Barrett s ALIMENTARY TRACT. Subsquamous Extension of Intestinal Metaplasia Is Detected in 98% of Cases of Neoplastic Barrett s Esophagus

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1 Clinical Gastroenterology and Hepatology 2014;12: ALIMENTARY TRACT Subsquamous Extension of Intestinal Metaplasia Is Detected in 98% of Cases of Neoplastic Barrett s Esophagus Mario Anders,* Yasmin Lucks,* Muhammad Abbas El Masry, Alexander Quaas,* Thomas Rösch,* Guido Schachschal,* Christina Bähr,* Ulrich Gauger,* Guido Sauter,* Jakob R. Izbicki,* and Andreas H. Marx* *Departments of Interdisciplinary Endoscopy, Pathology, and General and Abdominal Surgery, University Hospital Hamburg- Eppendorf, Hamburg, Germany; and Division of Gastroenterology, Internal Medicine Department, Assiut University Hospital, Assiut, Egypt BACKGROUND & AIMS: METHODS: Subsquamous intestinal metaplasia (SSIM) has been observed after endotherapy in patients with neoplastic Barrett s esophagus (BE). However, it is not clear whether SSIM occurs in untreated patients. Incompletely eradicated SSIM could provide a source of recurrent disease. We assessed its prevalence in a large cohort of patients who had not received endoscopic therapy. Two experienced pathologists analyzed 138 samples of 506 resection specimens found to contain squamous epithelium from 110 patients with neoplastic BE treated by widespread endoscopic mucosal resection (92 men; mean age, 66 years). The maximum extent of SSIM was measured. RESULTS: Of the 138 samples analyzed, 124 (89.9%) were found to contain SSIM from 108 of the 110 patients (98.2%). The mean length of SSIM was 3.3 mm (range, mm; 25% 5 mm); SSIM length correlated with BE length (P <.05). In 83 of 138 samples (60.1%), the SSIM consisted partially or entirely of neoplasias of different grades, with a mean subsquamous extension of 3.3 mm; the extension correlated with grade of neoplasia (P [.0001). CONCLUSIONS: Most patients with BE with neoplasia (of all grades) have subsquamous extension of intestinal metaplasia, including subsquamous extension of lesions at the squamocolumnar junction. Therefore, biopsy and resection of neoplastic BE should extend at least 1 cm into the squamous epithelium. Keywords: EMR; Esophagus; Cancer; Treatment; Surgery. See editorial on page 411. Watch this article s video abstract and others at Scan the quick response (QR) code to the left with your mobile device to watch this article s video abstract and others. Don t have a QR code reader? Get one by searching QR Scanner in your mobile device s app store. Barrett s esophagus (BE), defined as intestinal metaplasia of the distal esophagus, is a premalignant condition for esophageal adenocarcinoma, a cancer with rising incidence rate during the past decades. 1 Once premalignant or early malignant lesions are recognized during surveillance endoscopy, endoscopic management has been established by using endoscopic mucosal resection (EMR) and further refined by radiofrequency ablation (RFA). Both methods are nowadays used complementary to achieve complete ablation of the entire Barrett epithelium and not only neoplastic areas When planning the extent of resection or ablation, it is noteworthy that Barrett intestinal metaplasia may reach beyond the squamocolumnar junction zone underneath the squamous epithelium (SQE). It may therefore not be visible and hence escape endoscopic therapy of Barrett neoplasia if not intentionally included in the area to be resected or ablated. The rate of such subsquamous intestinal metaplasia (SSIM) before endotherapy, however, Abbreviations used in this paper: BE, Barrett s esophagus; EMR, endoscopic mucosal resection; PPI, proton pump inhibitor; RFA, radiofrequency ablation; SQE, squamous epithelium; SSIM, subsquamous intestinal metaplasia by the AGA Institute /$

2 406 Anders et al Clinical Gastroenterology and Hepatology Vol. 12, No. 3 Table 1. Clinical, Endoscopic, and Histologic Data of Included Patients (n ¼ 110) No. of patients 110 (92 male, 18 female) Mean age, y (range) 66 (43 89) Mean no. of EMR specimens per patient 5 (range, 1 28) EMR specimens with SQE 138 Endoscopic length of BE Mean/range (cm) 4.2 ( ) Short BE ( 3 cm) 48 Long BE (>3 cm) 62 Most severe histopathologic diagnosis per patient T1 carcinoma 66 T1a (mucosal) 54 (53 G1, 2 G2) T1b (submucosal) 12 sm 1 9 (6 G1, 2 G2, 1 G3) sm 2 3 (all G2) HGIN 15 LGIN 3 Non-neoplastic BE 26 a G, grading; HGIN, high-grade intraepithelial neoplasia; LGIN, low-grade intraepithelial neoplasia. a Positive biopsy for neoplasia from the referring physician/institution (mostly HGIN), but resection specimens were all negative in these patients. remains unclear. A previous smaller study that used EMR samples suggested that SSIM occurred in up to 28% of cases. 