Outcomes of Barrett s oesophagus related to systemic sclerosis: a 3-year EULAR Scleroderma Trials and Research prospective follow-up study
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1 RHEUMATOLOGY Rheumatology 2011;50: doi: /rheumatology/ker110 Advance Access publication 16 March 2011 Concise report Outcomes of Barrett s oesophagus related to systemic sclerosis: a 3-year EULAR Scleroderma Trials and Research prospective follow-up study Julien Wipff 1, Romain Coriat 2, Michela Masciocchi 3, Paola Caramaschi 4, Chris T. Derk 5, Eric Hachulla 6, Valeria Riccieri 7, Luc Mouthon 8, Dorota Krasowska 9, Lidia P. Ananyeva 10, André Kahan 1, Marco Matucci-Cerinic 11, Stanislas Chaussade 2 and Yannick Allanore 1 CLINICAL SCIENCE Abstract Objective. Barrett s oesophagus (BE) is the major risk factor for oesophageal adenocarcinoma (EAC). SSc is associated with an increased risk of BE related to chronic reflux. The aim of this study is to determine the outcomes of BE and estimate the EAC risk in over a 3-year prospective study. Methods. were recruited through EUSTAR network centres. Inclusion criterion was a recent histological finding of BE. The patients were then prospectively followed and, as recommended, a second oesophageal endoscopy was performed according to the presence of BE-related at baseline. Results. A total of 50 with BE (40 without and 10 with ) were included and 46 completed the follow-up (138 patient-years). During the 3-year follow-up, 4 of the 46 BE patients (3% per year) were diagnosed with high-grade /EAC, of which one developed cardial EAC. EAC incidence in the BE subgroup with increased to 4% per year compared with the absence of EAC cases in the BE subgroup without at baseline. Conclusion. Our results, in accordance with previous published data suggesting an increased risk of EAC or cardial adenocarcinoma in SSc, highlight the need for accurate follow-up of BE at risk of developing adenocarcinoma. Key words: Systemic sclerosis, Barrett s oesophagus, Dysplasia, Oesophageal adenocarcinoma, Endoscopy, Follow-up. Introduction 1 Rheumatology A Department, 2 Gastro-enterology Department, Paris Descartes University, Cochin Hospital, AP-HP, Paris, France, 3 Immunology Department, Immunological Clinic, Mangiagalli Regina Elena Foundation, Milan, 4 Department of Medicine, Verona University, Verona, Italy, 5 Department of Medicine, Division of Rheumatology, Thomas Jefferson University, Philadelphia, PA, USA, 6 Internal Medicine, Lille II University, Lille, France, 7 Medical Clinic and Therapy Department, Sapienza University of Rome, Rome, Italy, 8 Internal Medicine, Cochin Hospital, Paris Descartes University, AP-HP, Paris, France, 9 Department of Dermatology, Medical University of Lublin, Lublin, Poland, 10 Rheumatology Department, Institute of Rheumatology, Russian Academy of Medical Science, Moscow, Russia and 11 Department of Biomedicine, Division of Rheumatology AOUC, University of Florence, Florence, Italy. Submitted 13 September 2010; revised version accepted 10 February Correspondence to: Julien Wipff, Rheumatology A Department, Paris Descartes University, Cochin Hospital, AP-HP, 27 Rue du Faubourg St Jacques, Paris, France. julien.wipff@cch.aphp.fr Since the 1980s, a dramatic increase in the incidence of oesophageal adenocarcinoma (EAC) has been observed [1]. The principal risk factor for EAC is the presence of Barrett s oesophagus (BE), particularly BE with high-grade (HGD) [2]. Low-grade (LGD) is also a risk factor with a relative risk of 3. BE is defined by the presence of intestinal architecture in the lower oesophagus displaying a villiform columnar-lined mucosa with goblet cells. The incidence of EAC in BE patients is estimated to be 1 per 220 patient-years or 0.45% per year [3]. This has led to the publication of recommendations for assessing common BE and the need for regular endoscopy [4]. Only a few studies have determined the prevalence of BE and EAC in SSc, with conflicting results [5, 6]. In a! The Author Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please journals.permissions@oup.com
