly, a report from Korea [75] found no difference between the ESD and surgical resection groups after mean observation periods of 43 and 63 months, respectively, in terms of OS, DSS, or recurrence-free survival. Another report from Shanghai [76] that specifically addressed outcomes according to invasion depths concluded that ESD oncologic outcomes were comparable to those achieved with esophagectomy, but were associated with minimal invasion, lower cost, and lower incidence of serious adverse events. However, in sm2/sm3 tumor patients, the ESD R0 resection rates were lower than those of esophagectomy [76].
Long-term outcomes were recently analyzed in a systematic review and meta-analysis that included 3796 patients and 5 comparative studies [77]. In terms of the comparison between ESD and esophagectomy, there was no difference in the OS (86.4 % vs. 81.8 %; hazard ratio 0.66, 95 %CI 0.39–1.11) as well as in DSS and recurrence-free survival. In addition, ESD was associated with fewer adverse events (19.8 % vs. 44.0 %; odds ratio 0.3, 95 %CI 0.23–0.39).
ER is, therefore, considered safer and less invasive than surgical resection in patients with pT1 cancers, as well as being superior in terms of medical economics. Furthermore, patients are likely to prefer ER over surgical resection. Hence, balancing the benefits of organ preservation and the harm of postoperative complications, ESD should be recommended as first-line therapy for selected lesions (if a tumor classification no more severe than T1b-sm1 is expected).
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4.1.3 Comparison with chemoradiotherapy (CRT)
In a phase II trial (JCOG9708) [78] of CRT including 72 patients with cT1N0M0 esophageal SCC, over 90 % of patients achieved a complete response, with a 4-year OS rate of 80.5 %. However, local recurrences were observed in 31 % of patients, with a 4-year DSS rate of only 52.8 %. More recently, a retrospective study of definitive CRT in 36 patients with T1bN0M0 esophageal SCC found that local and metastatic recurrences were common, with a 5-year OS rate of 86 % and a 5-year DSS rate of 59 % [79].
Data from the JCOG9708 trial [78] showed that adverse events of grade ≥ 2 included dyspnea in 11.1 %, esophagitis in 2.7 %, ischemic heart disease in 2.7 %, myocarditis in 2.7 %, and arrhythmia in 1.4 % of patients. The abovementioned recent report found grade ≥ 2 adverse events that included esophageal stenosis in 11 % and pleural effusion in 14 % of patients, with grade 4 pericardial effusion in 3 % and grade 5 pneumonia in 3 % of patients [79]. The benefit and harm profiles of ESD and CRT therefore differ.
However, the benefit–harm balance of ESD limited to patients with superficial cancers appears superior to that of CRT, reflecting the minimal invasiveness of ESD. Thus, if either ESD or CRT is indicated, we recommend ESD as the first-line treatment and CRT as a possible after-treatment option. Nevertheless, ESD is also technically feasible in patients with local failure after CRT, especially as an initial salvage treatment and as treatment for second primary lesions within the irradiation field [80].
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4.2 Barrett’s esophagus (BE)-associated lesions
6 For BE-associated lesions, ESGE recommends to use EMR for ≤ 20 mm visible lesions with low probability of submucosal invasion (Paris type 0-IIa, 0-IIb) and for larger or multifocal benign (dysplastic) lesions.
Strong recommendation, high quality evidence.
7 For BE-associated lesions, ESGE suggests to use ESD for lesions suspicious for submucosal invasion (Paris type 0-Is, 0-IIc), for malignant lesions > 20 mm, and for lesions in scarred/fibrotic areas.
Weak recommendation, low quality evidence.
The efficacy of ESD in Barrett’s-associated neoplasia is well established both in the East and the West, with en bloc resection rates varying around 90 %. It remains, however, very difficult to delineate Barrett’s lesions since most series show a lower R0 resection for cancer (ranging between 70 % and 88 %) [70].
4.2.1 Comparison with EMR
In comparison with EMR, ESD results more frequently in R0 resection. This has been demonstrated in a Japanese retrospective study involving 13 centers that assessed long-term outcomes of EMR and ESD of lesions at the gastroesophageal junction [81]. Although potentially comparable in nature, it is however not clear how this finding translates to BE-associated neoplasia, for which the treatment mostly is a combination of resection and ablation of residual columnar epithelium at risk for recurrence, regardless of whether EMR or ESD is used [70] [82].
Since the 2015 guideline, three meta-analyses have been published that assess outcomes of ESD and compare ESD with EMR for Barrett’s-associated neoplasia. Yang et al. published a meta-analysis assessing safety and efficacy of ESD for early BE neoplasia. It included 11 studies and 501 patients, with a mean lesion size of 27 mm. The en bloc resection rate was 92.9 % (95 %CI 90.3 %–95.2 %), R0 resection was however lower at 74.5 % (95 %CI 66.3 %–81.9 %), and the curative resection rate was 64.9 % (95 %CI 55.7 %–73.6 %). Perforation occurred in 1.5 % (95 %CI 0.4 %–3.0 %), bleeding in 1.7 % (95 %CI 0.6 %–3.4 %), and the reported stricture rate was 11.6 % (95 %CI .9 %–29.6 %). Recurrence was found in 0.17 % (95 %CI 0 %–0.3 %) after a mean follow-up of 22.9 months [83].
A more recent meta-analysis on comparison of esophageal ESD versus EMR included 8 studies with BE neoplasia and 3 studies combining SCC and BE [84]. Only for lesions > 20 mm, the authors found higher en bloc resection rates for ESD (OR [odds ratio] 47.25, 95 %CI 23.86–93.57; P < 0.001), higher curative resection rates for ESD (OR 6.16, 95 %CI 2.5–15.19; P < 0.001), and lower local recurrence for ESD (OR 0.19, 95 %CI 0.05–0.81; P = 0.025). Complication rates for perforation, bleeding, and stricture were not different between EMR and ESD. The authors suggested that lesion size should be one of the determining factors to select resection technique. Indeed, since procedure time is significantly longer for ESD, it is more cost-effective to perform EMR in most of the lesions [84].
Finally, the most recent JGES guideline for ESD/EMR for esophageal cancer included a systematic literature search and systematic review comparing ESD to EMR for BE neoplasia (with 26 studies included). The en bloc resection rate for EMR was 50 % versus 96.4 % for ESD with corresponding R0 resection rates of 39.7 % and 81.9 %. The local recurrence rate for EMR was 12.4 % and for ESD it was 2.5 %. Overall complication rates were not different between ESD and EMR. The JGES guideline concluded that, because of the higher rates of en bloc and R0 resections and a lower rate of local recurrence, ESD was recommended over EMR for the treatment of lesions that were amenable for ER [68].
However, there is most likely to be selection bias in the ESD groups and a significant length time bias. In addition, in view of the currently available ablation techniques, recurrence of 12.5 % after a combination of EMR and radiofrequency ablation (RFA) is very unlikely. In fact, multimodality endotherapy with ER and RFA has been associated with only 4 % recurrence, with all recurrences amenable to endoscopic therapy [82].
A recent study suggested a higher rate of complete remission of dysplasia (CRD) after 2 years in patients treated with ESD and subsequent ablation (85.6 %) compared with patients treated with EMR and subsequent ablation (75.8 %; P < 0.01) [85]. This was a retrospective analysis of a prospective database that included 537 patients, with 456 undergoing cap-assisted EMR and 81 ESD, followed by different ablation techniques. The data in this study are, however, confusing. The main conclusion was based on the Kaplan–Meier curve showing a higher cumulative probability at 2 years of obtaining CRD for the ESD group; however, in absolute numbers 420 /537 patients (78 %) in the cap-EMR group obtained CRD over a median follow-up of 11.2 years and 48 /81 (59 %) of the ESD group obtained CRD over a median follow-up of 1.4 years. The follow-up terms at least suggest a significant length time bias. Also the study is probably somewhat underpowered for accurate comparison: complete remission of intestinal metaplasia (CRIM) was 78.5 % for cap-assisted EMR and only 40.7 % for ESD but this was statistically not significant.
It is clear from the previous trial [85] that ESD does not compromise subsequent ablation. This was further illustrated by a retrospective study by Subramaniam et al. that compared the success of RFA after ESD (n = 27) or after EMR (n = 43) or RFA alone (n = 21), and showed no significant difference regarding CRD or CRIM [86].
A well-conducted randomized controlled trial (RCT) indicated that when lesions are amenable for both EMR and ESD, there is no clinical benefit in performing ESD. Terheggen et al. included 40 patients with single lesions that should have been amenable for either technique, including types 0-Is, 0-IIa, 0-IIc or their combinations, limited in horizontal extent to a diameter of ≤ 3 cm in the longitudinal direction or less than half of the esophageal circumference in the lateral direction, and without any endoscopic suspicion of deep infiltration into the submucosal layer. Although R0 resection rate was higher for ESD (10/17 vs. 2/17 for EMR), CRD at 3 months was not different [87]. Therefore, this trial provided evidence that ESD has little role for lesions that are clearly amenable for both EMR and ESD.
However, different situations exist with lesions that are bulkier and may be difficult to resect. If a lesion is suspicious for submucosal invasion (Paris 0-Is, 0-IIc lesions) and a deep R0 resection for accurate staging is desirable, ESD may also be indicated. Especially in elderly patients who are unfit for surgery or CRT, a radical resection may in fact still be curative albeit with a higher chance for metastasis. As indicated by the study from Terheggen et al. [87]. and the meta-analysis by Yang et al. [83], ESD could be considered, particularly for larger lesions (> 2–3 cm). Some studies also indicate that ESD is successful in more challenging cases with nodular lesions, lesions larger than 2 cm, or with scarring (poor lifting) [88] [89] [90] [91].
Therefore, in conclusion, in terms of need for surgery, neoplasia remission and recurrence, ESD and EMR are both highly effective for ER of early Barrett’s neoplasia. ESD achieves a higher R0 resection rate, but for most patients this bears little clinical relevance, as it is more time-consuming and has the potential to cause severe adverse events [87] [92].
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4.2.2 Comparison with surgery
For the 2015 ESGE guideline only three studies were found showing that for T1a EAC, ER was as effective as surgery and had a better safety profile [93] [94] [95]. Recent studies confirmed that for early BE-related EAC, ER is associated with similar DSS but with shorter hospital stays, fewer readmissions and lower 90-day mortality [96] [97] [98]. Moreover, a recent study analyzing quality of life after these two options shows that multiple measures of symptom status are better following ER when compared to surgery [99].
Hence, based on ER efficacy and its fewer and more manageable complications, ER (when combined with ablation) appears to be a viable alternative to surgery even for lesions with superficial submucosal invasion.
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4.3 Stomach lesions
8 ESGE recommends ESD for differentiated gastric lesions clinically staged as dysplastic or as intramucosal carcinomas (of any size if not ulcerated and ≤ 30 mm if ulcerated), with EMR being an alternative for Paris 0-IIa lesions of size ≤ 10 mm with low likelihood of malignancy.
Strong recommendation, moderate quality evidence.
9 ESGE suggests that gastric adenocarcinomas that are ≤ 30 mm, submucosal (sm1), and well-differentiated, or ≤ 20 mm, intramucosal, and poorly differentiated type, both without ulcerative findings, can be considered for ESD, although the decision should be individualized.
Weak recommendation, low quality evidence.
4.3.1 Comparison with EMR
Since the publication of the first ESD guidelines, two meta-analyses including > 6000 patients and a large prospective cohort have compared efficacy and safety outcomes of EMR and ESD [100] [101] [102]. Compared with EMR, ESD is associated with significantly higher rates of en bloc and complete resection (including in lesions < 10 mm), lower recurrence, and similar post-procedural bleeding; on the other hand, it is associated with a slightly higher perforation risk and increased procedural duration. Several real-world ESD series confirm its high rates of en bloc and R0 resection (> 90 %), curative resection (75 %–80 %), low local recurrence (< 5 %) and acceptable rates of adverse events (post-procedural bleeding 5 %–10 %, perforation < 3 %) [102] [103]. It also seems that gastric ESD is being successfully implemented in Europe, and although published studies generally include a low number of patients, the outcomes of European series are generally comparable to those from Eastern countries [3]. Short- and long-term outcomes of ESD in cardia/esophagogastric lesions are also comparable to those for other gastric locations although there is a trend to lower R0 and curative resection rates [81].
ESD is thus recommended as the first-line endoscopic treatment for gastric superficial lesions with a null/very low risk of LNM. These are, namely:
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dysplastic lesions of any size;
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differentiated-type adenocarcinomas, clinically staged as intramucosal (that is, without signs of deep submucosal invasion), of any size in the absence of ulceration and ≤ 3 cm in the presence of ulceration.
EMR should be considered as an alternative for elevated (0-IIa) lesions, < 10 mm, and with low likelihood of advanced histology, and provided that the endoscopist feels that en bloc R0 resection can be achieved. For undifferentiated-type adenocarcinomas clinically staged as intramucosal, ER can be considered if the lesion is < 2 cm and without ulcerative findings, although the decision should be individualized, balancing surgical risks and patient preferences (in the expanded indication for ER) [104].
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4.3.2 Comparison with surgery
Several studies have also directly compared short- and long-term outcomes of ESD and gastrectomy in the treatment of gastric superficial lesions, as summarized in four meta-analyses [105] [106] [107] [108]. Although the majority of studies are retrospective and performed in Eastern countries, these meta-analyses have found that ESD is associated with significantly lower procedural time, length of stay, and adverse events. A significantly lower procedure-related mortality was also found in one meta-analysis [106]. Two prospective studies not included in that meta-analysis also directly compared short-term ESD and gastrectomy outcomes, with similar results [109] [110]. Concerning long-term outcomes, in the meta-analyses no differences were found in OS or DSS (DSS > 99 % for both treatment groups), although ESD was associated with a significantly higher recurrence risk and lower disease-free survival. Metachronous lesions were also significantly more frequent in ESD arms (5.2 %–6.0 % vs. 0.4 %–0.5 % in gastrectomy studies), which accounts for most of the events during follow-up. However, ESD was found to have a positive impact on health-related quality of life when compared with gastrectomy [109] [111] [112] [113].
Based on these data, when the lesion appears endoscopically resectable with a predictable high curability potential, ESD appears a better option than surgery.
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4.4 Duodenal and small-bowel lesions
10 ESGE does not recommend routine use of ESD for duodenal or small-bowel lesions, with its use being reserved for selected cases in expert centers.
Strong recommendation, moderate quality evidence.
11 ESGE recommends polypectomy and/or EMR (en bloc or piecemeal) as the treatment of choice for most duodenal and small-bowel superficial lesions.
Strong recommendation, moderate quality evidence.
Rates of R0 resection for duodenal ESD are highly variable, between 19.4 % in a European study [114] to 93.9 % in China [115]. In all studies analyzed it seems clear that R0 resection rates are lower in the duodenum compared with other organs particularly for less experienced endoscopists [116].
Regarding safety, perforation rates are high with an incidence > 10 % in different studies including in expert centers [115] [117], and reaching 15 % [118] to 37.5 % [119] in some of those studies. The major risk factor for delayed perforation, a dreadful complication that occurs mainly with ESD (and less with EMR), was lesion location that was distal to the ampulla of Vater [120].
4.4.1 Comparison with EMR
Available comparative data available are scarce and retrospective, but demonstrate a higher rate of R0 resection with ESD compared to EMR [114] [115] [116]. In retrospective studies whose data were compiled in a meta-analysis, ESD demonstrated a higher rate of complete resection than EMR with an OR of 1.63 but without any difference in the risk of local recurrence [116]. On the other hand, the risk of per-procedure and delayed perforation with duodenal ESD was higher than for EMR, and there was a higher risk of surgery for delayed perforation [116] [120]. Similar results were reported in Japan, although the rate of R0 resection was higher in Asian than in European studies (OR 2.16) [116]. Hybrid techniques did not show higher R0 resection rates than EMR [121].
Finally, EMR seems to remain the better therapeutic option for duodenal neoplasia because of its efficacy and safety profile, even for complex lesions, and its favorable comparison with surgery [122] [123] [124]. Moreover, the clinical benefit for the patient of achieving R0 resection has never been demonstrated for duodenal lesions, in particular because of the low incidence of invasive submucosal cancer. ESD has been proposed as an alternative when EMR is not technically feasible because of strong fibrosis after local recurrence [125].
Thus, for the moment, there are no clear indications for the use of ESD for nonampullary duodenal lesions. EMR remains the first option strategy for duodenal neoplasia since ESD is not as effective and safe as in other organs, with lower R0 resection rates than in other organs, a high perforation rate, and with no proven advantage in recurrence when compared to EMR.
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4.5 Colorectal lesions
12 ESGE recommends polypectomy and/or EMR (en bloc or piecemeal) as the treatment of choice for most superficial colorectal lesions.
Strong recommendation, high quality evidence.
13 ESGE suggests that ESD should be considered for en bloc resection of colorectal (but particularly rectal) lesions with suspicion of limited submucosal invasion (demarcated depressed area with irregular surface pattern or a large protruding or bulky component, particularly if the lesions are larger than 20 mm), or for lesions that otherwise cannot be completely removed by snare-based techniques.
Weak recommendation, moderate quality evidence.
Colorectal ESD is common practice in Eastern countries, with good results and established indications [35] [126] [127]. In experienced hands en bloc and R0 resection rates can be higher than 90 % [128]. In the West initial studies were disappointing even for rectal lesions, with an en bloc resection rate of only 61 % and a perforation rate of 18 % [129]. However, more recent studies have shown better results with 80 % en bloc and 69 % R0 resection rates, and an 8 % complication rate (with 2 % requiring emergent surgery) [130]. A recent systematic review of 109 studies on 19 484 colorectal lesions treated by ESD showed rates of en bloc resection of 91 %, R0 resection of 82.9 %, and 2 % recurrence; the rate of bleeding was 2.7 % and of perforation 5.2 %, and 1.1 % needed surgery because of adverse events [131]. However, these results were worse in non-Asian countries.
Therefore, even though ESD is the endoscopic technique that allows a greater chance of en bloc R0 resection in the colon, its safety profile looks worse than in the esophagus and in the stomach, particularly in Western countries.
4.5.1 Comparison with EMR
Several studies and meta-analyses compared EMR versus ESD for colorectal lesions, with similar conclusions: en bloc and R0 resection rates are higher and recurrence lower with ESD, but in the ESD group the procedure is longer, and the rates of perforation, complications, and additional surgery because of complications are higher [128] [132] [133] [134]. Moreover, to our knowledge, no comparative study has addressed the difference in adenoma recurrence between ESD and piecemeal EMR (pEMR) using thermal coagulation at the end of resection, a technique that has been proven in a large randomized controlled trial (RCT) to reduce recurrence after pEMR from 21 % to 5 % (P < 0.001) with no adverse events [135]. The effectiveness of this technique in clinical practice has now been confirmed with recurrence rates of only 1.4 % in those receiving complete margin thermal ablation [136].
Thus, the question is when we should use ESD instead of EMR? A recent systematic review including 11 260 colorectal ESDs showed that even in selected lesions there was only a low prevalence of the sm1 lesions that would justify the attempt at en bloc ESD resection: 15.7 % of the specimens disclosed submucosal invasion with only 8 % overall infiltrating less than 1000 microns and only 6 % of resections being curative. The number needed to treat for avoiding one surgery was 12.5 to 16.7. The authors concluded that ESD should not be used indiscriminately in the resection of colorectal neoplasia [137].
A cost–effectiveness study comparing ESD and wide-field EMR for removing large sessile and laterally spreading lesions > 20 mm showed that even for these lesions universal ESD could not be justified (the exception being high risk rectal lesions), and the best strategy would be selective ESD for the lesions suspicious for submucosal cancer [138]. The lesions at risk of submucosal invasion are: nongranular LSTs (LST-NGs), particularly if pseudodepressed 0-IIc; granular nodular mixed LSTs, particularly if more than 2 cm in size; especially lesions in the rectosigmoid area; and those showing an irregular pattern with CE. These lesions should be considered for ESD and/or surgery [33] [34] [35] [39].
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4.5.2 Comparison with surgery
Although surgery is a more definitive treatment for large and malignant polyps, and also allows lymph node resection, it is associated with a considerable burden of AEs and even mortality. In a retrospective cohort for complex nonmalignant polyps, surgery was associated with rates of 17 % for significant adverse events, 3 % for additional surgery, and 1 % for 12-month mortality; compared with ER, length of stay and costs were greater [139]. Another study from the tertiary Veterans Affairs Medical Centers showed that a strategy of a prior attempt at ER reduced morbidity compared to laparoscopic surgery, particularly for polyps < 4 cm [140]. A case-matched comparison of ESD versus laparoscopic surgery for complex polyps showed that ESD is more cost-effective than conventional segmental resection, suggesting that ESD can be offered as a colon-preserving procedure [141]. Furthermore, quality of life has been evaluated to be better after ESD compared to laparoscopy-assisted surgery [142] in one study, and costs are higher for transanal endoscopic microsurgery compared to ESD [142] [143]. Moreover, for patients with T1 CRC, prior ESD with histological en bloc resection did not adversely affect their oncologic prognosis after additional surgery [144].
