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short review memo (2019) 12:36–41 https://doi.org/10.1007/s12254-018-0461-6 Therapeutic endoscopic strategies in early esophageal cancer and dysplastic Barrett’s epithelium Teresa Fritz · Rainer Schöfl · Friedrich Wewalka · Alexander Ziachehabi Received: 31 July 2018 / Accepted: 7 November 2018 / Published online: 5 December 2018 © The Author(s) 2018 Summary Endoscopic therapy is the gold standard Introduction for curative treatment of early esophageal adenocarci- noma (EAC) including dysplastic Barrett´s epithelium Since esophageal tumor surgery is associated with (BE) and very early squamous cell carcinoma (SCC) a high adverse events rate [1], endoscopic local tu- because it is superior to surgery in regard to mor- mor therapy as a minimally invasive therapy option bidity, mortality and cost effectiveness while yielding has continuously attracted increasing attention dur- excellent results and low complication rates. ing the past decade. Today, endoscopic therapy is Tumor detection at an early stage is often challeng- recognized as the therapy of choice for very early ing and a multimodal approach using high resolu- squamous cell carcinoma (SCC) and early esophageal tion white light endoscopy, virtual chromoendoscopy adenocarcinoma (EAC) by gastroenterology societies (e.g. narrow band imaging, NBI) and endoscopic ul- but it is restricted to expert centers because of high trasonography (EUS) is recommended. Importantly, technical skill demands. histological diagnosis and EUS guided tumor staging Endoscopic tumor therapy originates from piece- should be performed before endoscopic tumor resec- meal endoscopic mucosal resection (EMR) and devel- tion, although EUS validity has its limitations in terms oped to endoscopic submucosal dissection (ESD). of superficial mucosal and submucosal tumor inva- Injection-assisted EMR was introduced for flexible sion. colonoscopy in 1973 and allows for the removal of sus- In early esophageal adenocarcinoma, endoscopic mu- picious mucosal lesions—smaller ones in one piece, cosal resection (EMR) is considered the first line ther- bigger ones in multiple pieces—throughout the gas- apy and endoscopic submucosal dissection (ESD) is trointestinal tract [2]. The problem hereby is—due recommended only in special cases. In contrast, in to the multiple pieces—the limitation of histological very early squamous cell carcinoma, ESD is superior staging and a higher potential for recurrence of neo- to EMR. This is mainly caused by a lower risk for lym- plastic lesions since en bloc EMR is practicable only phatic metastases in adenocarcinoma compared to for lesions of ≤15–20 mm in diameter. squamous cell carinoma. If endoscopic resection is ESD was developed in Japan and is a technique that not curative or not feasible,surgery is the treatment allows for en bloc resection of visible mucosal and su- of choice - assuming the patient´s comorbidities and perficial submucosal lesions irrespective of their size performance status are no exclusion criteria. [3, 4]. Originally, it was used to dissect neoplastic lesions in the stomach, but since this procedure was Keywords ESD · EMR · EUS · Esophageal cancer so successful regarding effectiveness and safety, it was finally extended for use in the esophagus and colorec- tum. Compared with EMR, ESD is more time consuming and associated with higher complication rates [5, 6], but en bloc resection of large lesions infiltrating the T. Fritz ()·R. Schöfl ·F. Wewalka ·A.Ziachehabi superficial submucosal layer is feasible and it facili- 4. Interne Abteilung, Ordensklinikum Linz/Elisabethinen, tates appropriate histological evaluation. Moreover, Fadingerstraße 1, 4020 Linz, Austria teresa.fritz@ordensklinikum.at 36 Therapeutic endoscopic strategies in early esophageal cancer and dysplastic Barrett’s epithelium K short review ESD is superior to surgery in terms of morbidity, mor- inflamed tissue as well as between intramucosal and tality [7], and cost efficacy [8]. submucosal tumor invasion [15, 16]. The evaluation of a suspicious lesion using IPCL classification is therefore an indispensable tool in Staging making a decision on which therapeutic strategy Before endoscopic tumor therapy is initiated, the should be followed in early esophageal squamous cell neoplasia should be histologically verified. Endo- carcinoma. scopic ultrasound (EUS)-guided tumor staging plays In Barrett’s epithelium with dysplastic or tumor- a leading role to exclude deep tumor infiltration of suspicious visible lesions, endoscopists should also the esophageal wall, but is limited in distinguishing perform magnifying NBI-guided endoscopy to eval- superficial from deep submucosal tumor infiltration, uate the mucosal microsurface and microvascular pit implying a relevant risk for EUS-guided tumor under- pattern. or overstaging [9]. In general, non-dysplastic Barrett’s mucosa presents In a meta-analysis of 49 studies (n = 2558), the with a regular surface pit pattern including rounded, pooled sensitivity and specificity of EUS for detec- circular, or oval crypts. If an irregular or disrupted tion of T1 