11 To further elucidate the frequency of SSIM before endotherapy, we analyzed a large collective that had undergone widespread EMR for neoplastic BE. Methods Resection specimens gained by widespread EMR from 110 patients (92 men, 18 women; mean age, 66 years) between 2004 and 2010 were included in this retrospective study. Indication for endoscopic resection was BE with suspected or confirmed dysplasia or presumed mucosal carcinoma. Widespread EMR aimed at complete ablation of all BE tissue together with the neoplastic area(s) and in some cases additional thermal methods were done after EMR sessions (details not reported here). Histopathologic slides were either unavailable (first EMR done elsewhere) or incomplete from an additional 30 resections, which could therefore not be analyzed. Because of primary reasons (unclear new Z line after first EMR), only specimens from the first session were analyzed from each patient; it had been at the discretion of the endoscopist to choose one or two/three sessions for complete BE resection, mostly depending on BE extent/length. All specimens were analyzed by 2 experienced pathologists (A.M., A.Q.) with a special interest in BE. Orientation of the resected specimens pinned on cork was done in the endoscopy suite before the histopathologic work-up, with SQE oriented orally (at 12 o clock) to assess SSIM in a comparable fashion in all EMR samples. Subsequently, SSIM was measured in all specimens containing SQE in relation to a theoretical straight Figure 1. Flow sheet showing the course of patients treated for neoplastic BE. orally-aborally orientated line (12 to 6 o clock). EMR specimens were fixed in buffered 4% formalin, cut according to an oral-aboral orientation in 1-mm-thick slices, and embedded in paraffin. Large tissue sections (thickness, 4 mm) were made from all tissue blocks and hematoxylin-eosin stained to measure the subsquamous extensions of the lesions. Endoscopic and other histopathologic data of all patients were analyzed such as Barrett length (the Prague classification was not uniformly used in endoscopy reports), number, size, and location of focal lesions, and histopathologic grading and staging of malignancy. Statistical Analysis Contingency tables and c 2 analyses were used to analyze associations between SSIM results and categorical parameters with the aid of the JMP software package (SAS Institute Inc, Cary, NC; Version 5.0.1a).

3 March 2014 Subsquamous Extension of Barrett s Esophagus 407 Table 2. Data on Non-neoplastic and Neoplastic SSIM General data on patients, specimens, and rate of SSIM Total no. of patients who had SQE in any EMR 110 specimen Total no. of EMR specimens 506 Specimens with SQE 138 Patients with SSIM in any specimen 108/110 (98.2%) EMR specimens with SSIM 124/138 (89.9%) Maximum length of SSIM in all patients with SSIM (n ¼ 108) Mean (mm) 3.3 (range, ) <5 mm 81/108 (75%) 5 mm 27/108 (25%) Maximum length of SSIM in patients with neoplasia a (n ¼ 83) Mean (mm) 3.3 (range, ) <5 mm 12/83 (14.4%) 5 mm 71/83 (85.6%) Maximum length of SSIM in patients without neoplasia (n ¼ 25) Mean (mm) 3.3 (range, ) <5 mm 19/25 (76%) 5 mm 6/25 (24%) NOTE. For patient numbers in subgroups, see also Figure 1. a Neoplastic SSIM was regularly surrounded by non-neoplastic SSIM, so both are counted here. Results Data of all 110 patients included in this study are shown in Table 1 and Figure 1. Mean age was 66 years; the male:female ratio was 5.11:1. The most severe histologic diagnoses on a per-patient basis included early (T1) cancer in 66, high-grade intraepithelial neoplasia in 15, and low-grade epithelial neoplasia in 3 cases. Barrett length significantly correlated with increasing neoplasia grade, ranging from no neoplasia to T1b cancer (P <.0001). In 26 cases with positive biopsies at other institutions, no neoplasia was found in the resection specimens during widespread EMR at our institution. A total of 506 EMR specimens of 110 patients were available for histopathologic work-up, with 138 of the 506 specimens containing SQE (27.3%, Table 2). SSIM was found in 124 of these 138 cases (89.9%). Details of SSIM pattern, histology, and length are also shown in Table 2. The length of SSIM correlated significantly with the length of BE (P ¼.0036) (Figure 2). Furthermore, cases were analyzed for the pattern of SSIM extension by comparing different slices from one specimen in several patients; inhomogeneous extension in serial sections of the same patient was found in almost all cases, as suggested by Figure 3. SSIM