However, specifically analyzing only malignant T1 polyps (and excluding benign polyps), a study using the US National Cancer Database, that was one of the largest population-based analyses of patients with T1N0M0 malignant colon polyps, showed that OS was higher in patients who underwent surgery compared with polypectomy. This finding was consistent even after adjustments between the two groups for multiple patient and tumor factors [145]. This study contradicted a systematic review and meta-analysis that found that ER should be considered as the first-line treatment for endoscopically resectable T1 colorectal cancers, and that in cases of noncurative resection, additional surgery can have comparable outcomes to primary surgery [146]. Another study showed that for colonic neoplasms, laparoscopic surgery should be considered when ESD is technically difficult, but that for rectal neoplasms, ESD is desirable even for large-sized lesions [147].
Taking all this into account, if a lesion is clearly benign, ER should be the first-line therapy, though as we have seen EMR might be a better option than ESD for these lesions. For lesions suspicious for malignancy, then ESD and/or surgery are comparable options and the decision will depend on several factors (location, size, complexity of ESD, patient preferences, center experience). The exception appears to be the rectum where ESD could have an advantage over EMR for complex high risk benign lesions and over surgery for suspicious T1 lesions.
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5 Management after endoscopic resection
In this Guideline an adjustment of risk categories and terminology was deemed necessary, to reflect the different probabilities of LNM risks that depended upon the pathological characteristics of the resected tumor (see the section on Pathological aspects, and also [Table 2]).
CRT, chemoradiotherapy; ER, endoscopic resection; ESD, endoscopic submucosal dissection; HM, horizontal margin; L, lymphatic invasion; LNM, lymph node metastasis; LV1, lymphovascular invasion; SCC, squamous cell cancer; SM, submucosal; UL, ulcerated; V, vascular invasion; VM, vertical margin.
1 sm1 cancer: tumor invasion ≤ 200 μm (SCC), ≤ 500 μm (Barrett’s and gastric), and ≤ 1000 μm (colon); all other criteria must apply to consider ER as a low risk resection.
2 Expanded indication, individualized decision; all other criteria must apply to consider ER as a low risk resection.
5.1 Esophageal SCC lesions
14 ESGE recommends that an en bloc R0 resection of a superficial esophageal squamous cell lesion with histology no more advanced than intramucosal m2 cancer, well to moderately differentiated, with no lymphovascular invasion, should be considered a very low risk (curative) resection and no further staging procedure or treatment is recommended.
Strong recommendation, moderate quality evidence.
15 ESGE suggests that an en bloc R0 resection of an esophageal m3 or sm1 SCC that is well to moderately differentiated and with no lymphovascular invasion, should be considered a low risk (curative) resection and no further treatment is generally recommended.
Weak recommendation, moderate quality evidence.
However, in these cases, particularly if the lesion is bigger than 20 mm, there is a real (albeit low) risk of LNM and complete staging is recommended, with the risk from further therapy being balanced against the risk of LNM, in a multidisciplinary discussion.
Weak recommendation, low quality evidence.
16 ESGE suggests that complementary radiotherapy or CRT may be considered in a multidisciplinary discussion after a curative resection of esophageal m3/sm1 SCC (particularly if > 20 mm in size).
Weak recommendation, moderate quality evidence.
Among lesions in which the depth of invasion does not extend beyond the mucosal layer (T1a), those confined within m1–m2 layers are only extremely rarely associated with LNM; therefore, ER is considered curative [148] [149]. A recent meta-analysis suggests that after full evaluation, ER can be recommended as a curative treatment for patients with superficial SCC if the following conditions are met: (i) tumor size ≤ 20 mm; (ii) Paris 0-II macroscopic type of tumor; (iii) possible confinement of lesion to mucosa; and (iv) absence of lymphovascular invasion [150]. Lesions extending up to the muscularis mucosae or slightly infiltrating the submucosa (up to 200 μm) are also amenable to ER; however, as a whole they are associated with a greater risk of LNM. Nevertheless, if some criteria are met, ER of these lesions might also be highly likely to be curative. In fact, in a recent study no single patient with m3/sm1 cancer, high tumor differentiation, no lymphovascular invasion, and tumor length < 2 cm had LNM, and none of these patients experienced recurrence [151].
About 50 % of the lesions that show deeper (> 200 μm) invasion into the submucosa (T1b) are associated with metastasis, and in such cases ER should be considered to be a high risk resection and patients should be treated in the same manner as those with advanced carcinomas [148] [149].
ER plus adjuvant therapy appears to be a new combination treatment for SCC invading to deep mucosa (pT1a-m3) or submucosa (pT1b). Adjuvant therapy can take the form of esophagectomy, radiotherapy, or CRT. At present, there is no clear recommendation for or against the administration of additional treatments in patients with pT1a-m3 SCC. A recent randomized trial from China studied the combination of ESD with additional radiotherapy (59.4 Gy within 2 months after ESD) in T1a SCC. In the nonradiotherapy group 3/70 patients experienced intraluminal mucosal recurrence compared with none in the radiotherapy group. No local LNM or distant metastasis occurred in either group. The 3-year cumulative recurrence-free survival was 100 % in the radiotherapy group and 85.3 % in the nonradiotherapy group (P = 0.04). No severe radiation toxicities were recorded [152]. Another earlier study showed the benefit of additional radiotherapy in patients with T1a-m3/T1-sm1 tumors [153].
Is additional treatment recommended in patients with pT1b-sm1 SCC, based on histological findings following ER? Again, if no other high risk criteria are met and the tumor size is < 2 cm, the risk of LNM appears low [151]. Nevertheless, the efficacy of adding CRT after ER of SCC with submucosal invasion has been reported in several retrospective trials, with a better safety profile in comparison with surgery [154] [155] [156] [157]. The ECOG0508 trial was a prospective nonrandomized study to confirm the efficacy of selective CRT based on findings from ER in patients with T1b sm1–2 tumors [158]. Depending on the ER findings, patients received the following: no additional treatment for patients with pT1a tumors with a negative resection margin and no lymphovascular invasion (group A); prophylactic CRT for patients with pT1b tumors with a negative resection margin or pT1a tumors with lymphovascular invasion (group B); or definitive CRT for patients with a positive vertical resection margin (group C). The 3-year overall survival rates were similar among the groups (90.7 % for group B and 92.6 % in all patients). Efficacy was comparable to that of surgery. The JES guidelines conclude that there is strong evidence to recommend additional treatment (mainly CRT) after ER in patients identified as meeting high risk criteria (poorly differentiated tumor, lymphovascular invasion, deep submucosal invasion), taking into account the benefit–risk balance, strength of evidence, and patient preferences [159].
Based on these studies, the present authors consider that after a low risk (curative) ER of a T1a-m3 or T1b-sm1 tumor, surveillance and/or additional radiotherapy might be considered as a preferred less aggressive additional treatment, as compared to surgery or CRT, depending on the patient’s clinical status. Nevertheless, CRT might be preferred over radiotherapy alone in young and fit patients. Surgery is an option for young fit patients meeting high risk criteria (noncurative ER), particularly if there is deep submucosal invasion and lymphovascular invasion, since in these cases overall survival could be better with surgery [160] [161].
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5.2 BE-associated lesions
17 ESGE recommends that an en bloc R0 resection of a BE-associated superficial lesion with histology no more advanced than intramucosal cancer, well to moderately differentiated, with no lymphovascular invasion, should be considered a very low risk (curative) resection and no further staging procedure is generally recommended.
Strong recommendation, moderate quality evidence.
18 ESGE suggests that an en bloc R0 resection of a BE-associated superficial lesion with superficial submucosal invasion (sm1), and that is well to moderately differentiated, and with no lymphovascular invasion, should be considered a low risk (curative) resection and no further treatment (except for ablation of BE tissue) is generally recommended.
Weak recommendation, moderate quality evidence.
However, in these cases, there is a real (albeit low) risk of LNM, and complete staging is recommended with the risk from further therapy (surgery) being balanced against the risk of LNM, in a multidisciplinary discussion.
Weak recommendation, low quality evidence.
19 ESGE recommends ablation of all of the Barrett’s mucosa after a curative or local-risk resection.
Strong recommendation, high quality evidence.
The risk of LNM in BE-associated esophageal adenocarcinoma (EAC) appears to be lower than in SCC. For BE-associated adenocarcinomas, according to reports that analyzed the rate of LNM relative to the depth of tumor infiltration, ER appears to be curative for intramucosal carcinomas that are well or moderately differentiated and without lymphovascular invasion [72] [162] [163] [164] [165]. Based on limited data these criteria might be extended to lesions with invasion into the submucosa (≤ 500 μm, sm1), namely to low risk tumors (well or moderately differentiated, without lymphovascular invasion), because such lesions harbor a low risk of LNM (1.4 %–1.9 %) that appears to be lower than the risk of surgery for most patients [165] [166] [167]. Nevertheless, for sm1 tumors, this risk should be balanced against the risk of surgery for a particular patient. For sm2/sm3 EACs, surgery is recommended since the rate of LNM appears higher than the mortality risk of surgery, although a recent retrospective study reported a very low risk of LNM with less than 1000 μm of submucosal invasion [168] [169].
When remaining Barrett’s mucosa is left untreated, case series have reported recurrence of neoplasia, with rates varying from 11 % to 30 % [170] [171] [172]. The multicenter EURO-II study demonstrated that complete eradication of neoplasia and Barrett’s mucosa can be achieved with the combination of ER and RFA in 98 % and 93 %, respectively (in a per-protocol analysis). The recurrence rate for neoplasia was 4 % and for intestinal metaplasia it was 8 % [82]. According to a recent systematic review and meta-analysis the risk for recurrence of neoplasia is significantly higher in those patients who have residual Barrett’s mucosa after completion of endoscopic therapy compared with those in whom CRIM has been achieved (risk ratio [RR] 2.8, 95 %CI 1.7–4.6). The pooled cumulative incidence rate of dysplasia and Barrett’s adenocarcinoma recurrence was 3 % (95 %CI 2 %–4 %) after achieving CRIM and 6 % (95 %CI 0 %–16 %) after achieving CRD only [173]. Based on these studies ESGE suggests complete ablation of all of the Barrett’s mucosa after ER.
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5.3 Stomach lesions
20 ESGE recommends that an en bloc R0 resection of a superficial gastric lesion with histology no more advanced than intramucosal cancer, well to moderately differentiated, with no lymphovascular invasion, should be considered a very low risk (curative) resection, independently of size if without ulceration or of lesions ≤ 30 mm if ulcerated; and no further staging procedure or treatment is generally recommended.
Strong recommendation, moderate quality evidence.
21 ESGE suggests that an en bloc R0 resection of a ≤ 30 mm gastric adenocarcinoma, with superficial submucosal invasion (sm1), that is well to moderately differentiated and with no lymphovascular invasion and no ulcer, should be considered a low risk (curative) resection, and no further treatment is generally recommended.
Weak recommendation, moderate quality evidence.
However, in these cases there is a real (albeit low) risk of LNM and complete staging is recommended with the risk from further therapy (surgery) being balanced against the risk of LNM, in a multidisciplinary discussion.
Weak recommendation, moderate quality evidence.
22 ESGE suggests that an en bloc R0 resection of a ≤ 20 mm gastric intramucosal poorly differentiated carcinoma, with no lymphovascular invasion or ulcer, should be considered a low risk (curative) resection and no further treatment is generally recommended.
Weak recommendation, moderate quality evidence.
However, in these cases there is a real (albeit low) risk of LNM and complete staging is recommended with the risk from further therapy (surgery) being balanced against the risk of LNM, in a multidisciplinary discussion.
Weak recommendation, moderate quality evidence.
23 ESGE recommends that a resection of a > 30 mm gastric adenocarcinoma with superficial submucosal invasion (sm1) or with ulceration should be considered a high risk (noncurative) resection, and complete staging should be done and strong consideration for additional treatments (surgery) should be given, on an individual basis in a multidisciplinary discussion.
Strong recommendation, moderate quality evidence.
Overall, intramucosal adenocarcinomas (pT1a) have a 2 %–5 % incidence of LNM, while in submucosally invasive adenocarcinoma (pT1b) this risk increases to 10 %–25 %. However, if certain histological characteristics are met, the risk of LNM is null or minimal. This led to the proposal of criteria for curative ER, based on three landmark studies that correlated lesion characteristics with the presence of LNM in gastrectomy specimens [174] [175] [176]. Since the publication of the first edition of this guideline, several studies have evaluated the oncological safety of endoscopic treatment. Studies have also compared the outcomes of endoscopic and surgical treatment in lesions meeting curative criteria, confirming that 5-year OS and DSS are similar between the two treatment approaches [105].
Extensive research conducted in recent years confirms that deep submucosal invasion, undifferentiated histology, size ≥ 30 mm, and lymphovascular invasion are independent risk factors for LNM, reinforcing the value of the proposed criteria for curative resection. However, some recent studies also show LNM rates for expanded criteria resections that are higher than previously reported. Of note, although the risk of LNM is almost null in Japanese studies, in studies outside of Japan this risk is higher (though still less than 4 %), which may be related to differences in specimen handling [177]. It is also important to note that to date there is no convincing evidence that other independent risk factors can be used to better stratify LNM risk and refine curativeness criteria. Nevertheless, single studies have found some factors independently associated with LNM, namely: mucinous adenocarcinoma [178], muscularis mucosae invasion [179] and perineural invasion in pT1a lesions [180], submucosal invasion width > 4 mm [181], and the ratio of submucosal invasion width to superficial tumor size being greater than 0.04 [182]. A meta-analysis also did not find differences in LNM rates if a submucosal invasion depth of ≤ 300 µm was used as a cutoff as opposed to ≤ 500 µm [177].
Taking all the above into account, the following criteria for curativeness of resection should guide management:
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Curative/very low risk resection (LNM risk < 0.5 %–1 %): En bloc R0 resection; dysplastic/pT1a, differentiated lesion, no lymphovascular invasion, independent of size if no ulceration and ≤ 3 cm if ulcerated.
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Curative/low risk resection (LNM risk < 3 %): En bloc R0 resection; lesion with no lymphovascular invasion and:
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pT1a, predominant type is poorly differentiated or undifferentiated, size ≤ 2 cm, no ulceration; and
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pT1b, invasion ≤ 500 µm, differentiated, size ≤ 3 cm.
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Local-risk resection (very low risk of LNM but increased risk of persistence/recurrence):
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Piecemeal resection or tumor-positive horizontal margin of a lesion otherwise meeting curative/very low risk criteria;
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Provided that there is no submucosally invasive tumor at the resection margin: piecemeal resection or tumor-positive horizontal margin; pT1b; invasion ≤ 500 µm; well-differentiated; size ≤ 3 cm; VM0.
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High risk resection (noncurative): Any lesion with any of the following:
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positive vertical margin;
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lymphovascular invasion;
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deep submucosal invasion (> 500 µm from the muscularis mucosae);
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ulceration or size > 2 cm, in poorly differentiated lesions;
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size > 3 cm in pT1b differentiated lesions with submucosal invasion < 500 µm, or in intramucosal ulcerative lesions.
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It is also important to note that some other factors may also influence LNM risk, namely a papillary component, perineural invasion, and budding. Papillary adenocarcinoma is associated with worse short-term outcomes – higher rates of incomplete resection, submucosal invasion, and lymphovascular invasion, and thus lower rates of curative resection – but it does not have a proven independent prognostic value in lesions that meet curative criteria [183] [184], Perineural invasion is very rare in the absence of lymphatic or vascular involvement. But at present there is no convincing evidence that these three features should be included in risk stratification and management strategies.
There is also some debate on how to handle mixed-type adenocarcinomas since some studies with gastrectomy specimens found a higher risk of LNM in tumors with histological heterogeneity, even when compared with undifferentiated-type tumors [185] [186] [187] [188]. However the prognostic value of this feature does not seem to apply in intramucosal lesions that meet curability criteria [189], and thus definitive conclusions cannot be drawn. Thus, we recommend classifying tumors according to the quantitatively predominant component (> 50 %) into differentiated-type (which includes papillary and tubular adenocarcinoma) or undifferentiated-type (which includes poorly differentiated, signet ring cell, and mucinous adenocarcinoma if T1b). However the issue of the prognostic significance of histological heterogeneity, specifically in lesions meeting curability criteria deserves further evaluation.
It should be noted that after a high risk ER, even though surgery should always be an option, some patients who refuse surgery may have a similar prognosis to those who proceed to surgery, and this has been shown in both Eastern [190] [191] and Western countries [192].
It is clear that the risk of LNM differs according to histopathological features, and that surveillance can be a better option if surgical risk exceeds LNM risk. In this context, the e-Cura scoring system has been proposed. Patients are assigned into three risk categories depending on histopathological features. The score gives 3 points for lymphatic invasion, and 1 point each for tumor size > 30 mm, sm2 status, venous invasion, and positive vertical margin, and has been validated as an important decision tool after noncurative ER [193] [194]. However, it is important to stress that if LNM or distant metastasis occurs, the prognosis is generally dismal, with palliative chemotherapy or best supportive care being the treatment in the majority of the cases [190]. Thus in a multidisciplinary discussion patients considering surveillance instead of surgery should be informed that, even though the absolute risk of LNM or distant metastasis is low, if it should occur, the prognosis is poor.
Regarding the issue of resection with nonevaluable or positive horizontal margins (HMx/HM1), a meta-analysis showed that the risk of persistent disease was, respectively, 10 % or 36 %, with no increased risk of LNM [195]. A study showed that the risk of recurrence after resection with a positive horizontal margin, which was 30 % with observation only, could be reduced to 11 % when another endoscopic treatment was done as soon as 3 months after resection even when no clear lesion was seen [196].
Taking all this into account, an individualized decision for one of the following options, that balances recurrence and surgical risk, can be considered adequate: close observation, with scar biopsies taken at least in the first follow-up endoscopy; or for coagulation/ablation or re-ESD, namely resection of the ESD scar and/or coagulation of the scar before recurrence occurs; or for surgery. Given the poorer safety profile of surgery, it seems reasonable to reserve that option to endoscopically nontreatable recurrence. In the other cases, close endoscopic observation or an early endoscopic re-treatment (beginning within 3–6 months of the index ER) appear safe strategies. This scenario is considered an eCura C-1 resection in the Japanese Gastric Cancer Association guideline, and this suggested management is similar to the one recommended in that guideline [197].
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5.4 Duodenal and small-bowel lesions
24 ESGE suggests that, given the lack of evidence, the same post-resection criteria as in the colon should apply to the management of duodenal and small-bowel lesions, on an individual basis and with a multidisciplinary approach.
Weak recommendation, very low quality evidence.
Low and high risk resections are not defined in the case of duodenal or small-bowel lesions. For nonampullary duodenal neoplasia, the risk of LNM in the case of intramucosal carcinoma seems negligible [198], and the risk remains unknown in the case of submucosal invasion [199] with few cases reported. The rare cases of duodenal adenocarcinoma with submucosal invasion have been sent to surgery but the LNM status found at those surgeries is not known [122]. In the case of tumor-free margins, the recurrence rate has been 0 % in most series [122]. In the case of non-free margins (with data from piecemeal resections), the risk of recurrence is not null, with studies showing large discrepancies from 1.2 % [200] to 20.4 % in a recent prospective study [201], and with most recurrences allowing further endoscopic treatment. Data on submucosal invasion with lymphovascular invasion, budding, or undifferentiated types are not reported in the literature. In fact, we do not know the risk of distant metastasis and LNM in the case of T1 duodenal adenocarcinoma with submucosal invasion.
Given this absence of data, and the morbidity and mortality of duodenal surgery, ESGE suggests that a decision for surgery should be based on the same criteria as in the colon, in a multidisciplinary team discussion.
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5.5 Colorectal lesions
25 ESGE recommends that an en bloc R0 resection of a colorectal lesion with histology no more advanced than intramucosal adenocarcinoma, well to moderately differentiated with no lymphovascular invasion, should be considered a very low risk (curative) resection and no further staging procedure or treatment is generally recommended.
Strong recommendation, high quality evidence.
26 ESGE recommends that an en bloc R0 resection of a colorectal lesion with superficial submucosal invasion (sm1), that is well to moderately differentiated and with no lymphovascular invasion and no grade 2 or 3 budding, should be considered a low risk (curative) resection, and no further treatment is generally recommended.
Strong recommendation, high quality evidence.
27 ESGE suggests that after an en bloc R0 resection of a rectal lesion meeting the single high risk criterion of submucosal invasion deeper than sm1 (well to moderately differentiated with no lymphovascular invasion and no grade 2 or 3 budding), CRT and/or surveillance might be preferred over surgery on an individual basis in a multidisciplinary approach.
Weak recommendation, very low quality evidence.
Several studies and meta-analyses investigated risk factors for LNM. A meta-analysis that included 13 cohort studies with 7066 patients who only underwent radical surgery, showed that there is a significant risk of LNM with the following: submucosal invasion, that is ≥ sm2 or ≥ 1000 µm (OR 3.00, 95 %CI 1.36–6.62; P = 0.007); vascular invasion (OR 2.70, 95 %CI 1.95–3.74; P < 0.001); lymphatic invasion (OR 6.91, 95 %CI 5.40–8.85; P < 0.001); poorly differentiated carcinoma (OR 8.27, 95 %CI 4.67–14.66; P < 0.001); or tumor budding (OR 4.59, 95 %CI 3.44–6.13; P < 0.001) [202]. This study confirmed the results of a previous meta-analysis [203]. However, the risks of each of these factors may not be equivalent.