2 Barrett s oesophagus in SSc previous cross-sectional study [7], the prevalence of BE was estimated to be 13% (14 patients) and no patient had adenocarcinoma in a cohort of 110 consecutive SSc patients who underwent systematic endoscopy. Three (21%) patients had, of which one had HGD requiring specific endoscopic treatment. The risk of cancer following BE in SSc has never been addressed. However, a recent study has shown an overall increase in the incidence of cancer, in particular for oesophageal cancers [8]. Therefore, there is a crucial need to define the outcomes of BE in. Methods The project was approved by the EULAR Scleroderma Trials and Research (EUSTAR) board and was undertaken at all centres. We included with a recent (between 1995 and 2006) histological finding of BE diagnosed via oesophageal endoscopy (supplementary figure 1, available as supplementary data at Rheumatology Online). Some patients could have been previously diagnosed with BE before being included in this study based on a recent finding of BE. Exclusion criterion was the presence of oesophageal cancer at baseline. The cutaneous SSc subtype was defined according to LeRoy et al. [9]. Disease duration was the time from the first non-rp symptom and proton pump inhibitor (PPI) efficiency meant that reflux symptoms are controlled under treatment. Other demographic and digestive characteristics were collected (supplementary table 1, available as supplementary data at Rheumatology Online) as previously described [7]. All endoscopic procedures were carried out based on the usual practices of each centre. If macroscopic lesions suggestive of BE were detected, then biopsy samples were collected. BE was defined by the presence of intestinal architecture in the lower oesophagus displaying a villiform columnar-lined mucosa with goblet cells (supplementary figure 1, available as supplementary data at Rheumatology Online). As recommended in common BE cases [4], a second oesophageal endoscopy was carried out after a follow-up of 3 years for patients with BE and no, after 1 year for BE patients with LGD and every 3 months in cases of HGD (supplementary figure 1, available as supplementary data at Rheumatology Online). During the follow-up, centres were re-contacted after 3, 12 or 36 months, according to the planned endoscopic follow-up. Cases with HGD and EAC were grouped into a single group, HGD/EAC. The chi-square test and the Mann Whitney U test were used to compare baseline data. P < 0.05 was considered statistically significant. The association between baseline variables and our predefined endpoint were evaluated after the end of the 3-year prospective follow-up period with Cox regression analysis. Results The baseline digestive characteristics of the 50 recruited are reported in Table 1, and detailed for the presence (n = 10) or absence (n = 40) of at baseline. Of the 50 patients, 9 (82%) patients of the global BE SSc population had oesophageal symptoms related to reflux (pyrosis and/or dysphagia), thus 18% of BE patients still remained asymptomatic. Among the 10 patients with at baseline, 2 had HGD, 5 had LGD and levels were indeterminate in 3 patients. BE with had a higher mean disease duration [17.8 (13.7) vs 10.7 (8.9) years, P = 0.02] and a higher frequency of the limited cutaneous form (OR 9.94, 95% CI 1.15, 86.0, P = 0.01) and ACA positivity (OR 4.5, 95% CI 1.05, 19.2, P = 0.02) than patients without. The presence of dysphagia was more frequent in BE patients with (OR 10.5, 95% CI 1.9, 57.6, P = ). The 138 patient-years of follow-up were subdivided into 27 patient-years for the BE subgroup with and 111 patient-years for the BE subgroup without TABLE 1 Baseline digestive characteristics for all, and with and without BE All SSc patients (n = 50) with BE (n = 10) without BE (n = 40) P-value; OR