tumors (81.6% and 99.4%, respectively) mucosal pit pattern occurs, dysplasia or invasive can- and for T2 tumors (81.4% and 96.3%, respectively) cer must be suspected [17]. revealed the inferiority of EUS in early tumor stages Additionally, the microvascular pattern must be compared with more advanced tumor stages, since evaluated since abnormal blood vessels (irregular, T3 and T4 tumors were revealed to have the highest dilated, corkscrew type vessels) are a further sign of pooled sensitivity and specificity rates (91.4% and the presence of dysplasia or cancer. To date, there are 94.4% for T3 and 92.4% and 97.4% for T4 tumors, re- several classifications for pathologic microvascular spectively). Moreover, it could be demonstrated that and microsurface patterns available [18, 19], but to the use of fine needle aspiration (FNA) could improve date, there is no consensus on how to clearly distin- lymph node staging (sensitivity 84.7% vs. 96.7% and guish mucosal from submucosal tumor infiltration in specificity 84.6% vs. 95.5%, respectively; [10]). Barrett’s adenocarcinoma. On the other hand, Thomas et al. and others [11, This underlines the importance of the EMR proce- 12] showed that flat, non-nodular lesions in Barrett’s dure as a powerful staging mechanism, and sceptics of epithelium were limited exclusively to the mucosal EUS argue that early Barrett’s neoplasia can be staged layer, so that EUS had no benefit and should be re- accurately by histological assessment of EMR speci- considered in this special selected cohort [9]. mens [20] and that surgery can be added if no vertical Therefore, it is crucial for endoscopists to learn R0 resection is achieved. how to distinguish lesions infiltrating the superficial submucosa from intraepithelial tumors macroscopi- Endoscopic strategies for dysplastic Barrett’s ep- cally. This is done by a combination of high-resolution ithelium and EAC white light endoscopy and virtual chromoendoscopy with magnification (e.g., NBI). In the West, the incidence of esophageal adenocar- Submucosal invasion is often associated with cinoma (EAC) has dramatically increased during the significant morphological changes as these lesions past decades [21]. Adenocarcinoma arises from meta- mainly appear elevated and/or excavated with a de- plastic Barrett’s epithelium in the distal esophagus struction of their mucosal structure (e.g., ulcerations) and is mainly a result of gastroesophageal reflux dis- [13]. By contrast, intramucosal tumors generally ap- ease (GERD). pear flat without a significant effect on the mucosal Over time, Barrett’s epithelium can transform via surface. Importantly, these macroscopic criteria alone low-grade dysplastic mucosa and high-grade dyspla- are insufficient to distinguish between mucosal and sia to invasive cancer, but the estimated risk of can- submucosal invasion. Additionally, magnification cer progression from nondysplastic Barrett’s epithe- endoscopy together with virtual chromoendoscopy lium is low (0.3% per year) [22]. Therefore, screening (e.g., NBI, narrow-band imaging) should therefore be endoscopy only in patients with longstanding GERD performed. and other risk factors (age ≥50 years, obesity, smok- Narrow-band imaging yields a high contrast image ing, male sex, fist-degree relative with Barrett’s epithe- for the evaluation of squamous cell tissue for irregular lium/adenocarcinoma) is recommended. Screening intrapapillary capillary loops (IPCLs) [14]. should be repeated every 3–5 years if Barrett’s meta- Intrapapillary capillary loops are microvessels in plasia is diagnosed to detect potential malignant ep- the squamous cell mucosa and they are an indicator ithelial transformation at an early tumor stage [23]. of tissue atypia if special vessel patterns occur (dilata- Unfortunately, however, only 5–7% of patients with tion, meandering, caliber change, and non-uniformity EAC have a prior diagnosis of Barrett’s epithelium [24], in the appearance of each IPCL). These vessel patterns which highlights the limitations of this screening pro- mark a destruction of the IPCL structure and help gram, since a large proportion of patients with Barrett to distinguish between tumorous and non-tumorous/ K Therapeutic endoscopic strategies in early esophageal cancer and dysplastic Barrett’s epithelium 37 short review mucosa are asymptomatic and therefore remain un- a multimodal approach is the standard therapy regi- detected [25]. men for dysplastic and neoplastic BE in the West in When a visible lesion suggestive of dysplasia or order to prevent metachronous neoplasia [33]. In the early invasive cancer is detected in Barrett’s epithe- East, however, suspicious mucosal lesions are endo- lium, it should be endoscopically removed by EMR if scopically removed, often without removing residual deep tumor invasion or lymphatic metastasis was ex- BE. In general, endoscopic resection is the only feasi- cluded by EUS. Here, ESD is recommended only for ble therapy option in many Asian countries including special indications (see below) [26]. Japan. The diagnosis of any grade of dysplasia in random Radiofrequency ablation involves the direct