Isolated depth of invasion of > 1000 µm in the submucosa is not a consistent independent risk factor in several studies. By itself it is probably not a strong risk factor for LNM, and how much weight to give it in decision-making about further revision surgery after ER is debatable [204]. However, it should be noted that even though in this last-mentioned study submucosal invasion was not considered an independent risk factor (P = 0.075), the risk of LNM was 6 % in the absence of the independent risk factors; a risk that might be considered higher than the surgical risk. In fact, another study evaluating ER specimens does show by multivariate analysis that a depth of submucosal invasion ≥ 1000 μm is an independent risk factor for LNM (OR 5.56, 95 %CI 2.14–19.10) [205]. This is contradicted by a recent study that suggests that when no other risk factors are present choosing a cutoff depth of submucosal invasion of > 1900 µm may help to reduce the incidence of unnecessary surgery after ER [206]. However, a recently published meta-analysis including 16 observational studies and 10 181 patients confirmed submucosal invasion of at least 1000 µm as a risk factor for LNM (OR 3.53, P < 0.001) [207].
A positive vertical margin after ER has also been associated with local recurrence, LNM, and rescue surgery. In a recent study evaluating risk factors for an adverse prognosis after ER of T1 tumors, the variables related to surgical rescue were piecemeal resection (OR 4.48, 95 %CI 1.48–13.6), infiltrated/nonevaluable resection border (OR 7.44, 95 %CI 2.12–26.0), not well-differentiated histology (OR 4.76, 95 %CI 1.07–20.0), vascular infiltration (OR 8.24, 95 %CI 2.72–25.0), and Haggitt 4 infiltration of the submucosa (OR 5.68, 95 %CI 2.62–12.3). Residual disease after ER was associated with infiltrated/non-evaluable resection border (OR 34.9, 95 %CI 4.08–298), not well-differentiated histology (OR 6.67, 95 %CI 1.05–50.0), and vascular infiltration of the submucosa (OR 7.61, 95 %CI 1.55–37.4) [208]. So, clearly a positive vertical margin is a risk factor for residual disease and need for additional surgery and potential for LNM, as suggested by the study of Boenicke et al. This showed that in patients who underwent ER of malignant polyps followed by surgery, even though 63 % of resection margins were positive (a free margin was not defined as a tumor-free extent of more than 1 mm), subsequent surgical specimens showed residual carcinoma in only 2.8 % but LNM in 7.6 % [209]. What should be considered a positive vertical margin is, however, a matter of discussion (see section on Pathological aspects).
Perineural invasion was also demonstrated to be a risk factor of LNM in T1 colorectal cancer. However, there is not sufficient evidence to conclude that it has an independent role or to make any recommendation regarding perineural invasion per se [204].
Similarly to the other organs the importance of positive horizontal margins seems low in the colon, with recurrence rates after en bloc ER being as low as 2.2 % when the size of the positive invaded margins is small (< 8 mm) [210]. In contrast, piecemeal resection at ESD is associated with a higher risk of recurrence, reaching 15.2 % compared with 5.1 % for en bloc resections with positive margins or 2.2 % in the case of indeterminate margins [211]. Those recurrence rates are significantly higher than the risk of recurrence after R0 resection with free margins, evaluated to be null [212]. In all these studies a positive horizontal margin was not associated with LNM risk and so, in the absence of histological high risk factors, a “wait-and-see” policy is justified [213].
With all the above in mind, it is the present authors’ opinion that a more extensive resection accompanied by a lymph node dissection is necessary in most patients with resected T1 colorectal cancer with nonpedunculated ≥ sm2 (submucosal ≥ 1000 µm) invasion, lymphovascular invasion, poorly differentiated carcinoma, grade 2 or 3 tumor budding, or positive vertical margin. Nevertheless, we recognize that for some patients, if the only high risk criterion is ≥ sm2 tumor, particularly in the rectum, the risk of surgery may be similar to the risk of LNM, and surveillance could be an option. Even though, as shown in a recently published meta-analysis [207], rectal location may be a risk factor for LNM (OR 1.36, P = 0.003), the surgical options are also more aggressive than in the colon (and may imply abdominoperineal amputation) with mortality and severe morbidity rates as high as 3 % and 15 %, respectively [214] [215]. Moreover, in patients with high risk pT1 rectal cancer after local excision, CRT has been shown to be a safe and effective treatment alternative to revision radical resection [216] [217]. Therefore, even though based on a low level of evidence, it is the present authors’ opinion that after an en bloc R0 resection of a rectal lesion, when the single high risk criterion is submucosal invasion deeper than sm1 (i. e., the lesion is well to moderately differentiated with no lymphovascular invasion and no grade 2 or 3 budding), surveillance and/or CRT might be preferred over surgery on an individual basis in a multidisciplinary discussion.
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5.6 All organs
28 ESGE recommends that after an endoscopic complete resection, if there is a positive horizontal margin or if resection is piecemeal but there is no submucosal invasion and no other high risk criteria are met, this should be considered a local-risk resection and endoscopic surveillance/re-treatment is recommended rather than surgery or other additional treatment.
Strong recommendation, moderate quality evidence.
As we have seen, independently of the organ (see above evidence for each organ), when complete, a resection that is piecemeal or with positive/nonevaluable horizontal margins (Rx resection), with no other poor prognosis features (including with no submucosal invasion at the margins), does not per se have an increased risk of LNM or distant metastasis [195] [201] [213]. However, in these cases, the risk of local persistence/recurrence may be as high as 30 % and for this reason, such a resection should be considered a local-risk resection. Since many of these recurrences are amenable to further endoscopic treatment, it is the present authors’ opinion that endoscopic surveillance or re-treatment are better initial options than surgery or other additional treatment (with these being considered if endoscopic re-treatment is not possible or fails) [196] [201].
29 ESGE recommends that when there is a diagnosis of lymphovascular invasion or deeper infiltration than sm1 or positive vertical margins or undifferentiated tumor or, for colorectal lesions, grade 2 or 3 budding, that the resection should be considered a high risk (noncurative) resection; complete staging should be done and strong consideration for additional treatments (chemoradiotherapy and/or surgery) should be given, on an individual basis in a multidisciplinary discussion.
Strong recommendation, moderate quality evidence.
Again, independently of the organ (see above), the poor prognostic features are the same: undifferentiated tumor, lymphovascular invasion, deep submucosal invasion, tumor budding in the colon, or a positive vertical margin, when carcinoma is present [148] [149] [168] [169] [197] [202]. In these cases, even though many patients will have no residual disease, the global LNM risk is potentially higher than the risk of further treatment. So, when one of these features is present, the ER should be considered a high risk (noncurative) resection. Complete staging should be done and strong consideration for additional treatments should be given on an individual basis, in a multidisciplinary discussion. Nevertheless, it should be noted that all these poor prognostic features do not carry the same weight, and the risk for LNM increases with the number of risk factors (with lymphovascular invasion being the strongest and deep submucosal invasion the weakest predictor for LNM). This should be taken into account in the multidisciplinary decision-making, recognizing that surveillance may be an option in some scenarios, particularly in old and unfit patients.
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6 Surveillance after endoscopic resection
6.1 Endoscopic surveillance
30 ESGE recommends scheduled endoscopic surveillance with high definition white-light and chromoendoscopy (virtual or dye-based) with biopsies of only the suspicious areas after a curative ESD.
Strong recommendation, moderate quality evidence.
In general, close surveillance after ER is needed to detect local recurrences and metachronous lesions, since ER leaves a larger area of mucosa than does surgery and the risk of new lesions may be as high as 1 %–5 % per year, justifying scheduled endoscopic surveillance in every organ. As we have seen, CE increases detection, allows better characterization of lesions, can guide biopsies of irregular areas, and should be used routinely after ESD [218]. Since after a curative/R0 resection the risk of recurrence is consistently lower than 1 %–2 %, routine biopsies of the ESD scar are not recommended.
The question of when to stop endoscopic surveillance has not been answered, since the majority of studies show a steady increase of metachronous lesions over time (older patients being especially at higher risk), and so the benefit of discovering or treating an early lesion should be balanced against age, comorbidities, and life-expectancy. In conclusion, the decision to stop surveillance should be individualized.
31 ESGE recommends that after piecemeal resection or in the presence of positive lateral margins when criteria for additional treatment are not met, a high definition chromoendoscopy (virtual and/or dye-based) with biopsies is recommended at 3–6 months.
Weak recommendation, low quality evidence.
As we have seen, in all cases and organs, the presence of horizontal margins that are positive or nonevaluable (HM1/HMx) increases local recurrence rates, with the recurrences most of the time being amenable to further endoscopic treatment if diagnosed early. In these cases, we suggest at least two endoscopies/colonoscopies with biopsies in the first 12–18 months (the first in the first 3–6 months after ER and the second depending on the organ and on the result of the first). After the first endoscopy without histologically confirmed recurrence, we then recommend the same surveillance protocol as for curative resections.
32 For upper GI superficial lesions, ESGE suggests endoscopy at 3–6 months and then annually after a curative ESD resection or after a local-risk ESD resection without recurrence.
Weak recommendation, low quality evidence.
6.1.1 Esophageal SCC lesions
In a recent Western report on long term follow-up after ER, the recurrence rate was 23.7 % (19/80) in the endoscopic mucosal resection (EMR) group and 2.9 % (2/68) in the ESD group (P = 0.002). The median follow-up time before recurrence was 4 months (range 2–23 months), suggesting early follow-ups (at 3–6 months) and then annually [71]. Some new studies confirmed the need for close surveillance stated in the previous ESGE guideline of 2015. Even though some risk factors for recurrence have been described, such as male sex, alcohol consumption, smoking, and others, there is insufficient evidence to suggest different follow-up in these cases [219] [220] [221] [222]. A large trial in 886 specimens found 5 % had positive/nonevaluable horizontal tumor margins (HM1/HMx), with a 26.7 % recurrence rate. HM1/HMx lesions with less than 1 mm between the cancer and specimen edge were associated with substantial risk of local recurrence, and strict follow-up is recommended in these cases [223].
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6.1.2 BE-associated lesions
Recurrence of intestinal metaplasia (IM) and dysplasia occurs even after complete ablation of the entire BE segment and therefore surveillance should be performed after therapy [82] [173]. It is recommended that biopsies should be taken during surveillance endoscopy at the esophagogastric junction (EGJ) and within the extent of the previous BE.
In a recent publication Cotton and co-workers built and validated a model to predict the incidence of neoplasia recurrence after initially successful RFA [224]. They used data from the United States Radiofrequency Ablation Registry and the United Kingdom National Halo Registry. According to this model, surveillance endoscopies for patients with high grade dysplasia or intramucosal adenocarcinoma should be performed at 3, 6, and 12 months and then annually, resulting in detection of unresectable cancers during surveillance at rates of less than 1/1000 endoscopies.
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6.1.3 Stomach
After a curative ER, the risk of LNM is low or very low, but there is a very low risk of recurrence and a moderate risk of metachronous lesions during follow-up (10 %–20 %) [192] [225] [226] [227] [228] [229] [230] [231]. There is evidence that Helicobacter pylori eradication decreases the risk of metachronous lesions and thus eradication is recommended if the patient has active H. pylori infection [232]. No other strategies showed benefit in decreasing risk of metachronous lesions, but there is consistent evidence that older patients and patients with synchronous or multiple lesions at diagnosis and/or with extensive preneoplastic conditions are at higher risk [192] [225] [226] [227] [228] [229] [230] [231]. However, to date there are no data showing that these risk factors should influence surveillance intervals. Most centers perform an endoscopy 3–6 months after ESD and then annually for at least 5 years. Indeed, a study found that a surveillance interval > 12 months was associated with significantly larger and more advanced metachronous lesions, and a significantly higher proportion needed surgical treatment when compared with metachronous lesions in patients with surveillance intervals ≤ 12 months [233].
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6.1.4 Colorectal lesions
33 ESGE suggests colonoscopy at 12 months and then further surveillance in accordance with polypectomy and colorectal cancer guidelines, after a local-risk ESD resection without recurrence or after a low or very low risk (curative) ESD of a colorectal malignant lesion.
Weak recommendation, low quality evidence.
After a curative resection for T1 colorectal carcinoma, the risk of local and distant recurrences seems negligible [234] [235]. Local recurrences were found to be 0.7 % at 2 years after curative treatment in 3278 patients with CRC who warranted adjuvant treatment (the majority because of N + disease) [236]. However, the same study showed that the incidence of a second primary CRC was as high as 1.5 % at 5 years [236]. From these results, Hassan et al. showed that 1-year surveillance colonoscopy was then cost-effective, allowing lesions to be found at an earlier stage than the previously recommended colonoscopy at 3 years [237].
Hence, there is no clear evidence to inform decisions on optimal post-ESD surveillance. If ESD had been performed for a good indication then it is predictable that the resected lesion will be high risk or malignant. Most authors recommend follow-up endoscopy in the first year after resection in order to verify complete removal and exclude synchronous/metachronous lesions. If technical success is confirmed, ESGE then recommends further surveillance in accordance with polypectomy and colorectal cancer surveillance guidelines [238] [239].
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6.2 Other surveillance methods
34 ESGE does not suggest routine use of EUS, MRI, CT, or PET in the follow-up after a very low or low risk (curative) endoscopic resection, but this might be considered in the cases of T1a-m3 /T1b-sm1 esophageal SCC particularly if no additional treatment has been decided.
Weak recommendation, very low quality evidence.
Since the risk of LNM after a curative resection is very low (in most cases and organs < 1 %–3 %), there is no evidence to suggest routine radiological surveillance in these cases. The exception might be after ER of T1a-m3/T1b-sm1 esophageal SCCs since, as we have seen, the natural history of these tumors is not clearly defined.
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7 Pathological aspects
A complete discussion of pathological issues and the definitions are provided in Appendix 2 s (Pathology and definitions). ESGE recommends that patients who undergo ESD because of malignant lesions are treated by multidisciplinary teams, with the following recommendations for management, based on endoscopic and pathology reports as detailed in [Table 2].
In this update of the ESD guideline, we considered four levels of risk related to ER, including two levels of “curative” ER based on different levels of LNM risk.
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Very low risk resection. In this case the risk of LNM is almost null and lower than 0.5 % (global LNM risk should not be higher than 1 %). In general, this applies to en bloc, R0 resection of dysplasia/pT1a cancers, that are differentiated with no lymphatic and no vascular invasion (L0 and V0). In these cases, the risk of local or distant recurrence is almost nonexistent, and only endoscopic surveillance is recommended with no further staging method or treatment.
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Low risk resection. In these cases the risk of LNM is generally very low and lower than 2 % (global LNM risk should be lower than 3 %). In general, this applies to en bloc, R0 resection of T1b-sm1 cancers that are differentiated, L0 and V0, and with other organ-specific characteristics. The risk of distant recurrence is low, and lower than the risks of further therapy. Although additional treatments are generally not recommended they can be considered in specific patients and scenarios, to further decrease the risk of LNM. However in all these cases, even though ER is considered “curative,” complete staging is recommended since these lesions represent true malignant disease.
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Local risk resection. This category includes piecemeal resection or where the horizontal margin is positive or unassessable (HM1 or HMx; thus Rx resection) and with no poor prognostic features for distant metastasis (including no submucosal invasion at the margins). In these cases, the risk of LNM is almost null, but the risk of local persistence/recurrence may be as high as 30 % and a stricter endoscopic surveillance (and/or treatment) is recommended.
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High risk resection (“noncurative”). This includes R0 or Rx ERs but with at least one poor prognostic feature (poor differentiation, lymphovascular invasion, deep submucosal invasion, tumor budding in the colon); or R1 resection (implying a positive vertical margin [VM1]), when carcinoma is present. In these cases, even though most patients will have no residual disease, the global LNM risk is higher than 3 % and in general this risk is higher than the risk of further treatment. Complete staging and additional nonendoscopic treatments are recommended in these cases (although surveillance may be an option in old and unfit patients).
It is important to note that most of this evidence comes from retrospective studies based on surgical specimens that may not have been pathologically handled and analyzed in the same manner as ER specimens. Furthermore, organ-specific considerations should be taken into account when deciding the type of ER and further decisions (see above).
Regarding what should be considered a safe VM (for more details, see Appendix 2 s), this issue is highly controversial, particularly as regards the colon since in the other organs this is rarely reported. For the colon most Western societies recommend that a safe margin should be ≥ 1 mm [239] [240]. But in fact, no validated data are available on the size of the safety margin after ER, which is why it is not mentioned in Asian guidelines [35]. In the largest meta-analysis that evaluated pathologic factors for LNM in early colorectal cancer, no increased risk was observed for a positive margin (OR 1.44, 95 %CI 0.52–4.03) [202]. Moreover, in the study that most societies use to justify the 1 mm margin, residual invasive disease in the colon wall was noted in 16 % with < 1 mm polypectomy margin, in 21 % with an indeterminate margin, and in 0 % with a margin ≥ 1 mm (P = 0.009), but this was not a risk factor for LNM [241]. Another study showed that although 63 % of resection margins were not deemed tumor-free, subsequent surgical specimens showed residual carcinoma in only 2.8 % of all patients but LNM in 7.6 %. However, in this study a free margin was not defined as a tumor-free extent of more than 1 mm; instead the resected specimen was only considered positive if there was lesion at the margin (R1) or limited assessability due to coagulation artefacts (Rx) [209].
Therefore, we believe that there is no evidence supporting the concept that a tumor-free margin of extent less than 1 mm should be considered a positive margin and, consequently, an indication for surgery. However, we recognize that smaller margins may increase the risk of persistent local disease (that can be recognized in the surveillance endoscopies). Therefore, in the present Guideline ESGE recommends the use of the term “preferably 1 mm,” but if the margin is smaller than 1 mm but free of tumor this should have no consequences for the clinical routine other than a stricter follow-up.
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Disclaimer
The legal disclaimer for ESGE guidelines [5] applies to this Guideline.
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Competing interests
P. Bhandari provides consultancy to Boston Scientific (2018–2022); his department has received research grants from Olympus UK (2019–2022), Fujifilm Europe (2019–2022), 3-D Matrix (2019–2022), and NEC Japan (2018–2022). M.J. Bourke has received research support from Boston Scientific, Olympus, and Cook Medical (2016 to 2022, ongoing). P.H. Deprez has received lecture fees from Olympus (2010–2021) and Erbe (2010–2020). M. Dinis Ribeiro is Co-Editor-in-Chief of Endoscopy; he has provided consultancy to Medtronic (2021) and Roche (2022); his department has received a research grant (loan) from Fujifilm (2021–2022). A. Lemmers has received consultancy fees from Cook Endoscopy (2021); his department receives a research grant from Boston Scientific (2021–2023). R. Maselli has provided consultancy to Erbe Medical (2018 to present); her department has received consultancy from Fujifilm (2018 to present). O. Pech has received speaker’s honoraria from Medtronic, Boston Scientific, Fujifilm, and Olympus (over 5 years). M. Pioche has provided consultancy and training for Olympus, Pentax, Cook, and Norgine (2017–2022). J.E. van Hooft’s department has received research grants from Cook Medical (2014–2019) and Abbott (2014–2017); she has received lecture fees from Medtronics (2014–2015, 2019), Cook Medical (2019), and Abbvie (2021), and consultancy fees from Boston Scientific (2014–2017) and Olympus (2021). B.L.A.M. Weusten has received financial support for IRB-approved studies from Pentax Medical (2017–2022), and financial research support from Aqua Medical (2020–2022), and has provided consultancy to Pentax Medical (2021–2022). D. Libânio, B.A.J. Bastiaansen, R. Bisschops, G. Esposito, H. Messman, P. Pimentel-Nunes, and M. Vieth have no competing interests.
Acknowledgments
The authors are grateful to Dr. Cesare Hassan, Humanitas University, Rozzano, Milan, Italy, and Dr. Enrique Rodriguez de Santiago, Hospital Univesitario Ramón y Cajal, Madrid, Spain, for their review of the Guideline.
* Joint first authors
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References
- 1 Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T. et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: 829-854
- 2 Veitch AM, Vanbiervliet G, Gershlick AH. et al. Endoscopy in patients on antiplatelet or anticoagulant therapy, including direct oral anticoagulants: British Society of Gastroenterology (BSG) and European Society of Gastrointestinal Endoscopy (ESGE) guidelines. Endoscopy 2016; 48: 385-402
- 3 Pimentel-Nunes P, Pioche M, Albeniz E. et al. Curriculum for endoscopic submucosal dissection training in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2019; 51: 980-992
- 4 Atkins D, Eccles M, Flottorp S. et al. Systems for grading the quality of evidence and the strength of recommendations I: critical appraisal of existing approaches The GRADE Working Group. BMC Health Serv Res 2004; 4: 38
- 5 Hassan C, Ponchon T, Bisschops R. et al. European Society of Gastrointestinal Endoscopy (ESGE) Publications Policy – Update 2020. Endoscopy 2020; 52: 123-126
- 6 Endoscopic Classification Review Group. Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 2005; 37: 570-578
- 7 Dekker E, Houwen B, Puig I. et al. Curriculum for optical diagnosis training in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2020; 52: 899-923
- 8 Morita FH, Bernardo WM, Ide E. et al. Narrow band imaging versus lugol chromoendoscopy to diagnose squamous cell carcinoma of the esophagus: a systematic review and meta-analysis. BMC Cancer 2017; 17: 54
- 9 Gruner M, Denis A, Masliah C. et al. Narrow-band imaging versus Lugol chromoendoscopy for esophageal squamous cell cancer screening in normal endoscopic practice: randomized controlled trial. Endoscopy 2021; 53: 674-682
- 10 Costa-Santos MP, Ferreira AO, Mouradides C. et al. Is Lugol necessary for endoscopic resection of esophageal squamous cell neoplasia?. Endosc Int Open 2020; 8: E1471-E1477
- 11 Yu T, Geng J, Song W. et al. Diagnostic accuracy of magnifying endoscopy with narrow band imaging and its diagnostic value for invasion depth staging in esophageal squamous cell carcinoma: a systematic review and meta-analysis. Biomed Res Int 2018; 2018: 8591387
- 12 Oyama T, Inoue H, Arima M. et al. Prediction of the invasion depth of superficial squamous cell carcinoma based on microvessel morphology: magnifying endoscopic classification of the Japan Esophageal Society. Esophagus 2017; 14: 105-112
- 13 Fujiyoshi T, Tajika M, Tanaka T. et al. Comparative evaluation of new and conventional classifications of magnifying endoscopy with narrow band imaging for invasion depth of superficial esophageal squamous cell carcinoma. Dis Esophagus 2017; 30: 1-8
- 14 Katada C, Tanabe S, Wada T. et al. Retrospective assessment of the diagnostic accuracy of the depth of invasion by narrow band imaging magnifying endoscopy in patients with superficial esophageal squamous cell carcinoma. J Gastrointest Cancer 2019; 50: 292-297
- 15 Ueda T, Dohi O, Naito Y. et al. Diagnostic performance of magnifying blue laser imaging versus magnifying narrow-band imaging for identifying the depth of invasion of superficial esophageal squamous cell carcinoma. Dis Esophagus 2020; DOI: 10.1093/dote/doaa078.