contained all histologic stages ranging from non-neoplastic BE to cancer, as shown in Table 2. Histologic examples are shown in Figure 4. Discussion Our study shows an almost regular occurrence of SSIM in patients with (neoplastic) BE. Because our Figure 2. Scatter plot showing distribution and frequency of SSIM. Subsquamous Barrett s epithelium was seen in 108 patients, ranging from 0.2 mm (minimum) to 9.6 mm (maximum); mean 3.3. analysis has been designed solely to address the question of subsquamous extension of Barrett epithelium, uses large tissue specimens from widespread EMR extending into the SQE, and includes a substantial number of patients, our findings may be considered of some general impact on BE surveillance and therapy. Our study cannot fully answer the question whether SSIM is a regular event in patients with non-neoplastic BE also, because only cases in which EMR was done for suspected BEassociated neoplasia were included. However, 26 cases had no neoplastic histology in the resection specimens despite initial positive biopsy at other institutions. Although occurrence of SSIM was not different between the groups of confirmed neoplastic and normal BE, the extent was greater in neoplastic BE. However, we examined a selected group of mostly neoplastic BE; therefore, biopsy studies in patients with proven nonneoplastic BE may be principally better suited to answer the question of SSIM occurrence in normal BE. On the other hand, such studies are likely to underreport the true SSIM frequency because of the substantial risk of addressing the wrong spots when using biopsies only.

4 408 Anders et al Clinical Gastroenterology and Hepatology Vol. 12, No. 3 Figure 3. Schematic drawing of variations in SSIM extent (see text); different extents of Barrett s epithelium underneath squamous epithelium (SSIM) are shown; measurement along the green line does not show any SSIM, while maximum extent of SSIM is depicted by the blue line. C, visible circular BE length; M, total extension of visible BE tongues. The impact of this sampling error is also underlined by our data, which show a somewhat lower rate of SSIM when calculated per specimen (89%) when compared with the calculation on a patient basis (98%). Furthermore, our study also revealed that SSIM extension mostly appears in an irregular, finger-like pattern. In previous studies, it was also debated whether the depth of conventional biopsies acquired from (neo-) SQE is sufficient to detect SSIM. Biddlestone et al12 suggested that SSIM is located in the deep portion of the epithelium and the lamina propria. Therefore, biopsies need to contain at least those layers to rule out the presence of SSIM. On the basis of these data, Overholt et al13 did not find differences in esophageal biopsy Figure 4. Histologic slides of SSIM. (A) The oral extension of BE glands (red arrow) underneath the SQE of the esophagus measures more than 3 mm; H&E 100x. (B) Another case also showing BE extension (red arrow); Alcian blue staining, 200x. (C) Subsquamous extension of a highly differentiated intramucosal Barrett s adenocarcinoma (red arrow); H&E 200x. depth between ablation-naive SQE and neo-squamous epithelium after photodynamic therapy or RFA. In line with these data, Pouw et al14 reported Lamina propria or deeper in 37% of biopsies derived from neo-squamous areas after RFA and 36% of ablation-naive squamous biopsies. On the other hand, squamous biopsies were less likely to contain subepithelial structures compared with columnar biopsy samples.15 In our

5 March 2014 Subsquamous Extension of Barrett s Esophagus 409 study, only EMR specimens were analyzed, which provide much more submucosal tissue than biopsies usually can. Our results considerably exceed the observations of a previous smaller study by Chennat et al, 11 who reported on subsquamous extension of Barrett epithelium in 13 of 47 patients. We also noted a considerably higher portion of patients with SSIM extension of 5 mm or more compared with the work of Chennat et al. Generally, evaluation of EMR specimens is hampered by orientation and related deviations in length measurement of SSIM; thus, precise ex vivo examination of specimens in the proximal-distal orientation as in the esophagus is not feasible. Therefore, it is not possible to determine whether SSIM was originally localized at the proximal margin or along the edges of visible BE tongues. Nevertheless, because no considerable squamous islands within BE were observed in our cohort, our data do represent solely SSIM along the proximal and/or marginal borders of visible BE and SQE. Furthermore, as compared with the previous study by Chennat et al in which the number of specimens per case is not mentioned, we analyzed a higher number of specimens overall and probably per patient also. Thus, our methodology is more likely to diminish the sampling error and may explain the higher SSIM frequency found in our study. In line with these findings, our data strengthen the hypothesis that subsquamous BE islands, so-called buried glands, do not represent a phenomenon on endoscopic therapy as has been suggested by previous reports, ie, after antireflux surgery, with a presumed regression of BE with SSIM being found in a variable percentage of patients. 