appli- biopsies from Barrett’s epithelium should be con- cation of heat to Barrett’s mucosa, whether by using firmed by an expert gastrointestinal (GI) pathologist a special balloon device for circumferential treatment and it is important to rule out macroscopic signs of (360° ablation), or by a probe attached to the scope or inflammation in the Barrett’s mucosa before biopsies a through-the-scope probe for focal treatment. are taken. Since histological assessment after RFA treatment When high-grade intraepithelial neoplasia (HGIN) is invalid, all visible lesions must be resected be- is diagnosed and confirmed by the GI expert, radiofre- fore RFA application. Several studies demonstrated quency ablation (RFA) is recommended [23]. a benefit from RFA treatment vs. surveillance of Bar- Histologic confirmation by an expert is especially rett’s epithelium with low-grade dysplasia, resulting in crucial for patients with random low-grade intraep- a significant decrease of disease progression to high- ithelial neoplasia (LGIN), because it was demon- grade dysplasia/invasive adenocarcinoma [34–36]. strated that the majority (73%) of community-di- Long-term follow-up revealed excellent results when agnosed low-grade dysplasia was downstaged by Barrett’s epithelium was completely eradicated: After experts. On the other hand, patients with expert- 3 years, 91% of patients presented without Barrett’s confirmed low-grade dysplasia had a relevant risk for mucosa and 98% of patients presented without dys- malignant disease progression (9.1% per patient year) plasia, while strictures occurred in 7.3% [37]. [27]. Radiofrequency ablation in low-grade intraepithe- Endoscopic submucosal dissection vs. endoscopic lial neoplasia is only recommended if it is confirmed mucosal resection in EAC twice within 6 months under ongoing proton pump inhibitor therapy [23]. Radiofrequency ablation ses- Endoscopic submucosal dissection is performed with sions should be performed until Barrett’s epithelium special “knives” through the channel of the endo- is completely eradicated. scope, developed by Japanese experts. After applying heat as marking dots around the neoplastic area, saline injection to the submucosa followed by a sub- Endoscopic mucosal resection in early EAC mucosal cut allows for en bloc dissection of the To date, EMR is the gold standard for removing visible desired area within the submucosal layer. lesions in Barrett’s mucosa and it is considered cu- Notably, ESD in early adenocarcinoma is limited to rative when the vertical resection margins are tumor special indications. This is primarily based on the free, when the tumor is well differentiated, and lym- finding that predictable piecemeal mucosectomy is phovascular/vascular tumor infiltration can be his- a high-risk factor for neoplastic recurrence rates (rel- tologically excluded [26]. It is usually performed as ative risk: 2.44 [95% CI: 1.13–4.89], p = 0.02; [38]). a cap-assisted (cEMR) procedure—this involves sub- Therefore, ESD should be considered for tumors of mucosal saline injection, sucking of the lifted lesion ≥15 mm in diameter. Moreover, ESD is recommended into the cap, and dissection by a cap-placed snare when poor tumor lifting is expected (e.g., if the area [28]. Alternatively, multiband mucosectomy (MBM) to be dissected contains fibrotic tissue). Finally, if su- can be performed, using a multiband ligator system perficial submucosal tumor invasion is assumed via to fix the neoplastic mucosal area by deploying a rub- white light and virtual chromoendoscopy (e.g., ele- ber bandaroundit and finally removing it underneath vated, depressed, or ulcerated lesions together with the rubber band by snare [29]. Both EMR techniques a pathologic microvessel pattern; [13]) and deep tu- show similar resection depths [30], specimen diam- mor infiltration or lymphatic metastasis is excluded eters, and complication rates [31], while MBM was by EUS, ESD is preferred to EMR. This is because it shown to be faster and less expensive [32]. provides a minimally invasive, curative treatment [26] if the following four criteria are met: (1) submucosal layer invasion is ≤500μm, (2) poor tumor differentia- The role of radiofrequency ablation tion is excluded, (3) lymphatic/venous vessel infiltra- There is a critical difference in the treatment of dys- tion is missing, and (4) tumor size ≤30 mm. Notably, plastic/neoplastic Barrett’s epithelium between East- the risk of lymph node metastasis for Barrett’s ade- ern and Western countries, since RFA is not available nocarcinoma is significantly increased with the depth in the East. The combination of EMR/ESD and RFA as 38 Therapeutic endoscopic strategies in early esophageal cancer and dysplastic Barrett’s epithelium K short review of tumor infiltration (0% in HGIN/mucosal infiltration filtrated, while deeper invasion bears a lymph node vs. 12% in submucosal infiltration, p = 0.045) [39]. risk of up to 11–53% for sm1 and 30–54% for sm2 tu- Nevertheless, the absence of the aforementioned mors [48–50]. This explains why ESD is considered criteria is associated with a low lymphatic metastasis curative only for