- 16 Pech O, Gossner L, Manner H. et al. Prospective evaluation of the macroscopic types and location of early Barrett’s neoplasia in 380 lesions. Endoscopy 2007; 39: 588-593
- 17 Thomas T, Gilbert D, Kaye PV. et al. High-resolution endoscopy and endoscopic ultrasound for evaluation of early neoplasia in Barrett’s esophagus. Surg Endosc 2010; 24: 1110-1116
- 18 Kandiah K, Chedgy FJQ, Subramaniam S. et al. International development and validation of a classification system for the identification of Barrett’s neoplasia using acetic acid chromoendoscopy: the Portsmouth acetic acid classification (PREDICT). Gut 2018; 67: 2085-2091
- 19 Coletta M, Sami SS, Nachiappan A. et al. Acetic acid chromoendoscopy for the diagnosis of early neoplasia and specialized intestinal metaplasia in Barrett’s esophagus: a meta-analysis. Gastrointest Endosc 2016; 83: 57-67.e51
- 20 Sharma P, Bergman JJ, Goda K. et al. Development and validation of a classification system to identify high-grade dysplasia and esophageal adenocarcinoma in Barrett’s esophagus using narrow-band imaging. Gastroenterology 2016; 150: 591-598
- 21 Nogales O, Caballero-Marcos A, Clemente-Sanchez A. et al. Usefulness of non-magnifying narrow band imaging in EVIS EXERA III video systems and high-definition endoscopes to diagnose dysplasia in Barrett’s esophagus using the Barrett International NBI Group (BING) classification. Dig Dis Sci 2017; 62: 2840-2846
- 22 Muto M, Yao K, Kaise M. et al. Magnifying endoscopy simple diagnostic algorithm for early gastric cancer (MESDA-G). Dig Endosc 2016; 28: 379-393
- 23 Uchita K, Yao K, Uedo N. et al. Highest power magnification with narrow-band imaging is useful for improving diagnostic performance for endoscopic delineation of early gastric cancers. BMC Gastroenterol 2015; 15: 155
- 24 Makazu M, Hirasawa K, Sato C. et al. Histological verification of the usefulness of magnifying endoscopy with narrow-band imaging for horizontal margin diagnosis of differentiated-type early gastric cancers. Gastric Cancer 2018; 21: 258-266
- 25 Horii Y, Dohi O, Naito Y. et al. Efficacy of magnifying narrow band imaging for delineating horizontal margins of early gastric cancer. Digestion 2019; 100: 93-99
- 26 Nakayoshi T, Tajiri H, Matsuda K. et al. Magnifying endoscopy combined with narrow band imaging system for early gastric cancer: correlation of vascular pattern with histopathology (including video). Endoscopy 2004; 36: 1080-1084
- 27 Ok KS, Kim GH, Park doY. et al. Magnifying endoscopy with narrow band imaging of early gastric cancer: Correlation with histopathology and mucin phenotype. Gut Liver 2016; 10: 532-541
- 28 Yagi K, Saka A, Nozawa Y. et al. Prediction of submucosal gastric cancer by narrow-band imaging magnifying endoscopy. Dig Liver Dis 2014; 46: 187-190
- 29 Kikuchi D, Iizuka T, Hoteya S. et al. Usefulness of magnifying endoscopy with narrow-band imaging for determining tumor invasion depth in early gastric cancer. Gastroenterol Res Pract 2013; 2013: 217695
- 30 Kobara H, Mori H, Fujihara S. et al. Prediction of invasion depth for submucosal differentiated gastric cancer by magnifying endoscopy with narrow-band imaging. Oncol Rep 2012; 28: 841-847
- 31 Kakushima N, Yoshida M, Yamaguchi Y. et al. Magnified endoscopy with narrow-band imaging for the differential diagnosis of superficial non-ampullary duodenal epithelial tumors. Scand J Gastroenterol 2019; 54: 128-134
- 32 Takahashi T, Ando T, Kabeshima Y. et al. Borderline cases between benignancy and malignancy of the duodenum diagnosed successfully by endoscopic submucosal dissection. Scand J Gastroenterol 2009; 44: 1377-1383
- 33 Kobayashi K, Tanaka S, Murakami Y. et al. Predictors of invasive cancer of large laterally spreading colorectal tumors: A multicenter study in Japan. JGH Open 2020; 4: 83-89
- 34 Bogie RMM, Veldman MHJ, Snijders L. et al. Endoscopic subtypes of colorectal laterally spreading tumors (LSTs) and the risk of submucosal invasion: a meta-analysis. Endoscopy 2018; 50: 263-282
- 35 Tanaka S, Kashida H, Saito Y. et al. Japan Gastroenterological Endoscopy Society guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc 2020; 32: 219-239
- 36 Hayashi N, Tanaka S, Hewett DG. et al. Endoscopic prediction of deep submucosal invasive carcinoma: validation of the narrow-band imaging international colorectal endoscopic (NICE) classification. Gastrointest Endosc 2013; 78: 625-632
- 37 Sumimoto K, Tanaka S, Shigita K. et al. Clinical impact and characteristics of the narrow-band imaging magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Gastrointest Endosc 2017; 85: 816-821
- 38 Vosko S, Shahidi N, Sidhu M. et al. Optical evaluation for predicting cancer in large nonpedunculated colorectal polyps is accurate for flat lesions. Clin Gastroenterol Hepatol 2021; DOI: 10.1016/j.cgh.2021.05.017.
- 39 Burgess NG, Hourigan LF, Zanati SA. et al. Risk stratification for covert invasive cancer among patients referred for colonic endoscopic mucosal resection: A large multicenter cohort. Gastroenterology 2017; 153: 732-742 e731
- 40 Bisschops R, East JE, Hassan C. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2019. Endoscopy 2019; 51: 1155-1179
- 41 Luo LN, He LJ, Gao XY. et al. Endoscopic ultrasound for preoperative esophageal squamous cell carcinoma: A meta-analysis. PLoS One 2016; 11: e0158373
- 42 Choi J, Chung H, Lee A. et al. Role of endoscopic ultrasound in selecting superficial esophageal cancers for endoscopic resection. Ann Thorac Surg 2020; 111: 1689-1695
- 43 Tao Z, Yan C, Zhao H. et al. Comparison of endoscopic ultrasonography and magnifying endoscopy for assessment of the invasion depth of shallow gastrointestinal neoplasms: a systematic review and meta-analysis. Surg Endosc 2017; 31: 4923-4933
- 44 Mizumoto T, Hiyama T, Oka S. et al. Diagnosis of superficial esophageal squamous cell carcinoma invasion depth before endoscopic submucosal dissection. Dis Esophagus 2018; 31 DOI: 10.1093/dote/dox142.
- 45 Guo J, Wang Z, Qin J. et al. A prospective analysis of the diagnostic accuracy of 3 T MRI, CT and endoscopic ultrasound for preoperative T staging of potentially resectable esophageal cancer. Cancer Imaging 2020; 20: 64
- 46 Qu J, Zhang H, Wang Z. et al. Comparison between free-breathing radial VIBE on 3-T MRI and endoscopic ultrasound for preoperative T staging of resectable oesophageal cancer, with histopathological correlation. Eur Radiol 2018; 28: 780-787
- 47 Nakajima M, Muroi H, Yokoyama H. et al. (18)-F-Fluorodeoxyglucose positron emission tomography can be used to determine the indication for endoscopic resection of superficial esophageal cancer. Cancer Med 2018; 7: 3604-3610
- 48 Toriyama K, Tajika M, Tanaka T. et al. Clinical relevance of fluorodeoxyglucose positron emission tomography/computed tomography and magnifying endoscopy with narrow band imaging in decision-making regarding the treatment strategy for esophageal squamous cell carcinoma. World J Gastroenterol 2019; 25: 6767-6780
- 49 Ishihara R, Goda K, Oyama T. Endoscopic diagnosis and treatment of esophageal adenocarcinoma: Introduction of Japan Esophageal Society classification of Barrett’s esophagus. J Gastroenterol 2019; 54: 1-9
- 50 Bulsiewicz WJ, Dellon ES, Rogers AJ. et al. The impact of endoscopic ultrasound findings on clinical decision making in Barrett’s esophagus with high-grade dysplasia or early esophageal adenocarcinoma. Dis Esophagus 2014; 27: 409-417
- 51 Thota PN, Sada A, Sanaka MR. et al. Correlation between endoscopic forceps biopsies and endoscopic mucosal resection with endoscopic ultrasound in patients with Barrett’s esophagus with high-grade dysplasia and early cancer. Surg Endosc 2017; 31: 1336-1341
- 52 Fairweather M, Jajoo K, Sainani N. et al. Accuracy of EUS and CT imaging in preoperative gastric cancer staging. J Surg Oncol 2015; 111: 1016-1020
- 53 Chung HW, Kim JH, Sung IK. et al. FDG PET/CT to predict the curability of endoscopic resection for early gastric cancer. J Cancer Res Clin Oncol 2019; 145: 759-764
- 54 Shi D, Xi XX. Factors affecting the accuracy of endoscopic ultrasonography in the diagnosis of early gastric cancer invasion depth: a meta-analysis. Gastroenterol Res Pract 2019; 2019: 8241381
- 55 Lee JY, Choi IJ, Kim CG. et al. Therapeutic decision-making using endoscopic ultrasonography in endoscopic treatment of early gastric cancer. Gut Liver 2016; 10: 42-50
- 56 Kuroki K, Oka S, Tanaka S. et al. Clinical significance of endoscopic ultrasonography in diagnosing invasion depth of early gastric cancer prior to endoscopic submucosal dissection. Gastric Cancer 2020; DOI: 10.1007/s10120–020–01100–5.
- 57 Kim EH, Park JC, Song IJ. et al. Prediction model for non-curative resection of endoscopic submucosal dissection in patients with early gastric cancer. Gastrointest Endosc 2017; 85: 976-983
- 58 Libanio D, Dinis-Ribeiro M, Pimentel-Nunes P. et al. Predicting outcomes of gastric endoscopic submucosal dissection using a Bayesian approach: a step for individualized risk assessment. Endosc Int Open 2017; 5: E563-E572
- 59 Ma X, Zhang Q, Zhu S. et al. Risk factors and prediction model for non-curative resection of early gastric cancer with endoscopic resection and the evaluation. Front Med (Lausanne) 2021; 8: 637875
- 60 Yamada T, Shimura T, Ebi M. et al. Subset analysis of a multicenter, randomized controlled trial to compare magnifying chromoendoscopy with endoscopic ultrasonography for stage diagnosis of early stage colorectal cancer. PLoS One 2015; 10: e0134942
- 61 Chan BPH, Patel R, Mbuagbaw L. et al. EUS versus magnetic resonance imaging in staging rectal adenocarcinoma: a diagnostic test accuracy meta-analysis. Gastrointest Endosc 2019; 90: 196-203.e191
- 62 Gao Y, Li J, Ma X. et al. The value of four imaging modalities in diagnosing lymph node involvement in rectal cancer: an overview and adjusted indirect comparison. Clin Exp Med 2019; 19: 225-234
- 63 Li XT, Sun YS, Tang L. et al. Evaluating local lymph node metastasis with magnetic resonance imaging, endoluminal ultrasound and computed tomography in rectal cancer: a meta-analysis. Colorectal Dis 2015; 17: O129-135
- 64 Li XT, Zhang XY, Sun YS. et al. Evaluating rectal tumor staging with magnetic resonance imaging, computed tomography, and endoluminal ultrasound: A meta-analysis. Medicine (Baltimore) 2016; 95: e5333
- 65 Nagami Y, Ominami M, Shiba M. et al. The five-year survival rate after endoscopic submucosal dissection for superficial esophageal squamous cell neoplasia. Dig Liver Dis 2017; 49: 427-433
- 66 Nishizawa T, Suzuki H. Long-term outcomes of endoscopic submucosal dissection for superficial esophageal squamous cell carcinoma. Cancers (Basel) 2020; 12 DOI: 10.3390/cancers12102849.
- 67 Oda I, Shimizu Y, Yoshio T. et al. Long-term outcome of endoscopic resection for intramucosal esophageal squamous cell cancer: a secondary analysis of the Japan Esophageal Cohort study. Endoscopy 2020; 52: 967-975
- 68 Ishihara R, Arima M, Iizuka T. et al. Endoscopic submucosal dissection/endoscopic mucosal resection guidelines for esophageal cancer. Dig Endosc 2020; 32: 452-493
- 69 Matsueda K, Matsuura N, Kanesaka T. et al. Validity of endoscopic resection for clinically diagnosed T1a-MM/T1b-SM1 N0 M0 esophageal squamous cell carcinoma. Esophagus 2021; DOI: 10.1007/s10388–021–00814–4.
- 70 Probst A, Aust D, Markl B. et al. Early esophageal cancer in Europe: endoscopic treatment by endoscopic submucosal dissection. Endoscopy 2015; 47: 113-121
- 71 Berger A, Rahmi G, Perrod G. et al. Long-term follow-up after endoscopic resection for superficial esophageal squamous cell carcinoma: a multicenter Western study. Endoscopy 2019; 51: 298-306
- 72 Cao Y, Liao C, Tan A. et al. Meta-analysis of endoscopic submucosal dissection versus endoscopic mucosal resection for tumors of the gastrointestinal tract. Endoscopy 2009; 41: 751-757
- 73 Guo HM, Zhang XQ, Chen M. et al. Endoscopic submucosal dissection vs endoscopic mucosal resection for superficial esophageal cancer. World J Gastroenterol 2014; 20: 5540-5547
- 74 Zhang Y, Ding H, Chen T. et al. Outcomes of endoscopic submucosal dissection vs esophagectomy for T1 esophageal squamous cell carcinoma in a real-world cohort. Clin Gastroenterol Hepatol 2019; 17: 73-81.e73
- 75 Min YW, Lee H, Song BG. et al. Comparison of endoscopic submucosal dissection and surgery for superficial esophageal squamous cell carcinoma: a propensity score-matched analysis. Gastrointest Endosc 2018; 88: 624-633
- 76 An W, Liu MY, Zhang J. et al. Endoscopic submucosal dissection versus esophagectomy for early esophageal squamous cell carcinoma with tumor invasion to different depths. Am J Cancer Res 2020; 10: 2977-2992
- 77 Yeh JH, Huang RY, Lee CT. et al. Long-term outcomes of endoscopic submucosal dissection and comparison to surgery for superficial esophageal squamous cancer: a systematic review and meta-analysis. Therap Adv Gastroenterol 2020; 13: 1756284820964316
- 78 Kato H, Sato A, Fukuda H. et al. A phase II trial of chemoradiotherapy for stage I esophageal squamous cell carcinoma: Japan Clinical Oncology Group Study (JCOG9708). Jpn J Clin Oncol 2009; 39: 638-643
- 79 Murakami Y, Takahashi I, Nishibuchi I. et al. Long-term results of definitive concurrent chemoradiotherapy for patients with esophageal submucosal cancer (T1bN0M0). Int J Clin Oncol 2015; 20: 897-904
- 80 Nakajo K, Yoda Y, Hori K. et al. Technical feasibility of endoscopic submucosal dissection for local failure after chemoradiotherapy or radiotherapy for esophageal squamous cell carcinoma. Gastrointest Endosc 2018; 88: 637-646
- 81 Abe S, Ishihara R, Takahashi H. et al. Long-term outcomes of endoscopic resection and metachronous cancer after endoscopic resection for adenocarcinoma of the esophagogastric junction in Japan. Gastrointest Endosc 2019; 89: 1120-1128
- 82 Phoa KN, Pouw RE, Bisschops R. et al. Multimodality endoscopic eradication for neoplastic Barrett oesophagus: results of an European multicentre study (EURO-II). Gut 2016; 65: 555-562
- 83 Yang D, Zou F, Xiong S. et al. Endoscopic submucosal dissection for early Barrett’s neoplasia: a meta-analysis. Gastrointest Endosc 2018; 87: 1383-1393
- 84 Han C, Sun Y. Efficacy and safety of endoscopic submucosal dissection versus endoscopic mucosal resection for superficial esophageal carcinoma: a systematic review and meta-analysis. Dis Esophagus 2020; DOI: 10.1093/dote/doaa081.
- 85 Codipilly DC, Dhaliwal L, Oberoi M. et al. Comparative outcomes of cap assisted endoscopic resection and endoscopic submucosal dissection in dysplastic Barrett’s esophagus. Clin Gastroenterol Hepatol 2020; DOI: 10.1016/j.cgh.2020.11.017.
- 86 Subramaniam S, Kandiah K, Chedgy F. et al. The safety and efficacy of radiofrequency ablation following endoscopic submucosal dissection for Barrett’s neoplasia. Dis Esophagus 2018; 31 DOI: 10.1093/dote/dox133.
- 87 Terheggen G, Horn EM, Vieth M. et al. A randomised trial of endoscopic submucosal dissection versus endoscopic mucosal resection for early Barrett’s neoplasia. Gut 2017; 66: 783-793
- 88 Coman RM, Gotoda T, Forsmark CE. et al. Prospective evaluation of the clinical utility of endoscopic submucosal dissection (ESD) in patients with Barrett’s esophagus: a Western center experience. Endosc Int Open 2016; 4: E715-721
- 89 Subramaniam S, Chedgy F, Longcroft-Wheaton G. et al. Complex early Barrett’s neoplasia at 3 Western centers: European Barrett’s Endoscopic Submucosal Dissection Trial (E-BEST). Gastrointest Endosc 2017; 86: 608-618
- 90 Yang D, Coman RM, Kahaleh M. et al. Endoscopic submucosal dissection for Barrett’s early neoplasia: a multicenter study in the United States. Gastrointest Endosc 2017; 86: 600-607
- 91 Chevaux JB, Piessevaux H, Jouret-Mourin A. et al. Clinical outcome in patients treated with endoscopic submucosal dissection for superficial Barrett’s neoplasia. Endoscopy 2015; 47: 103-112
- 92 Barret M, Cao DT, Beuvon F. et al. Endoscopic submucosal dissection for early Barrett’s neoplasia. United European Gastroenterol J 2016; 4: 207-215
- 93 Prasad GA, Wu TT, Wigle DA. et al. Endoscopic and surgical treatment of mucosal (T1a) esophageal adenocarcinoma in Barrett’s esophagus. Gastroenterology 2009; 137: 815-823
- 94 Pech O, Bollschweiler E, Manner H. et al. Comparison between endoscopic and surgical resection of mucosal esophageal adenocarcinoma in Barrett’s esophagus at two high-volume centers. Ann Surg 2011; 254: 67-72
- 95 Das A, Singh V, Fleischer DE. et al. A comparison of endoscopic treatment and surgery in early esophageal cancer: an analysis of surveillance epidemiology and end results data. Am J Gastroenterol 2008; 103: 1340-1345
- 96 Marino KA, Sullivan JL, Weksler B. Esophagectomy versus endoscopic resection for patients with early-stage esophageal adenocarcinoma: A National Cancer Database propensity-matched study. J Thorac Cardiovasc Surg 2018; 155: 2211-2218.e1
- 97 Raman V, Jawitz OK, Voigt SL. et al. The effect of age on survival after endoscopic resection versus surgery for T1a esophageal cancer. J Thorac Cardiovasc Surg 2020; 160: 295-302.e293
- 98 Smith I, Kahaleh M. Endoscopic versus surgical therapy for Barrett’s esophagus neoplasia. Expert Rev Gastroenterol Hepatol 2015; 9: 31-35
- 99 Reddy CA, Tavakkoli A, Chen VL. et al. Long-term quality of life following endoscopic therapy compared to esophagectomy for neoplastic Barrett’s esophagus. Dig Dis Sci 2020; DOI: 10.1007/s10620–020–06377–1.
