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Elevated Calprotectin Levels Reveal Bowel Inflammation In ARD Online First, published on May 10, 2016 as 10.1136/annrheumdis-2015-208025 Ann Rheum Dis: first published as 10.1136/annrheumdis-2015-208025 on 23 December 2015. Downloaded from Clinical and epidemiological research CONCISE REPORT Elevated calprotectin levels reveal bowel inflammation in spondyloarthritis H Cypers,1,2 G Varkas,1,2 S Beeckman,1 K Debusschere,1,2 T Vogl,3 J Roth,3 M B Drennan,1,2 M Lavric,4 D Foell,4 C A Cuvelier,5 M De Vos,6 J Delanghe,7 F Van den Bosch,1 D Elewaut1,2 Handling editor Tore K Kvien ABSTRACT ileum. Two types of inflammation can be distin- 1Department of Rheumatology, Introduction Microscopic bowel inflammation is guished based on histomorphology (not disease Ghent University Hospital, present in up to 50% of patients with spondyloarthritis duration): acute inflammation whereby the epithe- Ghent, Belgium fi 2 (SpA) and is associated with more severe disease. lium is in ltrated with granulocytes but mucosal Unit for Molecular fl fl Currently no reliable biomarkers exist to identify patients architecture is normal, and chronic in ammation Immunology and In ammation, fl VIB Inflammation Research at risk. Calprotectin is a sensitive marker of neutrophilic (with acute in ammation or quiescent) showing dis- Center Ghent University, inflammation, measurable in serum and stool. turbance of mucosal architecture and a chronic Ghent, Belgium Objectives To assess whether serum and faecal lymphoplasmacytic cellular infiltrate in the lamina 3 Institute of Immunology, calprotectin in addition to C-reactive protein (CRP) can propria. The mucosal changes seen in the latter University of Münster, Münster, be used to identify patients with SpA at risk of type bear particular resemblance to those seen in Germany 1 4Department of Pediatric microscopic bowel inflammation. early Crohn’s disease (CD). These findings were Rheumatology and Methods Serum calprotectin and CRP were measured recently confirmed in the GIANT (Ghent Immunology, University of in 125 patients with SpA. In 44 of these patients, faecal Inflammatory Arthritis and Spondylitis) cohort.2 Münster, Münster, Germany samples were available for calprotectin measurement. All Bowel inflammation seems to be an important 5Department of Pathology, Ghent University, Ghent, 125 patients underwent an ileocolonoscopy to assess prognostic factor in SpA, as it was shown to be Belgium the presence of microscopic bowel inflammation. associated with more extensive bone marrow 6Department of Results Microscopic bowel inflammation was present in oedema of the sacroiliac joints, a higher risk of Gastroenterology, Ghent 53 (42.4%) patients with SpA. Elevated serum progression to ankylosing spondylitis (AS), and a University Hospital, Ghent, 34 Belgium calprotectin and CRP were independently associated with higher risk of developing CD. However, diagno- 7Department of Clinical microscopic bowel inflammation. Faecal calprotectin was sis is made by means of endoscopy, as reliable Chemistry, Microbiology and also significantly higher in patients with microscopic biomarkers are lacking. Calprotectin, the heterodi- Immunology, Ghent University bowel inflammation. Patients with CRP and serum mer of S100A8 (MRP8) and S100A9 (MRP14), is a Hospital, Ghent, Belgium calprotectin elevated had a frequency of bowel cytosolic protein expressed in phagocytic myeloid fl Correspondence to in ammation of 64% vs 25% in patients with low levels cells. It is released from activated monocytes and Dr Dirk Elewaut, Department of both. When either CRP or serum calprotectin was granulocytes at local sites of inflammation (eg, of Rheumatology, Unit for elevated, the risk was intermediate (40%) and intestinal mucosa in IBD or synovium in inflamma- Molecular Immunology and measuring faecal calprotectin provided further tory arthritis) during the early phase of the http://ard.bmj.com/ Inflammation, VIB Inflammation Research Center, differentiation. Hence we suggest a screening approach immune response. Extracellularly, it has prominent Ghent University, De Pintelaan where initially serum calprotectin and CRP are assessed proinflammatory effects via toll-like receptor 4 185, Ghent 9000, Belgium; and, if necessary, faecal calprotectin. The model using dependent mechanisms. Hence it can be considered [email protected] this scenario provided an area under the ROC curve of a marker of innate immune activation.5 74.4% for detection of bowel inflammation. Calprotectin can be measured in serum and stool, Received 3 June 2015 Conclusions Calprotectin measurements in stool and and elevated serum concentrations have been found Accepted 27 November 2015 on September 29, 2021 by guest. Protected copyright. serum, in addition to CRP, may provide a promising in several inflammatory conditions. Moreover