intraepithelial (m1) and lamina pro- potential and therefore ESD can be considered cu- pria infiltrating (m2) tumors since there is low lym- rative even if the superficial submucosal layer (sm1 phometastatic potential. Submucosal tumor invasion ≤500μm) is involved [40–42]. in squamous cell carcinoma ≤200μm(sm1) canbe One randomized controlled study in 2017 focused tolerated if poor tumor differentiation, lymphatic or on the differences in outcome and adverse events of venous vessel invasion, and tumor infiltration of the EMR compared with ESD: Terheggen et al. demon- vertical dissection margins can be excluded. Other- strated no difference in complete remission from neo- wise, patients must be evaluated for tumor surgery. plasia at the 3-month follow-up (ESD 93.8% vs. EMR 94.1%, p = 1.0) while ESD was associated with a higher Safety and management of complications in en- rate of adverse events [43]. doscopic tumor resection in the esophagus Notably, ESD yields higher en bloc resection rates (OR: 13.9, 95% CI: 10.12–18.99; p = 0.001) and higher Compared with esophageal resection, EMR and ESD curative resection rates (OR: 3.53, 95% CI: 2.57–4.84; both are considered a safe procedure associated with p = 0.000) compared with EMR throughout the GI low complication rates. The most frequently occur- tract but is more time consuming and associated with ring complications are bleeding, perforations, and higher rates of adverse events [44]. However, this esophageal strictures. Usually, bleeding and small advantage does not seem to have any clinical impact perforations can be successfully treated endoscopi- on the need for elective surgery or the rates of com- cally. plete remission from neoplasia [43]. This explains A meta-analysis of 11 studies, where 501 ESDs of why EMR in combination with RFA is the preferred early esophageal adenocarcinoma between 2005 and technique to remove early EAC endoscopically. 2016 were analyzed, revealed a pooled perforation rate However, both in EMR and ESD, additional surgery of 1.5% (0.4–3%), a pooled bleeding rate of 1.7% (95% is recommended—depending on the patient’s comor- CI: 0.6–3.4%), and the pooled risk of stricture devel- bidities and performance status—when the vertical opment was 11.6% (95% CI: 0.9–29.6%) while the in- specimen margins are infiltrated by tumor. cidence of neoplastic recurrence after curative resec- tion was 0.17% (95% CI: 0–0.3%) at a mean follow-up of 22.9 months (95% CI: 17.5–28.3) [51]. Endoscopic strategies for very early esophageal Strictures often represent a long-term issue with squamous cell carcinoma recurrent need for balloon dilatation treatment. Stric- Detection of squamous cell carcinoma in the esoph- ture development depends primarily on the resection agus at a very early stage is challenging since these size. A resection size including more than 75% of lesions often appear subtle and are usually flat. The esophageal circumference accompanied by a tumor highest tumor detection rates can be achieved using infiltration deeper than the lamina propria layer (>m2) the combination of high-resolution white light en- is significantly associated with stricture development doscopy and virtual chromoendoscopy with NBI. With [52]. Currently, systemic steroid therapy and local regard to the detection rate of high-grade dysplasia steroid injections as stricture prophylaxis after ESD and squamous cell carcinoma, NBI is equal to Lu- in patients with relevant tumor resection size are gol staining, but NBI has a higher specificity (82% vs. under debate in multiple studies. To date, no guide- 37%), while sensitivity is similar [45]. Additionally, In- line-based recommendation for steroid therapy has oue et al. demonstrated that the microvascular pat- been published. Nevertheless, some studies pointed tern of the IPCL can be used to predict the degree of out that postinterventional systemic steroid treat- malignancy and invasiveness of a lesion [46]. ment beneficially influences stricture development, suggesting that this could at least be an attempt of treatment [53–55]. ESD in early squamous cell carcinoma Recently, another study revealed that 25% of pa- In contrast to EMR, ESD is the gold standard for re- tients who underwent ESD with circumferential re- moving very early esophageal squamous cell carci- section rates of >75% showed esophageal dysmotil- noma. ity in high-resolution manometry studies and 69% of The superiority of ESD to EMR in this tumor en- these patients also presented with clinically verifiable tity is based on higher en bloc resection rates [44], dysmotility symptoms although no stricture could be higher R0 resection rates (97.4% vs. 78.3%, p = 0.0002), detected endoscopically [56]. Therefore, dysmotility and lower tumor recurrence rates (0.9% vs. 9.8%, must also be considered as a potential adverse event p = 0.0065; [47]). 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K Therapeutic endoscopic strategies in early esophageal cancer and dysplastic Barrett’s epithelium 41
memo - Magazine of European Medical Oncology – Springer Journals
Published: Dec 5, 2018
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