- 100 Tao M, Zhou X, Hu M. et al. Endoscopic submucosal dissection versus endoscopic mucosal resection for patients with early gastric cancer: a meta-analysis. BMJ Open 2019; 9: e025803
- 101 Zhao Y, Wang C. Long-term clinical efficacy and perioperative safety of endoscopic submucosal dissection versus endoscopic mucosal resection for early gastric cancer: an updated meta-analysis. Biomed Res Int 2018; 2018: 3152346
- 102 Suzuki H, Takizawa K, Hirasawa T. et al. Short-term outcomes of multicenter prospective cohort study of gastric endoscopic resection: “Real-world evidence” in Japan. Dig Endosc 2019; 31: 30-39
- 103 Tanabe S, Ishido K, Matsumoto T. et al. Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a multicenter collaborative study. Gastric Cancer 2017; 20: 45-52
- 104 Gotoda T, Iwasaki M, Kusano C. et al. Endoscopic resection of early gastric cancer treated by guideline and expanded National Cancer Centre criteria. Br J Surg 2010; 97: 868-871
- 105 Abdelfatah MM, Barakat M, Ahmad D. et al. Long-term outcomes of endoscopic submucosal dissection versus surgery in early gastric cancer: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2019; 31: 418-424
- 106 Liu Q, Ding L, Qiu X. et al. Updated evaluation of endoscopic submucosal dissection versus surgery for early gastric cancer: A systematic review and meta-analysis. Int J Surg 2020; 73: 28-41
- 107 Gu L, Khadaroo PA, Chen L. et al. Comparison of long-term outcomes of endoscopic submucosal dissection and surgery for early gastric cancer: a systematic review and meta-analysis. J Gastrointest Surg 2019; 23: 1493-1501
- 108 Li H, Feng LQ, Bian YY. et al. Comparison of endoscopic submucosal dissection with surgical gastrectomy for early gastric cancer: An updated meta-analysis. World J Gastrointest Oncol 2019; 11: 161-171
- 109 Libânio D, Braga V, Ferraz S. et al. Prospective comparative study of endoscopic submucosal dissection and gastrectomy for early neoplastic lesions including patients' perspectives. Endoscopy 2019; 51: 30-39
- 110 Najmeh S, Cools-Lartigue J, Mueller C. et al. Comparing laparoscopic to endoscopic resections for early gastric cancer in a high volume North American center. J Gastrointest Surg 2016; 20: 1547-1553
- 111 Kim YI, Kim YA, Kim CG. et al. Serial intermediate-term quality of life comparison after endoscopic submucosal dissection versus surgery in early gastric cancer patients. Surg Endosc 2018; 32: 2114-2122
- 112 Kim SG, Ji SM, Lee NR. et al. Quality of life after endoscopic submucosal dissection for early gastric cancer: a prospective multicenter cohort study. Gut Liver 2017; 11: 87-92
- 113 Choi JH, Kim ES, Lee YJ. et al. Comparison of quality of life and worry of cancer recurrence between endoscopic and surgical treatment for early gastric cancer. Gastrointest Endosc 2015; 82: 299-307
- 114 Perez-Cuadrado-Robles E, Queneherve L, Margos W. et al. Comparative analysis of ESD versus EMR in a large European series of non-ampullary superficial duodenal tumors. Endosc Int Open 2018; 6: E1008-E1014
- 115 Zou J, Chai N, Linghu E. et al. Clinical outcomes of endoscopic resection for non-ampullary duodenal laterally spreading tumors. Surg Endosc 2019; 33: 4048-4056
- 116 Perez-Cuadrado-Robles E, Queneherve L, Margos W. et al. ESD versus EMR in non-ampullary superficial duodenal tumors: a systematic review and meta-analysis. Endosc Int Open 2018; 6: E998-E1007
- 117 Hoteya S, Yahagi N, Iizuka T. et al. Endoscopic submucosal dissection for nonampullary large superficial adenocarcinoma/adenoma of the duodenum: feasibility and long-term outcomes. Endosc Int Open 2013; 1: 2-7
- 118 Yahagi N, Kato M, Ochiai Y. et al. Outcomes of endoscopic resection for superficial duodenal epithelial neoplasia. Gastrointest Endosc 2018; 88: 676-682
- 119 Nonaka S, Oda I, Tada K. et al. Clinical outcome of endoscopic resection for nonampullary duodenal tumors. Endoscopy 2015; 47: 129-135
- 120 Inoue T, Uedo N, Yamashina T. et al. Delayed perforation: a hazardous complication of endoscopic resection for non-ampullary duodenal neoplasm. Dig Endosc 2014; 26: 220-227
- 121 Basford PJ, George R, Nixon E. et al. Endoscopic resection of sporadic duodenal adenomas: comparison of endoscopic mucosal resection (EMR) with hybrid endoscopic submucosal dissection (ESD) techniques and the risks of late delayed bleeding. Surg Endosc 2014; 28: 1594-1600
- 122 Hara Y, Goda K, Dobashi A. et al. Short- and long-term outcomes of endoscopically treated superficial non-ampullary duodenal epithelial tumors. World J Gastroenterol 2019; 25: 707-718
- 123 Klein A, Nayyar D, Bahin FF. et al. Endoscopic mucosal resection of large and giant lateral spreading lesions of the duodenum: success, adverse events, and long-term outcomes. Gastrointest Endosc 2016; 84: 688-696
- 124 Klein A, Ahlenstiel G, Tate DJ. et al. Endoscopic resection of large duodenal and papillary lateral spreading lesions is clinically and economically advantageous compared with surgery. Endoscopy 2017; 49: 659-667
- 125 Lupu A, Faller J, Oung B. et al. Endoscopic submucosal dissection using countertraction with clips and rubber band allows safe en bloc resection of recurrent duodenal superficial lesions with intense fibrosis. Endoscopy 2020; 52: E398-E399
- 126 Niimi K, Fujishiro M, Kodashima S. et al. Long-term outcomes of endoscopic submucosal dissection for colorectal epithelial neoplasms. Endoscopy 2010; 42: 723-729
- 127 Saito Y, Yamada M, So E. et al. Colorectal endoscopic submucosal dissection: Technical advantages compared to endoscopic mucosal resection and minimally invasive surgery. Dig Endosc 2014; 26 (Suppl. 01) 52-61
- 128 Russo P, Barbeiro S, Awadie H. et al. Management of colorectal laterally spreading tumors: a systematic review and meta-analysis. Endosc Int Open 2019; 7: E239-E259
- 129 Rahmi G, Hotayt B, Chaussade S. et al. Endoscopic submucosal dissection for superficial rectal tumors: prospective evaluation in France. Endoscopy 2014; 46: 670-676
- 130 Ronnow CF, Uedo N, Toth E. et al. Endoscopic submucosal dissection of 301 large colorectal neoplasias: Outcome and learning curve from a specialized center in Europe. Endosc Int Open 2018; 6: E1340-E1348
- 131 Fuccio L, Hassan C, Ponchon T. et al. Clinical outcomes after endoscopic submucosal dissection for colorectal neoplasia: A systematic review and meta-analysis. Gastrointest Endosc 2017; 86: 74-86.e17
- 132 De Ceglie A, Hassan C, Mangiavillano B. et al. Endoscopic mucosal resection and endoscopic submucosal dissection for colorectal lesions: A systematic review. Crit Rev Oncol Hematol 2016; 104: 138-155
- 133 Fujiya M, Tanaka K, Dokoshi T. et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc 2015; 81: 583-595
- 134 Arezzo A, Passera R, Marchese N. et al. Systematic review and meta-analysis of endoscopic submucosal dissection vs endoscopic mucosal resection for colorectal lesions. United European Gastroenterol J 2016; 4: 18-29
- 135 Klein A, Tate DJ, Jayasekeran V. et al. Thermal ablation of mucosal defect margins reduces adenoma recurrence after colonic endoscopic mucosal resection. Gastroenterology 2019; 156: 604-613 e603
- 136 Sidhu M, Shahidi N, Gupta S. et al. Outcomes of thermal ablation of the mucosal defect margin after endoscopic mucosal resection: A prospective, international, multicenter trial of 1000 large nonpedunculated colorectal polyps. Gastroenterology 2021; 161: 163-170 e163
- 137 Fuccio L, Repici A, Hassan C. et al. Why attempt en bloc resection of non-pedunculated colorectal adenomas? A systematic review of the prevalence of superficial submucosal invasive cancer after endoscopic submucosal dissection. Gut 2018; 67: 1464-1474
- 138 Bahin FF, Heitman SJ, Rasouli KN. et al. Wide-field endoscopic mucosal resection versus endoscopic submucosal dissection for laterally spreading colorectal lesions: a cost-effectiveness analysis. Gut 2018; 67: 1965-1973
- 139 Keswani RN, Law R, Ciolino JD. et al. Adverse events after surgery for nonmalignant colon polyps are common and associated with increased length of stay and costs. Gastrointest Endosc 2016; 84: 296-303.e291
- 140 Patel M, Haque M, Kohli D. et al. Endoscopic resection reduces morbidity when compared to surgery in veterans with large and complex colorectal polyps. Surg Endosc 2020; DOI: 10.1007/s00464–020–07482-y.
- 141 Gamaleldin M, Benlice C, Delaney CP. et al. Management of the colorectal polyp referred for resection: A case-matched comparison of advanced endoscopic surgery and laparoscopic colectomy. Surgery 2018; 163: 522-527
- 142 Nakamura F, Saito Y, Haruyama S. et al. Short-term prospective questionnaire study of early postoperative quality of life after colorectal endoscopic submucosal dissection. Dig Dis Sci 2017; 62: 3325-3335
- 143 Nam MJ, Sohn DK, Hong CW. et al. Cost comparison between endoscopic submucosal dissection and transanal endoscopic microsurgery for the treatment of rectal tumors. Ann Surg Treat Res 2015; 89: 202-207
- 144 Yamashita K, Oka S, Tanaka S. et al. Preceding endoscopic submucosal dissection for T1 colorectal carcinoma does not affect the prognosis of patients who underwent additional surgery: a large multicenter propensity score-matched analysis. J Gastroenterol 2019; 54: 897-906
- 145 Lowe D, Saleem S, Arif MO. et al. Role of endoscopic resection versus surgical resection in management of malignant colon polyps: A National Cancer Database analysis. J Gastrointest Surg 2020; 24: 177-187
- 146 Yeh JH, Tseng CH, Huang RY. et al. Long-term outcomes of primary endoscopic resection vs surgery for T1 colorectal cancer: A systematic review and meta-analysis. Clin Gastroenterol Hepatol 2020; 18: 2813-2823.e2815
- 147 Inoue T, Koyama F, Kuge H. et al. Short-term outcomes of endoscopic submucosal dissection versus laparoscopic surgery for colorectal neoplasms: An observational study. J Anus Rectum Colon 2018; 2: 97-102
- 148 Moon JY, Kim GH, Kim JH. et al. Clinicopathologic factors predicting lymph node metastasis in superficial esophageal squamous cell carcinoma. Scand J Gastroenterol 2014; 49: 589-594
- 149 Sgourakis G, Gockel I, Lang H. Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: a systematic review. World J Gastroenterol 2013; 19: 1424-1437
- 150 Xu W, Liu XB, Li SB. et al. Prediction of lymph node metastasis in superficial esophageal squamous cell carcinoma in Asia: a systematic review and meta-analysis. Dis Esophagus 2020; DOI: 10.1093/dote/doaa032.
- 151 Ye B, Zhang X, Su Y. et al. The possibility of endoscopic treatment of cN0 submucosal esophageal cancer: results from a surgical cohort. Surg Endosc 2020; DOI: 10.1007/s00464–020–07420-y.
- 152 Zhang Y, Liu L, Wang Q. et al. Endoscopic submucosal dissection with additional radiotherapy in the treatment of T1a esophageal squamous cell cancer: randomized controlled trial. Endoscopy 2020; 52: 1066-1074
- 153 Hisano O, Nonoshita T, Hirata H. et al. Additional radiotherapy following endoscopic submucosal dissection for T1a-MM/T1b-SM esophageal squamous cell carcinoma improves locoregional control. Radiat Oncol 2018; 13: 14
- 154 Ikeda A, Hoshi N, Yoshizaki T. et al. Endoscopic submucosal dissection (ESD) with additional therapy for superficial esophageal cancer with submucosal invasion. Intern Med 2015; 54: 2803-2813
- 155 Kawaguchi G, Sasamoto R, Abe E. et al. The effectiveness of endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer. Radiat Oncol 2015; 10: 31
- 156 Suzuki G, Yamazaki H, Aibe N. et al. Endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer: Choice of new approach. Radiat Oncol 2018; 13: 246
- 157 Yoshimizu S, Yoshio T, Ishiyama A. et al. Long-term outcomes of combined endoscopic resection and chemoradiotherapy for esophageal squamous cell carcinoma with submucosal invasion. Dig Liver Dis 2018; 50: 833-838
- 158 Minashi K, Nihei K, Mizusawa J. et al. Efficacy of endoscopic resection and selective chemoradiotherapy for stage I esophageal squamous cell carcinoma. Gastroenterology 2019; 157: 382-390.e383
- 159 Kitagawa Y, Uno T, Oyama T. et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: part 1. Esophagus 2019; 16: 1-24
- 160 Koterazawa Y, Nakamura T, Oshikiri T. et al. A comparison of the clinical outcomes of esophagectomy and chemoradiotherapy after noncurative endoscopic submucosal dissection for esophageal squamous cell carcinoma. Surg Today 2018; 48: 783-789
- 161 Tsou YK, Lee CH, Le PH. et al. Adjuvant therapy for pT1a-m3/pT1b esophageal squamous cell carcinoma after endoscopic resection: Esophagectomy or chemoradiotherapy?. A critical review. Crit Rev Oncol Hematol 2020; 147: 102883
- 162 Hirasawa K, Kokawa A, Oka H. et al. Superficial adenocarcinoma of the esophagogastric junction: long-term results of endoscopic submucosal dissection. Gastrointest Endosc 2010; 72: 960-966
- 163 Yoshinaga S, Gotoda T, Kusano C. et al. Clinical impact of endoscopic submucosal dissection for superficial adenocarcinoma located at the esophagogastric junction. Gastrointest Endosc 2008; 67: 202-209
- 164 Alvarez Herrero L, Pouw RE, van Vilsteren FG. et al. Risk of lymph node metastasis associated with deeper invasion by early adenocarcinoma of the esophagus and cardia: study based on endoscopic resection specimens. Endoscopy 2010; 42: 1030-1036
- 165 Manner H, May A, Pech O. et al. Early Barrett’s carcinoma with "low-risk" submucosal invasion: long-term results of endoscopic resection with a curative intent. Am J Gastroenterol 2008; 103: 2589-2597
- 166 Manner H, Pech O, Heldmann Y. et al. Efficacy, safety, and long-term results of endoscopic treatment for early stage adenocarcinoma of the esophagus with low-risk sm1 invasion. Clin Gastroenterol Hepatol 2013; quiz e645 11: 630-635
- 167 Manner H, Pech O, Heldmann Y. et al. The frequency of lymph node metastasis in early-stage adenocarcinoma of the esophagus with incipient submucosal invasion (pT1b sm1) depending on histological risk patterns. Surg Endosc 2015; 29: 1888-1896
- 168 Manner H, Wetzka J, May A. et al. Early-stage adenocarcinoma of the esophagus with mid to deep submucosal invasion (pT1b sm2–3): the frequency of lymph-node metastasis depends on macroscopic and histological risk patterns. Dis Esophagus 2017; 30: 1-11
- 169 Benech N, O’Brien JM, Barret M. et al. Endoscopic resection of Barrett’s adenocarcinoma: Intramucosal and low-risk tumours are not associated with lymph node metastases. United European Gastroenterol J 2021; 9: 362-369
- 170 Larghi A, Lightdale CJ, Ross AS. et al. Long-term follow-up of complete Barrett’s eradication endoscopic mucosal resection (CBE-EMR) for the treatment of high grade dysplasia and intramucosal carcinoma. Endoscopy 2007; 39: 1086-1091
- 171 Fleischer DE, Overholt BF, Sharma VK. et al. Endoscopic radiofrequency ablation for Barrett’s esophagus: 5-year outcomes from a prospective multicenter trial. Endoscopy 2010; 42: 781-789
- 172 Peters FP, Kara MA, Rosmolen WD. et al. Endoscopic treatment of high-grade dysplasia and early stage cancer in Barrett’s esophagus. Gastrointest Endosc 2005; 61: 506-514
- 173 Sawas T, Alsawas M, Bazerbachi F. et al. Persistent intestinal metaplasia after endoscopic eradication therapy of neoplastic Barrett’s esophagus increases the risk of dysplasia recurrence: meta-analysis. Gastrointest Endosc 2019; 89: 913-925 e916
- 174 Gotoda T, Yanagisawa A, Sasako M. et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 2000; 3: 219-225
- 175 Hirasawa T, Gotoda T, Miyata S. et al. Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer 2009; 12: 148-152
- 176 Nakahara K, Tsuruta O, Tateishi H. et al. Extended indication criteria for endoscopic mucosal resection of early gastric cancer with special reference to lymph node metastasis--examination by multivariate analysis. Kurume Med J 2004; 51: 9-14
- 177 Abdelfatah MM, Barakat M, Othman MO. et al. The incidence of lymph node metastasis in submucosal early gastric cancer according to the expanded criteria: a systematic review. Surg Endosc 2019; 33: 26-32
- 178 Chu YN, Yu YN, Jing X. et al. Feasibility of endoscopic treatment and predictors of lymph node metastasis in early gastric cancer. World J Gastroenterol 2019; 25: 5344-5355
- 179 Lee SH, Choi CW, Kim SJ. et al. Risk factors for lymph node metastasis in mucosal gastric cancer and re-evaluation of endoscopic submucosal dissection. Ann Surg Treat Res 2016; 91: 118-126
- 180 Choi KK, Bae JM, Kim SM. et al. The risk of lymph node metastases in 3951 surgically resected mucosal gastric cancers: implications for endoscopic resection. Gastrointest Endosc 2016; 83: 896-901
- 181 Ma DW, Lee SJ, Kook MC. et al. The suggestion of revised criteria for endoscopic resection of differentiated-type submucosal gastric cancer. Ann Surg Oncol 2020; 27: 795-801
- 182 Choi JY, Park YS, Jung HY. et al. Identifying predictors of lymph node metastasis after endoscopic resection in patients with minute submucosal cancer of the stomach. Surg Endosc 2015; 29: 1476-1483
- 183 Kim TS, Min BH, Kim KM. et al. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: low curative resection rate but favorable long-term outcomes after curative resection. Gastric Cancer 2019; 22: 363-368
- 184 Lee HJ, Kim GH, Park DY. et al. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: is it really safe?. Gastric Cancer 2017; 20: 978-986
- 185 Chen JN, Wang QW, Zhang QW. et al. Poorly differentiated is more significant than signet ring cell component for lymph node metastasis in mixed-type early gastric cancer: a retrospective study from a large-volume hospital. Surg Endosc 2020; DOI: 10.1007/s00464–020–07532–5.
- 186 Seo HS, Lee GE, Kang MG. et al. Mixed histology is a risk factor for lymph node metastasis in early gastric cancer. J Surg Res 2019; 236: 271-277
- 187 Lee IS, Lee S, Park YS. et al. Applicability of endoscopic submucosal dissection for undifferentiated early gastric cancer: Mixed histology of poorly differentiated adenocarcinoma and signet ring cell carcinoma is a worse predictive factor of nodal metastasis. Surg Oncol 2017; 26: 8-12
- 188 Lee JH, Choi IJ, Han HS. et al. Risk of lymph node metastasis in differentiated type mucosal early gastric cancer mixed with minor undifferentiated type histology. Ann Surg Oncol 2015; 22: 1813-1819
- 189 Takizawa K, Ono H, Yamamoto Y. et al. Incidence of lymph node metastasis in intramucosal gastric cancer measuring 30 mm or less, with ulceration; mixed, predominantly differentiated-type histology; and no lymphovascular invasion: a multicenter retrospective study. Gastric Cancer 2016; 19: 1144-1148
- 190 Takizawa K, Hatta W, Gotoda T. et al. Recurrence patterns and outcomes of salvage surgery in cases of non-curative endoscopic submucosal dissection without additional radical surgery for early gastric cancer. Digestion 2019; 99: 52-58
- 191 Yamada S, Hatta W, Shimosegawa T. et al. Different risk factors between early and late cancer recurrences in patients without additional surgery after noncurative endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc 2019; 89: 950-960
- 192 Libanio D, Pimentel-Nunes P, Afonso LP. et al. Long-term outcomes of gastric endoscopic submucosal dissection: Focus on metachronous and non-curative resection management. GE Port J Gastroenterol 2017; 24: 31-39
- 193 Hatta W, Gotoda T, Oyama T. et al. A scoring system to stratify curability after endoscopic submucosal dissection for early gastric cancer: "eCura system". Am J Gastroenterol 2017; 112: 874-881
- 194 Hatta W, Gotoda T, Oyama T. et al. Is the eCura system useful for selecting patients who require radical surgery after noncurative endoscopic submucosal dissection for early gastric cancer? A comparative study. Gastric Cancer 2018; 21: 481-489
- 195 Figueiredo PC, Pimentel-Nunes P, Libanio D. et al. A systematic review and meta-analysis on outcomes after Rx or R1 endoscopic resection of superficial gastric cancer. Eur J Gastroenterol Hepatol 2015; 27: 1249-1258
- 196 Jeon MY, Park JC, Hahn KY. et al. Long-term outcomes after noncurative endoscopic resection of early gastric cancer: the optimal time for additional endoscopic treatment. Gastrointest Endosc 2018; 87: 1003-1013.e1002
- 197 Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer 2020; DOI: 10.1007/s10120–020–01042-y.