a ; 95% CI BE duration, mean (S.D.), years 1.7 (4.5) 2.5 (6.3) 1.5 (3.9) 0.67 Reflux, n (%) 37 (74) 8 (80) 29 (72) 0.63 Dysphagia, n (%) 19 (38) 8 (80) 11 (27) ; 10.5; 1.9, 57.6 PPI use, n (%) 38 (76) 7 (70) 31 (77) 0.62 PPI dose, mean (S.D.), mg/day 27 (25) 36 (37) 25 (20) 0.80 PPI efficiency, n (%) 18 (36) 2 (20) 16 (40) 0.24 NSAID use, n (%) 1 (2) 0 (0) 1 (2) 0.49 Platelet anti-aggregating use, n (%) 15 (30) 3 (30) 12 (30) 0.99 Malabsorption, n (%) 5 (10) 0 (0) 5 (12) 0.12 Bacterial overgrowth, n (%) 5 (10) 2 (20) 3 (7) 0.24 Rectal incontinence, n (%) 3 (6) 1 (10) 2 (5) 0.55 a Comparison between dysplastic and non-dysplastic BE patients
3 Julien Wipff et al. at baseline. Four patients were excluded: two patients, belonging to BE subgroup without, who died (one due to SSc renal crisis and one due to pulmonary fibrosis) and two who were lost to follow-up. The risk of EAC alone in this study was about 1 patient in 138 patient-years (0.7% per year) for global BE patients. The risk of the finding of HGD/EAC in the overall BE group was 2.9% per year (4/138 patient-years). Three of these four cases of HGD/EAC required specific treatment: chemotherapy and surgery for recurrent EAC, endoscopic mucosectomy for the two cases of HGD, including surgical resection of the distal third of oesophagus in one case and surveillance for the last case of HGD. During the 3 years of follow-up of the BE patients without at baseline, three patients subsequently developed, of which only one developed HGD but no patients developed adenocarcinoma. In the BE subgroup with at baseline, three cases of HGD/ EAC were detected during the follow-up: one LGD patient developed a cardial EAC and the two patients with HGD were confirmed to have HGD. Results of the univariate analysis assessing risk factors for HGD/EAC are detailed in Table 2. At baseline, we did not find any factor to be predictive for the development of HGD/EAC during follow-up. Discussion This is the first study to address the risk of oesophageal cancer in with BE. There was a slightly greater incidence of oesophageal cancer (0.7% per year) in the European SSc BE population than in the classic BE population (recently published to be 0.45% per year) [3]. Of the most interest, no patients developed adenocarcinoma if BE without occurred at baseline. During the 3-year interval, EAC occurred in one patient, a patient with pre-existing BE. These findings suggest an increased risk of oesophageal cancer in, especially in those with, as previously reported [8]. This risk suggests the need for accurate follow-up of SSc patients with BE and confirmation in a larger prospective BE SSc cohort. There are several reasons why BE SSc patients may be a particular population for the risk of developing EAC and they are: (i) BE are strict opposites (non-smoking females with BMI < 30) of the prototype BE patients, i.e. males (80%) [10, 11], obese (50%) [12] and smoker (25%) [11] and (ii) the systematic use of PPIs in our population study whereas a recent systematic literature review appears to demonstrate that PPIs protect against the progression of BE to neoplastic lesions [13]. One explanation of the specific risk of developing BE in SSc without other classical risk factor may be attributed to the oesophageal involvement characterized by oesophageal dysmotility and lower oesophageal sphincter pressure that favours reflux. Retrospective studies suggest that EAC diagnosed during the surveillance programme are more often early-stage EAC [5], and that these programmes have increased survival [14]. Early diagnosis of BE in patients is therefore critical for preventing neoplastic transformation. One way of reaching this goal is to perform a systematic endoscopy in every newly diagnosed SSc patient, whatever their oesophageal symptom status, as previously proposed [15]. Thus, this may ensure that diagnosis of BE and in particular HGD at baseline are not missed in without oesophageal symptoms (18% in our study), HGD being, in this study, the only predictive risk factor for the occurrence of HGD/ EAC during follow-up. Moreover, BE patients with dysphagia, lcssc subtype and/or the presence of ACAs appear to be the subgroup of patients with a high risk of. This latter subgroup should be of particular interest when carrying out an accurate oesophageal survey. TABLE 2 Comparison of baseline characteristics between BE patients with HGD/EAC and those without during follow-up: univariate analysis with HGD/EAC (n =4) without HGD/EAC (n = 42) P-value; OR; 95% CI Disease duration, mean (S.D.), years 24.7 (8.3) 11.9 (9.9) 0.91 BE duration, mean (S.D.), years 3.2 (4.6) 3.3 (4.8) 0.49 Reflux, n (%) 4 (100) 32 (76) 0.15 Dysphagia, n (%) 3 (75) 15 (36) 0.12 PPI use, n (%) 3 (75) 32 (76) 0.99 PPI dose, mean (S.D.), mg/day 55 (50) 24.2 (20) 0.84 PPI efficiency, n (%) 1 (25) 15 (36) 0.67 Limited cutaneous form, n (%) 3 (75) 24 (57) 0.49 ACAs, n (%) 1 (25) 15 (36) 0.67 Platelet anti-aggregating use, n (%) 2 (50) 13 (31) 0.44 Malabsorption, n (%) 1 (25) 3 (7) 0.23 Dysplasia 3 (75) 6 (14) ; 18; 1.59,
4 Barrett s oesophagus in SSc The risk of developing EAC appears to be similar between an SSc BE population and a classic BE population, suggesting that endoscopic surveillance guidelines updated in 2008 may be applied to the SSc BE population [4]: thus, the patient would undergo an endoscopy every 3 years if intestinal metaplasia without occurs; every year for LGD, taking into account the risk of cancer being 3-fold greater in LGD than in patients without [16]. Assuming that EAC is often present when HGD is diagnosed [3], at present, HGD diagnosis should systematically lead to similar interventional procedures to those for early EAC, especially local endoscopic therapies, which are safe and have an excellent long-term survival rate [17]. The literature seems to show a weak but real risk of EAC. Whereas Segel et al. [6] only identified one patient with adenocarcinoma in a cohort of 680, the analysis of a recent cohort showed an increased risk of oesophageal cancer in particular in males [n = 7 with a RR = 55.5 (95% CI 6.85, 104.1)] [8] and a EUSTAR cohort confirmed oesophageal cancer as being a possible cause of death in [18]. In the most recent EUSTAR database (December 2010, data not published), two patients died directly or indirectly due to oesophageal transformation: one died due to EAC and one died from infection after surgery for BE. It is unclear whether the presence of intestinal metaplasia is required for diagnosing BE. Some research has already excluded this criterion for BE diagnosis, arguing similar neoplastic risk in patients with and without goblet cells [19]. Thus, the exclusion of this criterion should be tested in BE for similar lengths of follow-up [20]. Altogether, our results suggest modifying the management of with BE whereby patients should undergo a systematic endoscopy on SSc diagnosis [8] and regular endoscopic monitoring (supplementary figure 2, available as supplementary data at Rheumatology Online). These endoscopic surveys should consider initial histological findings and changes to clinical symptoms, particularly whether a patient displays incident or increased dysphagia. These recommendations will have, therefore, to be fully validated in future larger studies with longer follow-up. However, the interpretation of these results is limited by the small sample size of our cohort, a short follow-up period and no central histological assessment. The duration of of a particular stage (low and high grade) or timing of conversion from one stage to another cannot be certainly determined because not all patients had repeated endoscopy at regular intervals. Conclusion SSc is associated with an increased risk of BE related to chronic reflux. The risk of EAC is also increased in SSc. This result supports the need for accurate follow-up of with BE, to diagnose and/or cancer as early as