strategy to identify patients with SpA at risk of bowel faecal calprotectin has been well established as a inflammation and could play a role in overall patient marker of disease activity in IBD.6 However, no stratification. study has yet addressed the relation between serum or faecal levels of calprotectin and bowel histology in SpA. INTRODUCTION The link between bowel and joint in spondyloar- METHODS thritis (SpA) has been established for several Patients and study parameters decades. A subgroup of patients with SpA develops One hundred and twenty-five patients with SpA inflammatory bowel disease (IBD). Conversely, from the GIANT cohort were included in this ana- patients with inflammatory bowel disease (IBD) can lysis. This is a prospective follow-up study including To cite: Cypers H, develop SpA. Furthermore, in the 1980s, it was patients with newly diagnosed (expert opinion) Varkas G, Beeckman S, demonstrated that up to 50% of all patients with axial and/or peripheral SpA, classified according to et al. Ann Rheum Dis fl Published Online First: SpA have microscopic bowel in ammation, without the Assessment of SpondyloArthritis international [please include Day Month associated gastrointestinal (GI) symptoms. Bowel Society (ASAS) criteria.2 Patients were interviewed Year] doi:10.1136/ inflammation in SpA can affect the ileum as well as about their disease activity, drug intake and possible annrheumdis-2015-208025 the colon, but is most prominent in the terminal GI symptoms. A complete clinical examination was Cypers H, et al. Ann Rheum Dis 2015;0:1–6. doi:10.1136/annrheumdis-2015-208025 1 Copyright Article author (or their employer) 2016. Produced by BMJ Publishing Group Ltd (& EULAR) under licence. Ann Rheum Dis: first published as 10.1136/annrheumdis-2015-208025 on 23 December 2015. Downloaded from Clinical and epidemiological research performed with scoring of tender and swollen joints, enthesitis SpA (55% HLAB27+). Stool samples were available for 44 and evaluation of axial mobility. Serum samples were collected patients out of this group (13 AS, 28 nr-ax SpA, 3 peripheral from all patients at baseline. Serum samples of 39 healthy SpA). donors and 23 patients with rheumatoid arthritis (RA) were used as controls. We started collecting faecal samples in patients with Microscopic bowel inflammation in SpA and clinical SpA only later in the course of this cohort study, and this pro- characteristics vided a greater challenge than serum sampling; hence faecal Microscopic bowel inflammation was present in 53 patients samples were available in only 44 patients. Stool samples were (42.4%), none of whom reported relevant GI symptoms. collected within a week before colonoscopy (but prior to bowel Macroscopic lesions were found in 31% of patients and con- preparation) and were stored unprocessed at −80°C. Patients sisted of discrete ulcerations, erosions or erythema. All but 20 with significant GI symptoms or overt IBD were excluded from patients received therapy with NSAIDs. None of the patients this analysis. Non-steroidal anti-inflammatory drug (NSAID) had prior exposure to a biological. Because we wanted to intake 3 months prior to the ileocolonoscopy was estimated by exclude possible direct interference, patients were asked to inter- calculation of the NSAID index score, as proposed by ASAS.7 rupt NSAID 7 days prior to colonoscopy. However, this was only introduced in the second half of the study. Fifty-one (41%) Ileocolonoscopy patients were able to interrupt NSAID therapy before colonos- All patients with SpA underwent an ileocolonoscopy to assess copy. Patients on NSAIDs during colonoscopy had a higher per- the presence of microscopic bowel inflammation. For each centage of bowel inflammation (mainly the chronic type of patient, 4–14 biopsy samples were taken of affected (if any) and inflammation) than those interrupting NSAID 7 days prior to unaffected regions of terminal ileum and colon. colonoscopy (p=0.016). However, this association was no longer significant when we corrected for disease activity (Bath Histological classification Ankylosing Spondylitis Disease Activity Index (BASDAI) and Ileal and colonic biopsies were read by an experienced patholo- CRP; p=0.063). No difference was seen in the NSAID index gist (CAC) in a blinded fashion. Biopsies were classified as score 3 months prior to the ileocolonoscopy in patients with or normal, acutely or chronically inflamed, based on histomorpho- without microscopic bowel inflammation (p=0.711). Age, sex, logical characteristics, as previously described.1 smoking status, ASAS category, HLAB27 positivity, swollen joint count, Bath Ankylosing Spondylitis Metrology Index (BASMI) Serum and faecal calprotectin measurement and BASDAI did not differ significantly in patients with and Calprotectin in serum and stool
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