- 198 Hirashita T, Ohta M, Tada K. et al. Prognostic factors of non-ampullary duodenal adenocarcinoma. Jpn J Clin Oncol 2018; 48: 743-747
- 199 Goda K, Kikuchi D, Yamamoto Y. et al. Endoscopic diagnosis of superficial non-ampullary duodenal epithelial tumors in Japan: Multicenter case series. Dig Endosc 2014; 26 (Suppl. 02) 23-29
- 200 Kuroki K, Sanomura Y, Oka S. et al. Clinical outcomes of endoscopic resection for superficial non-ampullary duodenal tumors. Endosc Int Open 2020; 8: E354-E359
- 201 Probst A, Freund S, Neuhaus L. et al. Complication risk despite preventive endoscopic measures in patients undergoing endoscopic mucosal resection of large duodenal adenomas. Endoscopy 2020; 52: 847-855
- 202 Choi JY, Jung SA, Shim KN. et al. Meta-analysis of predictive clinicopathologic factors for lymph node metastasis in patients with early colorectal carcinoma. J Korean Med Sci 2015; 30: 398-406
- 203 Bosch SL, Teerenstra S, de Wilt JH. et al. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 2013; 45: 827-834
- 204 Ronnow CF, Arthursson V, Toth E. et al. Lymphovascular infiltration, not depth of invasion, is the critical risk factor of metastases in early colorectal cancer: retrospective population-based cohort study on prospectively collected data, including validation. Ann Surg 2020; DOI: 10.1097/SLA.0000000000003854.
- 205 Kawachi H, Eishi Y, Ueno H. et al. A three-tier classification system based on the depth of submucosal invasion and budding/sprouting can improve the treatment strategy for T1 colorectal cancer: a retrospective multicenter study. Mod Pathol 2015; 28: 872-879
- 206 Han J, Hur H, Min BS. et al. Predictive factors for lymph node metastasis in submucosal invasive colorectal carcinoma: a new proposal of depth of invasion for radical surgery. World J Surg 2018; 42: 2635-2641
- 207 Ebbehoj AL, Jorgensen LN, Krarup PM. et al. Histopathological risk factors for lymph node metastases in T1 colorectal cancer: meta-analysis. Br J Surg 2021; DOI: 10.1093/bjs/znab168.
- 208 Cubiella J, Gonzalez A, Almazan R. et al. pT1 Colorectal cancer detected in a colorectal cancer mass screening program: treatment and factors associated with residual and extraluminal disease. Cancers (Basel) 2020; 12 DOI: 10.3390/cancers12092530.
- 209 Boenicke L, Fein M, Sailer M. et al. The concurrence of histologically positive resection margins and sessile morphology is an important risk factor for lymph node metastasis after complete endoscopic removal of malignant colorectal polyps. Int J Colorectal Dis 2010; 25: 433-438
- 210 Kim JY, Han SJ, Jung Y. et al. The relationship between local recurrence and positive lateral margin after en bloc resection of colorectal neoplasm. Scand J Gastroenterol 2018; 53: 1541-1546
- 211 Makazu M, Sakamoto T, So E. et al. Relationship between indeterminate or positive lateral margin and local recurrence after endoscopic resection of colorectal polyps. Endosc Int Open 2015; 3: E252-257
- 212 Yamada M, Saito Y, Takamaru H. et al. Long-term clinical outcomes of endoscopic submucosal dissection for colorectal neoplasms in 423 cases: a retrospective study. Endoscopy 2017; 49: 233-242
- 213 Backes Y, de Vos Tot Nederveen Cappel WH, van Bergeijk J. et al. Risk for incomplete resection after macroscopic radical endoscopic resection of T1 colorectal cancer: A multicenter cohort study. Am J Gastroenterol 2017; 112: 785-796
- 214 Chen K, Cao G, Chen B. et al. Laparoscopic versus open surgery for rectal cancer: A meta-analysis of classic randomized controlled trials and high-quality nonrandomized Studies in the last 5 years. Int J Surg 2017; 39: 1-10
- 215 Wu Q, Wei M, Ye Z. et al. Laparoscopic colectomy versus open colectomy for treatment of transverse colon cancer: A systematic review and meta-analysis. J Laparoendosc Adv Surg Tech A 2017; 27: 1038-1050
- 216 Jeong JU, Nam TK, Kim HR. et al. Adjuvant chemoradiotherapy instead of revision radical resection after local excision for high-risk early rectal cancer. Radiat Oncol 2016; 11: 114
- 217 Sasaki T, Ito Y, Ohue M. et al. Postoperative chemoradiotherapy after local resection for high-risk T1 to T2 low rectal cancer: Results of a single-arm, multi-institutional, phase II clinical trial. Dis Colon Rectum 2017; 60: 914-921
- 218 Barbeiro S, Libanio D, Castro R. et al. Narrow-band imaging: Clinical application in gastrointestinal endoscopy. GE Port J Gastroenterol 2018; 26: 40-53
- 219 Kim GH, Min YW, Lee H. et al. Risk factors of metachronous recurrence after endoscopic submucosal dissection for superficial esophageal squamous cell carcinoma. PLoS One 2020; 15: e0238113
- 220 Sawada G, Niida A, Uchi R. et al. Genomic landscape of esophageal squamous cell carcinoma in a Japanese population. Gastroenterology 2016; 150: 1171-1182
- 221 Uno K, Koike T, Kusaka G. et al. Risk of metachronous recurrence after endoscopic submucosal dissection of esophageal squamous cell carcinoma. Dis Esophagus 2017; 30: 1-8
- 222 Urabe Y, Kagemoto K, Nakamura K. et al. Construction of a risk model for the development of metachronous squamous cell carcinoma after endoscopic resection of esopahageal squamous cell carcinoma. Esophagus 2019; 16: 141-146
- 223 Fukuda H, Ishihara R, Shimamoto Y. et al. Effect of horizontal margin status and risk of local recurrence after endoscopic submucosal dissection for superficial esophageal cancer. JGH Open 2020; 4: 160-165
- 224 Cotton CC, Haidry R, Thrift AP. et al. Development of evidence-based surveillance intervals after radiofrequency ablation of Barrett’s esophagus. Gastroenterology 2018; 155: 316-326.e316
- 225 Brito-Goncalves G, Libanio D, Marcos P. et al. Clinicopathologic characteristics of patients with gastric superficial neoplasia and risk factors for multiple lesions after endoscopic submucosal dissection in a Western country. GE Port J Gastroenterol 2020; 27: 76-89
- 226 Okada K, Suzuki S, Naito S. et al. Incidence of metachronous gastric cancer in patients whose primary gastric neoplasms were discovered after Helicobacter pylori eradication. Gastrointest Endosc 2019; 89: 1152-1159.e1151
- 227 Park WY, Lee SJ, Kim YK. et al. Occurrence of metachronous or synchronous lesions after endoscopic treatment of gastric epithelia dysplasia- impact of histologic features of background mucosa. Pathol Res Pract 2018; 214: 95-99
- 228 Yang HJ, Kim SG, Lim JH. et al. Novel risk stratification for metachronous recurrence after curative endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc 2018; 87: 419-428.e413
- 229 Yang HJ, Kim SG, Lim JH. et al. Surveillance strategy according to age after endoscopic resection of early gastric cancer. Surg Endosc 2018; 32: 846-854
- 230 Moon HS, Yun GY, Kim JS. et al. Risk factors for metachronous gastric carcinoma development after endoscopic resection of gastric dysplasia: Retrospective, single-center study. World J Gastroenterol 2017; 23: 4407-4415
- 231 Abe S, Oda I, Suzuki H. et al. Long-term surveillance and treatment outcomes of metachronous gastric cancer occurring after curative endoscopic submucosal dissection. Endoscopy 2015; 47: 1113-1118
- 232 Pimentel-Nunes P, Libanio D, Marcos-Pinto R. et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019; 51: 365-388
- 233 Hahn KY, Park JC, Kim EH. et al. Incidence and impact of scheduled endoscopic surveillance on recurrence after curative endoscopic resection for early gastric cancer. Gastrointest Endosc 2016; 84: 628-638.e621
- 234 Oka S, Tanaka S, Saito Y. et al. Local recurrence after endoscopic resection for large colorectal neoplasia: a multicenter prospective study in Japan. Am J Gastroenterol 2015; 110: 697-707
- 235 Yoshii S, Nojima M, Nosho K. et al. Factors associated with risk for colorectal cancer recurrence after endoscopic resection of T1 tumors. Clin Gastroenterol Hepatol 2014; 12: 292-302.e293
- 236 Green RJ, Metlay JP, Propert K. et al. Surveillance for second primary colorectal cancer after adjuvant chemotherapy: an analysis of Intergroup 0089. Ann Intern Med 2002; 136: 261-269
- 237 Hassan C, Pickhardt PJ, Zullo A. et al. Cost-effectiveness of early colonoscopy surveillance after cancer resection. Dig Liver Dis 2009; 41: 881-885
- 238 Hassan C, Antonelli G, Dumonceau JM. et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2020. Endoscopy 2020; 52: 687-700
- 239 Benson AB, Venook AP, Al-Hawary MM. et al. NCCN guidelines insights: Colon Cancer, version 2, 2018. J Natl Compr Canc Netw 2018; 16: 359-369
- 240 Shaukat A, Kaltenbach T, Dominitz JA. et al. Endoscopic recognition and management strategies for malignant colorectal polyps: Recommendations of the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 2020; 115: 1751-1767
- 241 Butte JM, Tang P, Gonen M. et al. Rate of residual disease after complete endoscopic resection of malignant colonic polyp. Dis Colon Rectum 2012; 55: 122-127
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References
- 1 Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T. et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: 829-854
- 2 Veitch AM, Vanbiervliet G, Gershlick AH. et al. Endoscopy in patients on antiplatelet or anticoagulant therapy, including direct oral anticoagulants: British Society of Gastroenterology (BSG) and European Society of Gastrointestinal Endoscopy (ESGE) guidelines. Endoscopy 2016; 48: 385-402
- 3 Pimentel-Nunes P, Pioche M, Albeniz E. et al. Curriculum for endoscopic submucosal dissection training in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2019; 51: 980-992
- 4 Atkins D, Eccles M, Flottorp S. et al. Systems for grading the quality of evidence and the strength of recommendations I: critical appraisal of existing approaches The GRADE Working Group. BMC Health Serv Res 2004; 4: 38
- 5 Hassan C, Ponchon T, Bisschops R. et al. European Society of Gastrointestinal Endoscopy (ESGE) Publications Policy – Update 2020. Endoscopy 2020; 52: 123-126
- 6 Endoscopic Classification Review Group. Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 2005; 37: 570-578
- 7 Dekker E, Houwen B, Puig I. et al. Curriculum for optical diagnosis training in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2020; 52: 899-923
- 8 Morita FH, Bernardo WM, Ide E. et al. Narrow band imaging versus lugol chromoendoscopy to diagnose squamous cell carcinoma of the esophagus: a systematic review and meta-analysis. BMC Cancer 2017; 17: 54
- 9 Gruner M, Denis A, Masliah C. et al. Narrow-band imaging versus Lugol chromoendoscopy for esophageal squamous cell cancer screening in normal endoscopic practice: randomized controlled trial. Endoscopy 2021; 53: 674-682
- 10 Costa-Santos MP, Ferreira AO, Mouradides C. et al. Is Lugol necessary for endoscopic resection of esophageal squamous cell neoplasia?. Endosc Int Open 2020; 8: E1471-E1477
- 11 Yu T, Geng J, Song W. et al. Diagnostic accuracy of magnifying endoscopy with narrow band imaging and its diagnostic value for invasion depth staging in esophageal squamous cell carcinoma: a systematic review and meta-analysis. Biomed Res Int 2018; 2018: 8591387
- 12 Oyama T, Inoue H, Arima M. et al. Prediction of the invasion depth of superficial squamous cell carcinoma based on microvessel morphology: magnifying endoscopic classification of the Japan Esophageal Society. Esophagus 2017; 14: 105-112
- 13 Fujiyoshi T, Tajika M, Tanaka T. et al. Comparative evaluation of new and conventional classifications of magnifying endoscopy with narrow band imaging for invasion depth of superficial esophageal squamous cell carcinoma. Dis Esophagus 2017; 30: 1-8
- 14 Katada C, Tanabe S, Wada T. et al. Retrospective assessment of the diagnostic accuracy of the depth of invasion by narrow band imaging magnifying endoscopy in patients with superficial esophageal squamous cell carcinoma. J Gastrointest Cancer 2019; 50: 292-297
- 15 Ueda T, Dohi O, Naito Y. et al. Diagnostic performance of magnifying blue laser imaging versus magnifying narrow-band imaging for identifying the depth of invasion of superficial esophageal squamous cell carcinoma. Dis Esophagus 2020; DOI: 10.1093/dote/doaa078.
- 16 Pech O, Gossner L, Manner H. et al. Prospective evaluation of the macroscopic types and location of early Barrett’s neoplasia in 380 lesions. Endoscopy 2007; 39: 588-593
- 17 Thomas T, Gilbert D, Kaye PV. et al. High-resolution endoscopy and endoscopic ultrasound for evaluation of early neoplasia in Barrett’s esophagus. Surg Endosc 2010; 24: 1110-1116
- 18 Kandiah K, Chedgy FJQ, Subramaniam S. et al. International development and validation of a classification system for the identification of Barrett’s neoplasia using acetic acid chromoendoscopy: the Portsmouth acetic acid classification (PREDICT). Gut 2018; 67: 2085-2091
- 19 Coletta M, Sami SS, Nachiappan A. et al. Acetic acid chromoendoscopy for the diagnosis of early neoplasia and specialized intestinal metaplasia in Barrett’s esophagus: a meta-analysis. Gastrointest Endosc 2016; 83: 57-67.e51
- 20 Sharma P, Bergman JJ, Goda K. et al. Development and validation of a classification system to identify high-grade dysplasia and esophageal adenocarcinoma in Barrett’s esophagus using narrow-band imaging. Gastroenterology 2016; 150: 591-598
- 21 Nogales O, Caballero-Marcos A, Clemente-Sanchez A. et al. Usefulness of non-magnifying narrow band imaging in EVIS EXERA III video systems and high-definition endoscopes to diagnose dysplasia in Barrett’s esophagus using the Barrett International NBI Group (BING) classification. Dig Dis Sci 2017; 62: 2840-2846
- 22 Muto M, Yao K, Kaise M. et al. Magnifying endoscopy simple diagnostic algorithm for early gastric cancer (MESDA-G). Dig Endosc 2016; 28: 379-393
- 23 Uchita K, Yao K, Uedo N. et al. Highest power magnification with narrow-band imaging is useful for improving diagnostic performance for endoscopic delineation of early gastric cancers. BMC Gastroenterol 2015; 15: 155
- 24 Makazu M, Hirasawa K, Sato C. et al. Histological verification of the usefulness of magnifying endoscopy with narrow-band imaging for horizontal margin diagnosis of differentiated-type early gastric cancers. Gastric Cancer 2018; 21: 258-266
- 25 Horii Y, Dohi O, Naito Y. et al. Efficacy of magnifying narrow band imaging for delineating horizontal margins of early gastric cancer. Digestion 2019; 100: 93-99
- 26 Nakayoshi T, Tajiri H, Matsuda K. et al. Magnifying endoscopy combined with narrow band imaging system for early gastric cancer: correlation of vascular pattern with histopathology (including video). Endoscopy 2004; 36: 1080-1084
- 27 Ok KS, Kim GH, Park doY. et al. Magnifying endoscopy with narrow band imaging of early gastric cancer: Correlation with histopathology and mucin phenotype. Gut Liver 2016; 10: 532-541
- 28 Yagi K, Saka A, Nozawa Y. et al. Prediction of submucosal gastric cancer by narrow-band imaging magnifying endoscopy. Dig Liver Dis 2014; 46: 187-190
- 29 Kikuchi D, Iizuka T, Hoteya S. et al. Usefulness of magnifying endoscopy with narrow-band imaging for determining tumor invasion depth in early gastric cancer. Gastroenterol Res Pract 2013; 2013: 217695
- 30 Kobara H, Mori H, Fujihara S. et al. Prediction of invasion depth for submucosal differentiated gastric cancer by magnifying endoscopy with narrow-band imaging. Oncol Rep 2012; 28: 841-847
- 31 Kakushima N, Yoshida M, Yamaguchi Y. et al. Magnified endoscopy with narrow-band imaging for the differential diagnosis of superficial non-ampullary duodenal epithelial tumors. Scand J Gastroenterol 2019; 54: 128-134
- 32 Takahashi T, Ando T, Kabeshima Y. et al. Borderline cases between benignancy and malignancy of the duodenum diagnosed successfully by endoscopic submucosal dissection. Scand J Gastroenterol 2009; 44: 1377-1383
- 33 Kobayashi K, Tanaka S, Murakami Y. et al. Predictors of invasive cancer of large laterally spreading colorectal tumors: A multicenter study in Japan. JGH Open 2020; 4: 83-89
- 34 Bogie RMM, Veldman MHJ, Snijders L. et al. Endoscopic subtypes of colorectal laterally spreading tumors (LSTs) and the risk of submucosal invasion: a meta-analysis. Endoscopy 2018; 50: 263-282
- 35 Tanaka S, Kashida H, Saito Y. et al. Japan Gastroenterological Endoscopy Society guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc 2020; 32: 219-239
- 36 Hayashi N, Tanaka S, Hewett DG. et al. Endoscopic prediction of deep submucosal invasive carcinoma: validation of the narrow-band imaging international colorectal endoscopic (NICE) classification. Gastrointest Endosc 2013; 78: 625-632
- 37 Sumimoto K, Tanaka S, Shigita K. et al. Clinical impact and characteristics of the narrow-band imaging magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Gastrointest Endosc 2017; 85: 816-821
- 38 Vosko S, Shahidi N, Sidhu M. et al. Optical evaluation for predicting cancer in large nonpedunculated colorectal polyps is accurate for flat lesions. Clin Gastroenterol Hepatol 2021; DOI: 10.1016/j.cgh.2021.05.017.
- 39 Burgess NG, Hourigan LF, Zanati SA. et al. Risk stratification for covert invasive cancer among patients referred for colonic endoscopic mucosal resection: A large multicenter cohort. Gastroenterology 2017; 153: 732-742 e731
- 40 Bisschops R, East JE, Hassan C. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2019. Endoscopy 2019; 51: 1155-1179
- 41 Luo LN, He LJ, Gao XY. et al. Endoscopic ultrasound for preoperative esophageal squamous cell carcinoma: A meta-analysis. PLoS One 2016; 11: e0158373
- 42 Choi J, Chung H, Lee A. et al. Role of endoscopic ultrasound in selecting superficial esophageal cancers for endoscopic resection. Ann Thorac Surg 2020; 111: 1689-1695
- 43 Tao Z, Yan C, Zhao H. et al. Comparison of endoscopic ultrasonography and magnifying endoscopy for assessment of the invasion depth of shallow gastrointestinal neoplasms: a systematic review and meta-analysis. Surg Endosc 2017; 31: 4923-4933
- 44 Mizumoto T, Hiyama T, Oka S. et al. Diagnosis of superficial esophageal squamous cell carcinoma invasion depth before endoscopic submucosal dissection. Dis Esophagus 2018; 31 DOI: 10.1093/dote/dox142.
- 45 Guo J, Wang Z, Qin J. et al. A prospective analysis of the diagnostic accuracy of 3 T MRI, CT and endoscopic ultrasound for preoperative T staging of potentially resectable esophageal cancer. Cancer Imaging 2020; 20: 64
- 46 Qu J, Zhang H, Wang Z. et al. Comparison between free-breathing radial VIBE on 3-T MRI and endoscopic ultrasound for preoperative T staging of resectable oesophageal cancer, with histopathological correlation. Eur Radiol 2018; 28: 780-787
- 47 Nakajima M, Muroi H, Yokoyama H. et al. (18)-F-Fluorodeoxyglucose positron emission tomography can be used to determine the indication for endoscopic resection of superficial esophageal cancer. Cancer Med 2018; 7: 3604-3610
- 48 Toriyama K, Tajika M, Tanaka T. et al. Clinical relevance of fluorodeoxyglucose positron emission tomography/computed tomography and magnifying endoscopy with narrow band imaging in decision-making regarding the treatment strategy for esophageal squamous cell carcinoma. World J Gastroenterol 2019; 25: 6767-6780
- 49 Ishihara R, Goda K, Oyama T. Endoscopic diagnosis and treatment of esophageal adenocarcinoma: Introduction of Japan Esophageal Society classification of Barrett’s esophagus. J Gastroenterol 2019; 54: 1-9
- 50 Bulsiewicz WJ, Dellon ES, Rogers AJ. et al. The impact of endoscopic ultrasound findings on clinical decision making in Barrett’s esophagus with high-grade dysplasia or early esophageal adenocarcinoma. Dis Esophagus 2014; 27: 409-417
- 51 Thota PN, Sada A, Sanaka MR. et al. Correlation between endoscopic forceps biopsies and endoscopic mucosal resection with endoscopic ultrasound in patients with Barrett’s esophagus with high-grade dysplasia and early cancer. Surg Endosc 2017; 31: 1336-1341
- 52 Fairweather M, Jajoo K, Sainani N. et al. Accuracy of EUS and CT imaging in preoperative gastric cancer staging. J Surg Oncol 2015; 111: 1016-1020
- 53 Chung HW, Kim JH, Sung IK. et al. FDG PET/CT to predict the curability of endoscopic resection for early gastric cancer. J Cancer Res Clin Oncol 2019; 145: 759-764
- 54 Shi D, Xi XX. Factors affecting the accuracy of endoscopic ultrasonography in the diagnosis of early gastric cancer invasion depth: a meta-analysis. Gastroenterol Res Pract 2019; 2019: 8241381
- 55 Lee JY, Choi IJ, Kim CG. et al. Therapeutic decision-making using endoscopic ultrasonography in endoscopic treatment of early gastric cancer. Gut Liver 2016; 10: 42-50
- 56 Kuroki K, Oka S, Tanaka S. et al. Clinical significance of endoscopic ultrasonography in diagnosing invasion depth of early gastric cancer prior to endoscopic submucosal dissection. Gastric Cancer 2020; DOI: 10.1007/s10120–020–01100–5.