possible. Close management of BE may allow early and effective treatment of these severe complications. Rheumatology key messages. SSc is associated with an increased risk of BE related to chronic reflux.. The risk of EAC is also increased in SSc.. Early diagnosis of in BE is critical in preventing neoplastic transformation. Acknowledgements The authors thank Dr Conri from Bordeaux (France), Dr Opris from Bucharest (Romania) and Dr Granel from Marseille (France), for their active participation, collaboration and inclusion of patients in this study. EUSTAR is supported by a research grant from EULAR and is under the auspices of the Standing Committee for International Studies Including Clinical Trials (ESCCA) Disclosure statement: The authors have declared no conflicts of interest. Supplementary data Supplementary data are available at Rheumatology Online. References 1 Bollschweiler E, Wolfgarten E, Gutschow C et al. Demographic variations in the rising incidence of esophageal adenocarcinoma in white males. Cancer 2001;92: Heath E, Limburg P, Hawk E et al. Adenocarcinoma of the esophagus: risk factors and prevention. Oncology 2000; 14: Conio M, Blanchi S, Lapertosa G et al. Long-term endoscopic surveillance of patients with Barrett s esophagus. Incidence of and adenocarcinoma: a prospective study. Am J Gastroenterol 2003;98: Wang KK, Sampliner RE. Updated guidelines 2008 for the diagnosis, surveillance and therapy of Barrett s esophagus. Am J Gastroenterol 2008;103: Katzka D, Reynolds JC, Saul S et al. Barrett s metaplasia and adenocarcinoma of the esophagus in scleroderma. Am J Med 1987;82: Segel M, Campbell W, Medsger T et al. Systemic sclerosis (scleroderma) and esophageal adenocarcinoma: is increased patient screening necessary? Gastroenterology 1985;89: Wipff J, Allanore Y, Soussi F et al. Prevalence of Barrett s esophagus in systemic sclerosis. Arthritis Rheum 2005;52: Derk CT, Rasheed M, Artlett CM et al. A cohort study of cancer incidence in systemic sclerosis. J Rheumatol 2006; 33: LeRoy EC, Black C, Fleischmajer R et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 1988;15: Bani-Hani K, Sue-Ling H, Johnston D et al. Barrett s esophagus: results from a 13-year surveillance programme. Eur J Gastroenterol Hepatol 2000;12:
5 Julien Wipff et al. 11 Gammon MD, Schoenberg JB, Ahsan H et al. Tobacco, alcohol and socioeconomic status and adenocarcinoma of the esophagus and gastric cardia. J Natl Cancer Inst 1997;89: Lagergren J, Bergstrom R, Nyren O. Association between body mass and adenocarcinoma of the esophagus and gastric cardia. Ann Int Med 1999;130: Islami F, Kamangar F. Use of proton pump inhibitors and risk of progression of Barrett s esophagus to neoplastic lesions. Am J Gastroenterol 2009;104: Corley DA, Levin TR, Habel LA et al. Surveillance and survival in Barrett s adenocarcinomas: a population-based study. Gastroenterology 2002;122: Domsic R, Fasanella K, Bielefeldt K. Gastrointestinal manifestations of systemic sclerosis. Dig Dis Sci 2008;53: Gatenby P, Ramus J, Caygill C et al. Routinely diagnosed low-grade in Barrett s esophagus: a population-based study of natural history. Histopathology 2009;54: Pech O, Behrens A, May A et al. Long-term results and risk factors for recurrence after curative endoscopic therapy in 349 patients with high-grade intraepithelial neoplasia and mucosal adenocarcinoma on Barrett s oesophagus. Gut 2008;57: Tyndall AJ, Bannert B, Vonk M et al. Causes and risk factors for death in systemic sclerosis: a study from the EULAR scleroderma trials and research (EUSTAR) database. Ann Rheum Dis 2010;69: Gatenby PA, Ramus JR, Caygill CP et al. Relevance of the detection of intestinal metaplasia in non-dysplastic columnar-lined oesophagus. Scand J Gastroenterol 2008; 43: Riddell RH, Odze RD. Definition of Barrett s esophagus: time for a rethink - is intestinal metaplasia dead? Am J Gastroenterol 2009;104:
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