16 However, as early as 1988, Sampliner et al 17 found SQE in 7 of 45 patients with biopsies from their proximal Barrett margin, although only 1 of these 7 patients had undergone antireflux surgery. SSIM was also described under squamous islands, which can be found within a Barrett segment, such as in 38.5% of 22 patients under proton pump inhibitor (PPI) therapy. 18 In line with this observation, PPIs, which are frequently given before or in parallel with endoscopic surveillance and therapy, have been suggested to promote the development of SSIM. Bronner et al 19 notedanincreaseinsquamousovergrowth from 2.9% of their patients (n ¼ 70) before treatment with PPIs to 33% (22 of 67) on treatment with PPIs during a period of 5 years. Furthermore, SSIM has been frequently described after endoscopic ablative therapies, which was recently summarized in a review article. 20 In some of the studies, baseline biopsies were taken, and SSIM was found in 0% 28% of cases combining results from 5 studies with a total of 456 cases. The development of SSIM after ablative therapy appears to be independent of the ablative treatment method applied. Even after RFA, in the large series with long-term follow-up of the randomized RFA trial, 21 it was reported that 4 of 14 subjects who attained complete eradication of BE and experienced recurrence of intestinal metaplasia at or after the 1-year follow-up had subsquamous BE or SSIM. 22 However, systematic biopsies were not taken in any of those studies mentioned above, and the sampling error is probably much higher than from an analysis of resection specimens. Because SSIM does not seem to spread homogenously along the esophageal circumference, it becomes more evident when the more specimens per patient are analyzed. Within our concept of attempted widespread EMR aiming at eliminating neoplasia plus all remaining Barrett tissue, in case of success, a new Z line at the esophagogastric junction is formed. Recurrences can therefore occur either at this location or from residual and/or buried glands in the neo-squamous epithelium. This fact is only occasionally dealt with in previous publications. In their series of widespread EMR, Pouw et al 23 did not describe the location of recurring neoplasia but found 10% of remaining Barrett islands within the SQE and 7% of Barrett histology below the neo-z line. The same groups reported long-term follow-up of 54 study patients treated with EMR and/or RFA; all 3 neoplasia recurrences found were located proximal to the neo-z line. 24 Gupta et al 25 noted recurrent BE in 37 of 229 patients after initial complete remission by using RFA. Recurrent BE was in the original BE area (n ¼ 18), at the neo-z line (n ¼ 17), or at both locations (n ¼ 2). Dysplastic recurrences were noted at the neo-z line (n ¼ 5) andwithintheesophagealbody(n¼ 3). Thus, it appears that recurrences can occur anywhere in the treated area; if located at the neo-z line, they may be due to resection extent not reaching far enough into the cardia, or if located in the neo-squamous epithelium, they may be due to remaining Barrett islands or buried glands at the level of the previous Z line originating from SSIM not fully resected into the SQE. In conclusion, our data do provide evidence for a regular extension of BE along the proximal and/or marginal borders of visible BE and SQE regardless of its neoplastic stage. Therefore, it seems to be justified to extend random biopsies for BE surveillance as well as endoscopic resection and/or ablation to 1 or even 1.5 cm proximal of the Z line and beyond the lateral borders of BE tongues. References 1. Fock KM, Ang TL. Global epidemiology of Barrett s esophagus. Expert Rev Gastroenterol Hepatol 2011;5: Spechler SJ, Sharma P, Souza RF, et al. American Gastroenterological Association technical review on the management of Barrett s esophagus. Gastroenterology 2011;140:e18 e52, quiz e Pech O, Behrens A, May A, et al. Long-term results and risk factor analysis for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma in Barrett s oesophagus. Gut 2008; 57:

6 410 Anders et al Clinical Gastroenterology and Hepatology Vol. 12, No Ell C, May A, Pech O, et al. Curative endoscopic resection of early esophageal adenocarcinomas (Barrett s cancer). Gastrointest Endosc 2007;65: Ell C, May A, Gossner L, et al. Endoscopic mucosal resection of early cancer and high-grade dysplasia in Barrett s esophagus. Gastroenterology 2000;118: Pohl H, Sonnenberg A, Strobel S, et al. Endoscopic versus surgical therapy for early cancer in Barrett s esophagus: a decision analysis. Gastrointest Endosc 2009;70: van Vilsteren FG, Pouw RE, Seewald S, et al. Stepwise radical endoscopic resection versus radiofrequency ablation for Barrett s oesophagus with high-grade dysplasia or early cancer: a multicentre randomised trial. Gut 2011;60: Seewald S, Akaraviputh T, Seitz U, et al. Circumferential EMR and complete removal of Barrett s epithelium: a new approach to management of Barrett s esophagus containing high-grade intraepithelial neoplasia and intramucosal carcinoma. Gastrointest Endosc 2003;57: Giovannini M, Bories E, Pesenti C, et al. Circumferential endoscopic mucosal resection in Barrett s esophagus with highgrade intraepithelial neoplasia or mucosal cancer: preliminary results in 21 patients. Endoscopy 2004;36: Chennat J, Konda VJ, Ross AS, et al. Complete Barrett s eradication endoscopic mucosal resection: an effective treatment modality for high-grade dysplasia and intramucosal carcinoma an American single-center experience. Am J Gastroenterol 2009; 104: Chennat J, Ross AS, Konda VJ, et al. Advanced pathology under squamous epithelium on initial EMR specimens in patients with Barrett s esophagus and high-grade dysplasia or intramucosal carcinoma: implications for surveillance and endotherapy management. Gastrointest Endosc 2009;70: Biddlestone LR, Barham CP, Wilkinson SP, et al. The histopathology of treated Barrett s esophagus: squamous reepithelialization after acid suppression and laser and photodynamic therapy. Am J Surg Pathol 1998;22: Overholt BF, Dean PJ, Galanko JA, et al. Does ablative therapy for Barrett esophagus affect the depth of subsequent esophageal biopsy as compared with controls? J Clin Gastroenterol 2010;44: Pouw RE, Gondrie JJ, Rygiel AM, et al. Properties of the neosquamous epithelium after radiofrequency ablation of Barrett s esophagus containing neoplasia. Am J Gastroenterol 2009; 104: Shaheen NJ, Peery AF, Overholt BF, et al. Biopsy depth after radiofrequency ablation of dysplastic Barrett s esophagus. Gastrointest Endosc 2010;72: Skinner DB, Walther BC, Riddell RH, et al. Barrett s esophagus: comparison of benign and malignant cases. Ann Surg 1983; 198: Sampliner RE, Steinbronn K, Garewal HS, et al. Squamous mucosa overlying columnar epithelium in Barrett s esophagus in the absence of anti-reflux surgery. Am J Gastroenterol 1988; 83: Sharma P, Morales TG, Bhattacharyya A, et al. Squamous islands in Barrett s esophagus: what lies underneath? Am J Gastroenterol 1998;93: Bronner MP, Overholt BF, Taylor SL, et al. Squamous overgrowth is not a safety concern for photodynamic therapy for Barrett s esophagus with high-grade dysplasia. Gastroenterology 2009;136:56 64, quiz Gray NA, Odze RD, Spechler SJ. Buried metaplasia after endoscopic ablation of Barrett s esophagus: a systematic review. Am J Gastroenterol 2011;106: Shaheen NJ, Sharma P, Overholt BF, et al. Radiofrequency ablation in Barrett s esophagus with dysplasia. N Engl J Med 2009;360: Shaheen NJ, Overholt BF, Sampliner RE, et al. Durability of radiofrequency ablation in Barrett s esophagus with dysplasia. Gastroenterology 2011;141: Pouw RE, Seewald S, Gondrie JJ, et al. Stepwise radical endoscopic resection for eradication of Barrett s oesophagus with early neoplasia in a cohort of 169 patients. Gut 2010; 59: Phoa KN, Pouw RE, van Vilsteren FG, et al. Remission of Barrett s esophagus with early neoplasia 5 years after radiofrequency ablation with endoscopic resection: a Netherlands cohort study. Gastroenterology 2013;145: Gupta M, Iyer PG, Lutzke L, et al. Recurrence of esophageal intestinal metaplasia after endoscopic mucosal resection and radiofrequency ablation of Barrett s esophagus: results from a US multicenter consortium. Gastroenterology 2013;145: e1. Reprint requests Address requests for reprints to: Thomas Rösch, MD, Department of Interdisciplinary Endoscopy, University Hospital Hamburg Eppendorf, Martinistr. 52, Hamburg, Germany. t.roesch@uke.de; fax: þ Acknowledgments Drs Anders, Lucks, and El-Masry contributed equally to this work. Conflicts of interest The authors disclose no conflicts.

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