- 57 Kim EH, Park JC, Song IJ. et al. Prediction model for non-curative resection of endoscopic submucosal dissection in patients with early gastric cancer. Gastrointest Endosc 2017; 85: 976-983
- 58 Libanio D, Dinis-Ribeiro M, Pimentel-Nunes P. et al. Predicting outcomes of gastric endoscopic submucosal dissection using a Bayesian approach: a step for individualized risk assessment. Endosc Int Open 2017; 5: E563-E572
- 59 Ma X, Zhang Q, Zhu S. et al. Risk factors and prediction model for non-curative resection of early gastric cancer with endoscopic resection and the evaluation. Front Med (Lausanne) 2021; 8: 637875
- 60 Yamada T, Shimura T, Ebi M. et al. Subset analysis of a multicenter, randomized controlled trial to compare magnifying chromoendoscopy with endoscopic ultrasonography for stage diagnosis of early stage colorectal cancer. PLoS One 2015; 10: e0134942
- 61 Chan BPH, Patel R, Mbuagbaw L. et al. EUS versus magnetic resonance imaging in staging rectal adenocarcinoma: a diagnostic test accuracy meta-analysis. Gastrointest Endosc 2019; 90: 196-203.e191
- 62 Gao Y, Li J, Ma X. et al. The value of four imaging modalities in diagnosing lymph node involvement in rectal cancer: an overview and adjusted indirect comparison. Clin Exp Med 2019; 19: 225-234
- 63 Li XT, Sun YS, Tang L. et al. Evaluating local lymph node metastasis with magnetic resonance imaging, endoluminal ultrasound and computed tomography in rectal cancer: a meta-analysis. Colorectal Dis 2015; 17: O129-135
- 64 Li XT, Zhang XY, Sun YS. et al. Evaluating rectal tumor staging with magnetic resonance imaging, computed tomography, and endoluminal ultrasound: A meta-analysis. Medicine (Baltimore) 2016; 95: e5333
- 65 Nagami Y, Ominami M, Shiba M. et al. The five-year survival rate after endoscopic submucosal dissection for superficial esophageal squamous cell neoplasia. Dig Liver Dis 2017; 49: 427-433
- 66 Nishizawa T, Suzuki H. Long-term outcomes of endoscopic submucosal dissection for superficial esophageal squamous cell carcinoma. Cancers (Basel) 2020; 12 DOI: 10.3390/cancers12102849.
- 67 Oda I, Shimizu Y, Yoshio T. et al. Long-term outcome of endoscopic resection for intramucosal esophageal squamous cell cancer: a secondary analysis of the Japan Esophageal Cohort study. Endoscopy 2020; 52: 967-975
- 68 Ishihara R, Arima M, Iizuka T. et al. Endoscopic submucosal dissection/endoscopic mucosal resection guidelines for esophageal cancer. Dig Endosc 2020; 32: 452-493
- 69 Matsueda K, Matsuura N, Kanesaka T. et al. Validity of endoscopic resection for clinically diagnosed T1a-MM/T1b-SM1 N0 M0 esophageal squamous cell carcinoma. Esophagus 2021; DOI: 10.1007/s10388–021–00814–4.
- 70 Probst A, Aust D, Markl B. et al. Early esophageal cancer in Europe: endoscopic treatment by endoscopic submucosal dissection. Endoscopy 2015; 47: 113-121
- 71 Berger A, Rahmi G, Perrod G. et al. Long-term follow-up after endoscopic resection for superficial esophageal squamous cell carcinoma: a multicenter Western study. Endoscopy 2019; 51: 298-306
- 72 Cao Y, Liao C, Tan A. et al. Meta-analysis of endoscopic submucosal dissection versus endoscopic mucosal resection for tumors of the gastrointestinal tract. Endoscopy 2009; 41: 751-757
- 73 Guo HM, Zhang XQ, Chen M. et al. Endoscopic submucosal dissection vs endoscopic mucosal resection for superficial esophageal cancer. World J Gastroenterol 2014; 20: 5540-5547
- 74 Zhang Y, Ding H, Chen T. et al. Outcomes of endoscopic submucosal dissection vs esophagectomy for T1 esophageal squamous cell carcinoma in a real-world cohort. Clin Gastroenterol Hepatol 2019; 17: 73-81.e73
- 75 Min YW, Lee H, Song BG. et al. Comparison of endoscopic submucosal dissection and surgery for superficial esophageal squamous cell carcinoma: a propensity score-matched analysis. Gastrointest Endosc 2018; 88: 624-633
- 76 An W, Liu MY, Zhang J. et al. Endoscopic submucosal dissection versus esophagectomy for early esophageal squamous cell carcinoma with tumor invasion to different depths. Am J Cancer Res 2020; 10: 2977-2992
- 77 Yeh JH, Huang RY, Lee CT. et al. Long-term outcomes of endoscopic submucosal dissection and comparison to surgery for superficial esophageal squamous cancer: a systematic review and meta-analysis. Therap Adv Gastroenterol 2020; 13: 1756284820964316
- 78 Kato H, Sato A, Fukuda H. et al. A phase II trial of chemoradiotherapy for stage I esophageal squamous cell carcinoma: Japan Clinical Oncology Group Study (JCOG9708). Jpn J Clin Oncol 2009; 39: 638-643
- 79 Murakami Y, Takahashi I, Nishibuchi I. et al. Long-term results of definitive concurrent chemoradiotherapy for patients with esophageal submucosal cancer (T1bN0M0). Int J Clin Oncol 2015; 20: 897-904
- 80 Nakajo K, Yoda Y, Hori K. et al. Technical feasibility of endoscopic submucosal dissection for local failure after chemoradiotherapy or radiotherapy for esophageal squamous cell carcinoma. Gastrointest Endosc 2018; 88: 637-646
- 81 Abe S, Ishihara R, Takahashi H. et al. Long-term outcomes of endoscopic resection and metachronous cancer after endoscopic resection for adenocarcinoma of the esophagogastric junction in Japan. Gastrointest Endosc 2019; 89: 1120-1128
- 82 Phoa KN, Pouw RE, Bisschops R. et al. Multimodality endoscopic eradication for neoplastic Barrett oesophagus: results of an European multicentre study (EURO-II). Gut 2016; 65: 555-562
- 83 Yang D, Zou F, Xiong S. et al. Endoscopic submucosal dissection for early Barrett’s neoplasia: a meta-analysis. Gastrointest Endosc 2018; 87: 1383-1393
- 84 Han C, Sun Y. Efficacy and safety of endoscopic submucosal dissection versus endoscopic mucosal resection for superficial esophageal carcinoma: a systematic review and meta-analysis. Dis Esophagus 2020; DOI: 10.1093/dote/doaa081.
- 85 Codipilly DC, Dhaliwal L, Oberoi M. et al. Comparative outcomes of cap assisted endoscopic resection and endoscopic submucosal dissection in dysplastic Barrett’s esophagus. Clin Gastroenterol Hepatol 2020; DOI: 10.1016/j.cgh.2020.11.017.
- 86 Subramaniam S, Kandiah K, Chedgy F. et al. The safety and efficacy of radiofrequency ablation following endoscopic submucosal dissection for Barrett’s neoplasia. Dis Esophagus 2018; 31 DOI: 10.1093/dote/dox133.
- 87 Terheggen G, Horn EM, Vieth M. et al. A randomised trial of endoscopic submucosal dissection versus endoscopic mucosal resection for early Barrett’s neoplasia. Gut 2017; 66: 783-793
- 88 Coman RM, Gotoda T, Forsmark CE. et al. Prospective evaluation of the clinical utility of endoscopic submucosal dissection (ESD) in patients with Barrett’s esophagus: a Western center experience. Endosc Int Open 2016; 4: E715-721
- 89 Subramaniam S, Chedgy F, Longcroft-Wheaton G. et al. Complex early Barrett’s neoplasia at 3 Western centers: European Barrett’s Endoscopic Submucosal Dissection Trial (E-BEST). Gastrointest Endosc 2017; 86: 608-618
- 90 Yang D, Coman RM, Kahaleh M. et al. Endoscopic submucosal dissection for Barrett’s early neoplasia: a multicenter study in the United States. Gastrointest Endosc 2017; 86: 600-607
- 91 Chevaux JB, Piessevaux H, Jouret-Mourin A. et al. Clinical outcome in patients treated with endoscopic submucosal dissection for superficial Barrett’s neoplasia. Endoscopy 2015; 47: 103-112
- 92 Barret M, Cao DT, Beuvon F. et al. Endoscopic submucosal dissection for early Barrett’s neoplasia. United European Gastroenterol J 2016; 4: 207-215
- 93 Prasad GA, Wu TT, Wigle DA. et al. Endoscopic and surgical treatment of mucosal (T1a) esophageal adenocarcinoma in Barrett’s esophagus. Gastroenterology 2009; 137: 815-823
- 94 Pech O, Bollschweiler E, Manner H. et al. Comparison between endoscopic and surgical resection of mucosal esophageal adenocarcinoma in Barrett’s esophagus at two high-volume centers. Ann Surg 2011; 254: 67-72
- 95 Das A, Singh V, Fleischer DE. et al. A comparison of endoscopic treatment and surgery in early esophageal cancer: an analysis of surveillance epidemiology and end results data. Am J Gastroenterol 2008; 103: 1340-1345
- 96 Marino KA, Sullivan JL, Weksler B. Esophagectomy versus endoscopic resection for patients with early-stage esophageal adenocarcinoma: A National Cancer Database propensity-matched study. J Thorac Cardiovasc Surg 2018; 155: 2211-2218.e1
- 97 Raman V, Jawitz OK, Voigt SL. et al. The effect of age on survival after endoscopic resection versus surgery for T1a esophageal cancer. J Thorac Cardiovasc Surg 2020; 160: 295-302.e293
- 98 Smith I, Kahaleh M. Endoscopic versus surgical therapy for Barrett’s esophagus neoplasia. Expert Rev Gastroenterol Hepatol 2015; 9: 31-35
- 99 Reddy CA, Tavakkoli A, Chen VL. et al. Long-term quality of life following endoscopic therapy compared to esophagectomy for neoplastic Barrett’s esophagus. Dig Dis Sci 2020; DOI: 10.1007/s10620–020–06377–1.
- 100 Tao M, Zhou X, Hu M. et al. Endoscopic submucosal dissection versus endoscopic mucosal resection for patients with early gastric cancer: a meta-analysis. BMJ Open 2019; 9: e025803
- 101 Zhao Y, Wang C. Long-term clinical efficacy and perioperative safety of endoscopic submucosal dissection versus endoscopic mucosal resection for early gastric cancer: an updated meta-analysis. Biomed Res Int 2018; 2018: 3152346
- 102 Suzuki H, Takizawa K, Hirasawa T. et al. Short-term outcomes of multicenter prospective cohort study of gastric endoscopic resection: “Real-world evidence” in Japan. Dig Endosc 2019; 31: 30-39
- 103 Tanabe S, Ishido K, Matsumoto T. et al. Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a multicenter collaborative study. Gastric Cancer 2017; 20: 45-52
- 104 Gotoda T, Iwasaki M, Kusano C. et al. Endoscopic resection of early gastric cancer treated by guideline and expanded National Cancer Centre criteria. Br J Surg 2010; 97: 868-871
- 105 Abdelfatah MM, Barakat M, Ahmad D. et al. Long-term outcomes of endoscopic submucosal dissection versus surgery in early gastric cancer: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2019; 31: 418-424
- 106 Liu Q, Ding L, Qiu X. et al. Updated evaluation of endoscopic submucosal dissection versus surgery for early gastric cancer: A systematic review and meta-analysis. Int J Surg 2020; 73: 28-41
- 107 Gu L, Khadaroo PA, Chen L. et al. Comparison of long-term outcomes of endoscopic submucosal dissection and surgery for early gastric cancer: a systematic review and meta-analysis. J Gastrointest Surg 2019; 23: 1493-1501
- 108 Li H, Feng LQ, Bian YY. et al. Comparison of endoscopic submucosal dissection with surgical gastrectomy for early gastric cancer: An updated meta-analysis. World J Gastrointest Oncol 2019; 11: 161-171
- 109 Libânio D, Braga V, Ferraz S. et al. Prospective comparative study of endoscopic submucosal dissection and gastrectomy for early neoplastic lesions including patients' perspectives. Endoscopy 2019; 51: 30-39
- 110 Najmeh S, Cools-Lartigue J, Mueller C. et al. Comparing laparoscopic to endoscopic resections for early gastric cancer in a high volume North American center. J Gastrointest Surg 2016; 20: 1547-1553
- 111 Kim YI, Kim YA, Kim CG. et al. Serial intermediate-term quality of life comparison after endoscopic submucosal dissection versus surgery in early gastric cancer patients. Surg Endosc 2018; 32: 2114-2122
- 112 Kim SG, Ji SM, Lee NR. et al. Quality of life after endoscopic submucosal dissection for early gastric cancer: a prospective multicenter cohort study. Gut Liver 2017; 11: 87-92
- 113 Choi JH, Kim ES, Lee YJ. et al. Comparison of quality of life and worry of cancer recurrence between endoscopic and surgical treatment for early gastric cancer. Gastrointest Endosc 2015; 82: 299-307
- 114 Perez-Cuadrado-Robles E, Queneherve L, Margos W. et al. Comparative analysis of ESD versus EMR in a large European series of non-ampullary superficial duodenal tumors. Endosc Int Open 2018; 6: E1008-E1014
- 115 Zou J, Chai N, Linghu E. et al. Clinical outcomes of endoscopic resection for non-ampullary duodenal laterally spreading tumors. Surg Endosc 2019; 33: 4048-4056
- 116 Perez-Cuadrado-Robles E, Queneherve L, Margos W. et al. ESD versus EMR in non-ampullary superficial duodenal tumors: a systematic review and meta-analysis. Endosc Int Open 2018; 6: E998-E1007
- 117 Hoteya S, Yahagi N, Iizuka T. et al. Endoscopic submucosal dissection for nonampullary large superficial adenocarcinoma/adenoma of the duodenum: feasibility and long-term outcomes. Endosc Int Open 2013; 1: 2-7
- 118 Yahagi N, Kato M, Ochiai Y. et al. Outcomes of endoscopic resection for superficial duodenal epithelial neoplasia. Gastrointest Endosc 2018; 88: 676-682
- 119 Nonaka S, Oda I, Tada K. et al. Clinical outcome of endoscopic resection for nonampullary duodenal tumors. Endoscopy 2015; 47: 129-135
- 120 Inoue T, Uedo N, Yamashina T. et al. Delayed perforation: a hazardous complication of endoscopic resection for non-ampullary duodenal neoplasm. Dig Endosc 2014; 26: 220-227
- 121 Basford PJ, George R, Nixon E. et al. Endoscopic resection of sporadic duodenal adenomas: comparison of endoscopic mucosal resection (EMR) with hybrid endoscopic submucosal dissection (ESD) techniques and the risks of late delayed bleeding. Surg Endosc 2014; 28: 1594-1600
- 122 Hara Y, Goda K, Dobashi A. et al. Short- and long-term outcomes of endoscopically treated superficial non-ampullary duodenal epithelial tumors. World J Gastroenterol 2019; 25: 707-718
- 123 Klein A, Nayyar D, Bahin FF. et al. Endoscopic mucosal resection of large and giant lateral spreading lesions of the duodenum: success, adverse events, and long-term outcomes. Gastrointest Endosc 2016; 84: 688-696
- 124 Klein A, Ahlenstiel G, Tate DJ. et al. Endoscopic resection of large duodenal and papillary lateral spreading lesions is clinically and economically advantageous compared with surgery. Endoscopy 2017; 49: 659-667
- 125 Lupu A, Faller J, Oung B. et al. Endoscopic submucosal dissection using countertraction with clips and rubber band allows safe en bloc resection of recurrent duodenal superficial lesions with intense fibrosis. Endoscopy 2020; 52: E398-E399
- 126 Niimi K, Fujishiro M, Kodashima S. et al. Long-term outcomes of endoscopic submucosal dissection for colorectal epithelial neoplasms. Endoscopy 2010; 42: 723-729
- 127 Saito Y, Yamada M, So E. et al. Colorectal endoscopic submucosal dissection: Technical advantages compared to endoscopic mucosal resection and minimally invasive surgery. Dig Endosc 2014; 26 (Suppl. 01) 52-61
- 128 Russo P, Barbeiro S, Awadie H. et al. Management of colorectal laterally spreading tumors: a systematic review and meta-analysis. Endosc Int Open 2019; 7: E239-E259
- 129 Rahmi G, Hotayt B, Chaussade S. et al. Endoscopic submucosal dissection for superficial rectal tumors: prospective evaluation in France. Endoscopy 2014; 46: 670-676
- 130 Ronnow CF, Uedo N, Toth E. et al. Endoscopic submucosal dissection of 301 large colorectal neoplasias: Outcome and learning curve from a specialized center in Europe. Endosc Int Open 2018; 6: E1340-E1348
- 131 Fuccio L, Hassan C, Ponchon T. et al. Clinical outcomes after endoscopic submucosal dissection for colorectal neoplasia: A systematic review and meta-analysis. Gastrointest Endosc 2017; 86: 74-86.e17
- 132 De Ceglie A, Hassan C, Mangiavillano B. et al. Endoscopic mucosal resection and endoscopic submucosal dissection for colorectal lesions: A systematic review. Crit Rev Oncol Hematol 2016; 104: 138-155
- 133 Fujiya M, Tanaka K, Dokoshi T. et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc 2015; 81: 583-595
- 134 Arezzo A, Passera R, Marchese N. et al. Systematic review and meta-analysis of endoscopic submucosal dissection vs endoscopic mucosal resection for colorectal lesions. United European Gastroenterol J 2016; 4: 18-29
- 135 Klein A, Tate DJ, Jayasekeran V. et al. Thermal ablation of mucosal defect margins reduces adenoma recurrence after colonic endoscopic mucosal resection. Gastroenterology 2019; 156: 604-613 e603
- 136 Sidhu M, Shahidi N, Gupta S. et al. Outcomes of thermal ablation of the mucosal defect margin after endoscopic mucosal resection: A prospective, international, multicenter trial of 1000 large nonpedunculated colorectal polyps. Gastroenterology 2021; 161: 163-170 e163
- 137 Fuccio L, Repici A, Hassan C. et al. Why attempt en bloc resection of non-pedunculated colorectal adenomas? A systematic review of the prevalence of superficial submucosal invasive cancer after endoscopic submucosal dissection. Gut 2018; 67: 1464-1474
- 138 Bahin FF, Heitman SJ, Rasouli KN. et al. Wide-field endoscopic mucosal resection versus endoscopic submucosal dissection for laterally spreading colorectal lesions: a cost-effectiveness analysis. Gut 2018; 67: 1965-1973
- 139 Keswani RN, Law R, Ciolino JD. et al. Adverse events after surgery for nonmalignant colon polyps are common and associated with increased length of stay and costs. Gastrointest Endosc 2016; 84: 296-303.e291
- 140 Patel M, Haque M, Kohli D. et al. Endoscopic resection reduces morbidity when compared to surgery in veterans with large and complex colorectal polyps. Surg Endosc 2020; DOI: 10.1007/s00464–020–07482-y.
- 141 Gamaleldin M, Benlice C, Delaney CP. et al. Management of the colorectal polyp referred for resection: A case-matched comparison of advanced endoscopic surgery and laparoscopic colectomy. Surgery 2018; 163: 522-527
- 142 Nakamura F, Saito Y, Haruyama S. et al. Short-term prospective questionnaire study of early postoperative quality of life after colorectal endoscopic submucosal dissection. Dig Dis Sci 2017; 62: 3325-3335
- 143 Nam MJ, Sohn DK, Hong CW. et al. Cost comparison between endoscopic submucosal dissection and transanal endoscopic microsurgery for the treatment of rectal tumors. Ann Surg Treat Res 2015; 89: 202-207
- 144 Yamashita K, Oka S, Tanaka S. et al. Preceding endoscopic submucosal dissection for T1 colorectal carcinoma does not affect the prognosis of patients who underwent additional surgery: a large multicenter propensity score-matched analysis. J Gastroenterol 2019; 54: 897-906
- 145 Lowe D, Saleem S, Arif MO. et al. Role of endoscopic resection versus surgical resection in management of malignant colon polyps: A National Cancer Database analysis. J Gastrointest Surg 2020; 24: 177-187
- 146 Yeh JH, Tseng CH, Huang RY. et al. Long-term outcomes of primary endoscopic resection vs surgery for T1 colorectal cancer: A systematic review and meta-analysis. Clin Gastroenterol Hepatol 2020; 18: 2813-2823.e2815
- 147 Inoue T, Koyama F, Kuge H. et al. Short-term outcomes of endoscopic submucosal dissection versus laparoscopic surgery for colorectal neoplasms: An observational study. J Anus Rectum Colon 2018; 2: 97-102
- 148 Moon JY, Kim GH, Kim JH. et al. Clinicopathologic factors predicting lymph node metastasis in superficial esophageal squamous cell carcinoma. Scand J Gastroenterol 2014; 49: 589-594
- 149 Sgourakis G, Gockel I, Lang H. Endoscopic and surgical resection of T1a/T1b esophageal neoplasms: a systematic review. World J Gastroenterol 2013; 19: 1424-1437
- 150 Xu W, Liu XB, Li SB. et al. Prediction of lymph node metastasis in superficial esophageal squamous cell carcinoma in Asia: a systematic review and meta-analysis. Dis Esophagus 2020; DOI: 10.1093/dote/doaa032.
- 151 Ye B, Zhang X, Su Y. et al. The possibility of endoscopic treatment of cN0 submucosal esophageal cancer: results from a surgical cohort. Surg Endosc 2020; DOI: 10.1007/s00464–020–07420-y.
- 152 Zhang Y, Liu L, Wang Q. et al. Endoscopic submucosal dissection with additional radiotherapy in the treatment of T1a esophageal squamous cell cancer: randomized controlled trial. Endoscopy 2020; 52: 1066-1074
- 153 Hisano O, Nonoshita T, Hirata H. et al. Additional radiotherapy following endoscopic submucosal dissection for T1a-MM/T1b-SM esophageal squamous cell carcinoma improves locoregional control. Radiat Oncol 2018; 13: 14
- 154 Ikeda A, Hoshi N, Yoshizaki T. et al. Endoscopic submucosal dissection (ESD) with additional therapy for superficial esophageal cancer with submucosal invasion. Intern Med 2015; 54: 2803-2813
- 155 Kawaguchi G, Sasamoto R, Abe E. et al. The effectiveness of endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer. Radiat Oncol 2015; 10: 31
- 156 Suzuki G, Yamazaki H, Aibe N. et al. Endoscopic submucosal dissection followed by chemoradiotherapy for superficial esophageal cancer: Choice of new approach. Radiat Oncol 2018; 13: 246
- 157 Yoshimizu S, Yoshio T, Ishiyama A. et al. Long-term outcomes of combined endoscopic resection and chemoradiotherapy for esophageal squamous cell carcinoma with submucosal invasion. Dig Liver Dis 2018; 50: 833-838
- 158 Minashi K, Nihei K, Mizusawa J. et al. Efficacy of endoscopic resection and selective chemoradiotherapy for stage I esophageal squamous cell carcinoma. Gastroenterology 2019; 157: 382-390.e383
- 159 Kitagawa Y, Uno T, Oyama T. et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: part 1. Esophagus 2019; 16: 1-24
- 160 Koterazawa Y, Nakamura T, Oshikiri T. et al. A comparison of the clinical outcomes of esophagectomy and chemoradiotherapy after noncurative endoscopic submucosal dissection for esophageal squamous cell carcinoma. Surg Today 2018; 48: 783-789
- 161 Tsou YK, Lee CH, Le PH. et al. Adjuvant therapy for pT1a-m3/pT1b esophageal squamous cell carcinoma after endoscopic resection: Esophagectomy or chemoradiotherapy?. A critical review. Crit Rev Oncol Hematol 2020; 147: 102883
- 162 Hirasawa K, Kokawa A, Oka H. et al. Superficial adenocarcinoma of the esophagogastric junction: long-term results of endoscopic submucosal dissection. Gastrointest Endosc 2010; 72: 960-966
- 163 Yoshinaga S, Gotoda T, Kusano C. et al. Clinical impact of endoscopic submucosal dissection for superficial adenocarcinoma located at the esophagogastric junction. Gastrointest Endosc 2008; 67: 202-209
- 164 Alvarez Herrero L, Pouw RE, van Vilsteren FG. et al. Risk of lymph node metastasis associated with deeper invasion by early adenocarcinoma of the esophagus and cardia: study based on endoscopic resection specimens. Endoscopy 2010; 42: 1030-1036
- 165 Manner H, May A, Pech O. et al. Early Barrett’s carcinoma with "low-risk" submucosal invasion: long-term results of endoscopic resection with a curative intent. Am J Gastroenterol 2008; 103: 2589-2597
- 166 Manner H, Pech O, Heldmann Y. et al. Efficacy, safety, and long-term results of endoscopic treatment for early stage adenocarcinoma of the esophagus with low-risk sm1 invasion. Clin Gastroenterol Hepatol 2013; quiz e645 11: 630-635
- 167 Manner H, Pech O, Heldmann Y. et al. The frequency of lymph node metastasis in early-stage adenocarcinoma of the esophagus with incipient submucosal invasion (pT1b sm1) depending on histological risk patterns. Surg Endosc 2015; 29: 1888-1896
- 168 Manner H, Wetzka J, May A. et al. Early-stage adenocarcinoma of the esophagus with mid to deep submucosal invasion (pT1b sm2–3): the frequency of lymph-node metastasis depends on macroscopic and histological risk patterns. Dis Esophagus 2017; 30: 1-11
- 169 Benech N, O’Brien JM, Barret M. et al. Endoscopic resection of Barrett’s adenocarcinoma: Intramucosal and low-risk tumours are not associated with lymph node metastases. United European Gastroenterol J 2021; 9: 362-369
- 170 Larghi A, Lightdale CJ, Ross AS. et al. Long-term follow-up of complete Barrett’s eradication endoscopic mucosal resection (CBE-EMR) for the treatment of high grade dysplasia and intramucosal carcinoma. Endoscopy 2007; 39: 1086-1091
- 171 Fleischer DE, Overholt BF, Sharma VK. et al. Endoscopic radiofrequency ablation for Barrett’s esophagus: 5-year outcomes from a prospective multicenter trial. Endoscopy 2010; 42: 781-789
- 172 Peters FP, Kara MA, Rosmolen WD. et al. Endoscopic treatment of high-grade dysplasia and early stage cancer in Barrett’s esophagus. Gastrointest Endosc 2005; 61: 506-514
- 173 Sawas T, Alsawas M, Bazerbachi F. et al. Persistent intestinal metaplasia after endoscopic eradication therapy of neoplastic Barrett’s esophagus increases the risk of dysplasia recurrence: meta-analysis. Gastrointest Endosc 2019; 89: 913-925 e916
- 174 Gotoda T, Yanagisawa A, Sasako M. et al. Incidence of lymph node metastasis from early gastric cancer: estimation with a large number of cases at two large centers. Gastric Cancer 2000; 3: 219-225
- 175 Hirasawa T, Gotoda T, Miyata S. et al. Incidence of lymph node metastasis and the feasibility of endoscopic resection for undifferentiated-type early gastric cancer. Gastric Cancer 2009; 12: 148-152
- 176 Nakahara K, Tsuruta O, Tateishi H. et al. Extended indication criteria for endoscopic mucosal resection of early gastric cancer with special reference to lymph node metastasis--examination by multivariate analysis. Kurume Med J 2004; 51: 9-14
- 177 Abdelfatah MM, Barakat M, Othman MO. et al. The incidence of lymph node metastasis in submucosal early gastric cancer according to the expanded criteria: a systematic review. Surg Endosc 2019; 33: 26-32
- 178 Chu YN, Yu YN, Jing X. et al. Feasibility of endoscopic treatment and predictors of lymph node metastasis in early gastric cancer. World J Gastroenterol 2019; 25: 5344-5355
- 179 Lee SH, Choi CW, Kim SJ. et al. Risk factors for lymph node metastasis in mucosal gastric cancer and re-evaluation of endoscopic submucosal dissection. Ann Surg Treat Res 2016; 91: 118-126
- 180 Choi KK, Bae JM, Kim SM. et al. The risk of lymph node metastases in 3951 surgically resected mucosal gastric cancers: implications for endoscopic resection. Gastrointest Endosc 2016; 83: 896-901
- 181 Ma DW, Lee SJ, Kook MC. et al. The suggestion of revised criteria for endoscopic resection of differentiated-type submucosal gastric cancer. Ann Surg Oncol 2020; 27: 795-801
- 182 Choi JY, Park YS, Jung HY. et al. Identifying predictors of lymph node metastasis after endoscopic resection in patients with minute submucosal cancer of the stomach. Surg Endosc 2015; 29: 1476-1483
- 183 Kim TS, Min BH, Kim KM. et al. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: low curative resection rate but favorable long-term outcomes after curative resection. Gastric Cancer 2019; 22: 363-368
- 184 Lee HJ, Kim GH, Park DY. et al. Endoscopic submucosal dissection for papillary adenocarcinoma of the stomach: is it really safe?. Gastric Cancer 2017; 20: 978-986
- 185 Chen JN, Wang QW, Zhang QW. et al. Poorly differentiated is more significant than signet ring cell component for lymph node metastasis in mixed-type early gastric cancer: a retrospective study from a large-volume hospital. Surg Endosc 2020; DOI: 10.1007/s00464–020–07532–5.
- 186 Seo HS, Lee GE, Kang MG. et al. Mixed histology is a risk factor for lymph node metastasis in early gastric cancer. J Surg Res 2019; 236: 271-277
- 187 Lee IS, Lee S, Park YS. et al. Applicability of endoscopic submucosal dissection for undifferentiated early gastric cancer: Mixed histology of poorly differentiated adenocarcinoma and signet ring cell carcinoma is a worse predictive factor of nodal metastasis. Surg Oncol 2017; 26: 8-12
- 188 Lee JH, Choi IJ, Han HS. et al. Risk of lymph node metastasis in differentiated type mucosal early gastric cancer mixed with minor undifferentiated type histology. Ann Surg Oncol 2015; 22: 1813-1819
- 189 Takizawa K, Ono H, Yamamoto Y. et al. Incidence of lymph node metastasis in intramucosal gastric cancer measuring 30 mm or less, with ulceration; mixed, predominantly differentiated-type histology; and no lymphovascular invasion: a multicenter retrospective study. Gastric Cancer 2016; 19: 1144-1148
- 190 Takizawa K, Hatta W, Gotoda T. et al. Recurrence patterns and outcomes of salvage surgery in cases of non-curative endoscopic submucosal dissection without additional radical surgery for early gastric cancer. Digestion 2019; 99: 52-58
- 191 Yamada S, Hatta W, Shimosegawa T. et al. Different risk factors between early and late cancer recurrences in patients without additional surgery after noncurative endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc 2019; 89: 950-960
- 192 Libanio D, Pimentel-Nunes P, Afonso LP. et al. Long-term outcomes of gastric endoscopic submucosal dissection: Focus on metachronous and non-curative resection management. GE Port J Gastroenterol 2017; 24: 31-39
- 193 Hatta W, Gotoda T, Oyama T. et al. A scoring system to stratify curability after endoscopic submucosal dissection for early gastric cancer: "eCura system". Am J Gastroenterol 2017; 112: 874-881
- 194 Hatta W, Gotoda T, Oyama T. et al. Is the eCura system useful for selecting patients who require radical surgery after noncurative endoscopic submucosal dissection for early gastric cancer? A comparative study. Gastric Cancer 2018; 21: 481-489
- 195 Figueiredo PC, Pimentel-Nunes P, Libanio D. et al. A systematic review and meta-analysis on outcomes after Rx or R1 endoscopic resection of superficial gastric cancer. Eur J Gastroenterol Hepatol 2015; 27: 1249-1258
- 196 Jeon MY, Park JC, Hahn KY. et al. Long-term outcomes after noncurative endoscopic resection of early gastric cancer: the optimal time for additional endoscopic treatment. Gastrointest Endosc 2018; 87: 1003-1013.e1002
- 197 Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer 2020; DOI: 10.1007/s10120–020–01042-y.
- 198 Hirashita T, Ohta M, Tada K. et al. Prognostic factors of non-ampullary duodenal adenocarcinoma. Jpn J Clin Oncol 2018; 48: 743-747
- 199 Goda K, Kikuchi D, Yamamoto Y. et al. Endoscopic diagnosis of superficial non-ampullary duodenal epithelial tumors in Japan: Multicenter case series. Dig Endosc 2014; 26 (Suppl. 02) 23-29
- 200 Kuroki K, Sanomura Y, Oka S. et al. Clinical outcomes of endoscopic resection for superficial non-ampullary duodenal tumors. Endosc Int Open 2020; 8: E354-E359
- 201 Probst A, Freund S, Neuhaus L. et al. Complication risk despite preventive endoscopic measures in patients undergoing endoscopic mucosal resection of large duodenal adenomas. Endoscopy 2020; 52: 847-855
- 202 Choi JY, Jung SA, Shim KN. et al. Meta-analysis of predictive clinicopathologic factors for lymph node metastasis in patients with early colorectal carcinoma. J Korean Med Sci 2015; 30: 398-406
- 203 Bosch SL, Teerenstra S, de Wilt JH. et al. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 2013; 45: 827-834
- 204 Ronnow CF, Arthursson V, Toth E. et al. Lymphovascular infiltration, not depth of invasion, is the critical risk factor of metastases in early colorectal cancer: retrospective population-based cohort study on prospectively collected data, including validation. Ann Surg 2020; DOI: 10.1097/SLA.0000000000003854.
- 205 Kawachi H, Eishi Y, Ueno H. et al. A three-tier classification system based on the depth of submucosal invasion and budding/sprouting can improve the treatment strategy for T1 colorectal cancer: a retrospective multicenter study. Mod Pathol 2015; 28: 872-879
- 206 Han J, Hur H, Min BS. et al. Predictive factors for lymph node metastasis in submucosal invasive colorectal carcinoma: a new proposal of depth of invasion for radical surgery. World J Surg 2018; 42: 2635-2641
- 207 Ebbehoj AL, Jorgensen LN, Krarup PM. et al. Histopathological risk factors for lymph node metastases in T1 colorectal cancer: meta-analysis. Br J Surg 2021; DOI: 10.1093/bjs/znab168.
- 208 Cubiella J, Gonzalez A, Almazan R. et al. pT1 Colorectal cancer detected in a colorectal cancer mass screening program: treatment and factors associated with residual and extraluminal disease. Cancers (Basel) 2020; 12 DOI: 10.3390/cancers12092530.
- 209 Boenicke L, Fein M, Sailer M. et al. The concurrence of histologically positive resection margins and sessile morphology is an important risk factor for lymph node metastasis after complete endoscopic removal of malignant colorectal polyps. Int J Colorectal Dis 2010; 25: 433-438
- 210 Kim JY, Han SJ, Jung Y. et al. The relationship between local recurrence and positive lateral margin after en bloc resection of colorectal neoplasm. Scand J Gastroenterol 2018; 53: 1541-1546
- 211 Makazu M, Sakamoto T, So E. et al. Relationship between indeterminate or positive lateral margin and local recurrence after endoscopic resection of colorectal polyps. Endosc Int Open 2015; 3: E252-257
- 212 Yamada M, Saito Y, Takamaru H. et al. Long-term clinical outcomes of endoscopic submucosal dissection for colorectal neoplasms in 423 cases: a retrospective study. Endoscopy 2017; 49: 233-242
- 213 Backes Y, de Vos Tot Nederveen Cappel WH, van Bergeijk J. et al. Risk for incomplete resection after macroscopic radical endoscopic resection of T1 colorectal cancer: A multicenter cohort study. Am J Gastroenterol 2017; 112: 785-796
- 214 Chen K, Cao G, Chen B. et al. Laparoscopic versus open surgery for rectal cancer: A meta-analysis of classic randomized controlled trials and high-quality nonrandomized Studies in the last 5 years. Int J Surg 2017; 39: 1-10
- 215 Wu Q, Wei M, Ye Z. et al. Laparoscopic colectomy versus open colectomy for treatment of transverse colon cancer: A systematic review and meta-analysis. J Laparoendosc Adv Surg Tech A 2017; 27: 1038-1050
- 216 Jeong JU, Nam TK, Kim HR. et al. Adjuvant chemoradiotherapy instead of revision radical resection after local excision for high-risk early rectal cancer. Radiat Oncol 2016; 11: 114
- 217 Sasaki T, Ito Y, Ohue M. et al. Postoperative chemoradiotherapy after local resection for high-risk T1 to T2 low rectal cancer: Results of a single-arm, multi-institutional, phase II clinical trial. Dis Colon Rectum 2017; 60: 914-921
- 218 Barbeiro S, Libanio D, Castro R. et al. Narrow-band imaging: Clinical application in gastrointestinal endoscopy. GE Port J Gastroenterol 2018; 26: 40-53
- 219 Kim GH, Min YW, Lee H. et al. Risk factors of metachronous recurrence after endoscopic submucosal dissection for superficial esophageal squamous cell carcinoma. PLoS One 2020; 15: e0238113
- 220 Sawada G, Niida A, Uchi R. et al. Genomic landscape of esophageal squamous cell carcinoma in a Japanese population. Gastroenterology 2016; 150: 1171-1182
- 221 Uno K, Koike T, Kusaka G. et al. Risk of metachronous recurrence after endoscopic submucosal dissection of esophageal squamous cell carcinoma. Dis Esophagus 2017; 30: 1-8
- 222 Urabe Y, Kagemoto K, Nakamura K. et al. Construction of a risk model for the development of metachronous squamous cell carcinoma after endoscopic resection of esopahageal squamous cell carcinoma. Esophagus 2019; 16: 141-146
- 223 Fukuda H, Ishihara R, Shimamoto Y. et al. Effect of horizontal margin status and risk of local recurrence after endoscopic submucosal dissection for superficial esophageal cancer. JGH Open 2020; 4: 160-165
- 224 Cotton CC, Haidry R, Thrift AP. et al. Development of evidence-based surveillance intervals after radiofrequency ablation of Barrett’s esophagus. Gastroenterology 2018; 155: 316-326.e316
- 225 Brito-Goncalves G, Libanio D, Marcos P. et al. Clinicopathologic characteristics of patients with gastric superficial neoplasia and risk factors for multiple lesions after endoscopic submucosal dissection in a Western country. GE Port J Gastroenterol 2020; 27: 76-89
- 226 Okada K, Suzuki S, Naito S. et al. Incidence of metachronous gastric cancer in patients whose primary gastric neoplasms were discovered after Helicobacter pylori eradication. Gastrointest Endosc 2019; 89: 1152-1159.e1151
- 227 Park WY, Lee SJ, Kim YK. et al. Occurrence of metachronous or synchronous lesions after endoscopic treatment of gastric epithelia dysplasia- impact of histologic features of background mucosa. Pathol Res Pract 2018; 214: 95-99
- 228 Yang HJ, Kim SG, Lim JH. et al. Novel risk stratification for metachronous recurrence after curative endoscopic submucosal dissection for early gastric cancer. Gastrointest Endosc 2018; 87: 419-428.e413
- 229 Yang HJ, Kim SG, Lim JH. et al. Surveillance strategy according to age after endoscopic resection of early gastric cancer. Surg Endosc 2018; 32: 846-854
- 230 Moon HS, Yun GY, Kim JS. et al. Risk factors for metachronous gastric carcinoma development after endoscopic resection of gastric dysplasia: Retrospective, single-center study. World J Gastroenterol 2017; 23: 4407-4415
- 231 Abe S, Oda I, Suzuki H. et al. Long-term surveillance and treatment outcomes of metachronous gastric cancer occurring after curative endoscopic submucosal dissection. Endoscopy 2015; 47: 1113-1118
- 232 Pimentel-Nunes P, Libanio D, Marcos-Pinto R. et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019; 51: 365-388
- 233 Hahn KY, Park JC, Kim EH. et al. Incidence and impact of scheduled endoscopic surveillance on recurrence after curative endoscopic resection for early gastric cancer. Gastrointest Endosc 2016; 84: 628-638.e621
- 234 Oka S, Tanaka S, Saito Y. et al. Local recurrence after endoscopic resection for large colorectal neoplasia: a multicenter prospective study in Japan. Am J Gastroenterol 2015; 110: 697-707
- 235 Yoshii S, Nojima M, Nosho K. et al. Factors associated with risk for colorectal cancer recurrence after endoscopic resection of T1 tumors. Clin Gastroenterol Hepatol 2014; 12: 292-302.e293
- 236 Green RJ, Metlay JP, Propert K. et al. Surveillance for second primary colorectal cancer after adjuvant chemotherapy: an analysis of Intergroup 0089. Ann Intern Med 2002; 136: 261-269
- 237 Hassan C, Pickhardt PJ, Zullo A. et al. Cost-effectiveness of early colonoscopy surveillance after cancer resection. Dig Liver Dis 2009; 41: 881-885
- 238 Hassan C, Antonelli G, Dumonceau JM. et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2020. Endoscopy 2020; 52: 687-700
- 239 Benson AB, Venook AP, Al-Hawary MM. et al. NCCN guidelines insights: Colon Cancer, version 2, 2018. J Natl Compr Canc Netw 2018; 16: 359-369
- 240 Shaukat A, Kaltenbach T, Dominitz JA. et al. Endoscopic recognition and management strategies for malignant colorectal polyps: Recommendations of the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 2020; 115: 1751-1767
- 241 Butte JM, Tang P, Gonen M. et al. Rate of residual disease after complete endoscopic resection of malignant colonic polyp. Dis Colon Rectum 2012; 55: 122-127
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