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Peripheral Eosinophilia in Patients With Inflammatory Bowel Disease Defines an Aggressive Disease Phenotype

Click, Benjamin, MD1; Anderson, Alyce M, PhD1; Koutroubakis, Ioannis E, MD, PhD1; Rivers, Claudia Ramos, MD1; Babichenko, Dmitriy, MS2; Machicado, Jorge D, MD1; Hartman, Douglas J, MD3; Hashash, Jana G, MD1; Dunn, Michael A, MD1; Schwartz, Marc, MD1; Swoger, Jason, MD1; Barrie, Arthur III, MD, PhD1; Wenzel, Sally E, MD4; Regueiro, Miguel, MD1; Binion, David G, MD1

American Journal of Gastroenterology: December 2017 - Volume 112 - Issue 12 - p 1849–1858
doi: 10.1038/ajg.2017.402
ORIGINAL CONTRIBUTIONS: INFLAMMATORY BOWEL DISEASE
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OBJECTIVES: Peripheral blood eosinophilia (PBE) in inflammatory bowel disease (IBD) is associated with ulcerative colitis (UC) and active disease. Little data exist on the long-term impact of PBE on disease course. We aimed to investigate the multi-year patterns of PBE and its impact on disease severity in a large IBD cohort.

METHODS: We performed a registry analysis of a consented, prospective, natural history IBD cohort at a tertiary center from 2009 to 2014. Demographics, comorbidities, disease activity, healthcare utilization, and time to hospitalization or surgical resection of patients who displayed PBE were compared to patients without PBE.

RESULTS: Of the 2,066 IBD patients, 19.2% developed PBE. PBE was significantly associated with UC (P<0.001), extensive colitis (P<0.001), and shorter disease duration (P=0.03). Over six years, PBE patients had more active disease (Harvey–Bradshaw IndexP=0.001; ulcerative colitis activity indexP<0.001), concurrent C-reactive protein elevation (P<0.001), healthcare utilization (hospitalizationP<0.001, IBD surgeryP<0.001), and more aggressive medical therapy (prednisoneP<0.001, anti-TNFP<0.001). Patients with PBE had a significantly reduced time to hospitalization in both UC (P<0.001) and Crohn’s disease (CD) (P<0.001) and reduced time to colectomy in UC (P=0.003). On multivariable modeling, PBE remained significantly associated with hospitalization and surgery in both CD and UC. New diagnosis of UC with PBE was associated with increased steroid (P=0.007) and anti-TNF (P=0.001) requirement.

CONCLUSION: This multi-year study of a large IBD cohort suggests that peripheral blood eosinophilia represents a biomarker of a distinct IBD subgroup, with a unique inflammatory signature, and at risk for worse clinical outcomes.

1Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA

2School of Information Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

3Department of Anatomic Pathology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA

4Asthma Institute, Division of Pulmonary, Allergy, and Critical Care Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA

Correspondence: David G. Binion, MD, Professor of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh School of Medicine, 200 Lothrop Street Mezzanine Level C Wing, Pittsburgh, Pennsylvania 15213, USA. E-mail: binion@pitt.edu

Received 01 December 2015; accepted 02 September 2017

Guarantor of the article: David Binion, MD.

Specific author contributions: B.C.: study conception, data collection, performing analysis, interpreting data, drafting of manuscript, approval of final manuscript. A.M.: study conception, interpreting analysis, drafting of manuscript, approval of final manuscript. I.K.: study conception, critical review of manuscript, approval of final manuscript. C.R.: data collection, critical review of manuscript, approval of final manuscript. D.B.: data collection, critical review of manuscript, approval of final manuscript. J.M.: performing analysis, critical review of manuscript, approval of final manuscript. D.H.: study conception, critical review of manuscript, approval of final manuscript. J.H.: data collection, critical review of manuscript, approval of final manuscript. M.D.: provided study funding, critical review of manuscript, approval of final manuscript. M.S.: data collection, critical review of manuscript, approval of final manuscript. J.S.: data collection, critical review of manuscript, approval of final manuscript. A.B.: data collection, critical review of manuscript, approval of final manuscript. S.W.: study conception, critical review of manuscript, approval of final manuscript. M.R.: study conception, critical review of manuscript, approval of final manuscript. D.B.: study conception, interpreting data, critical review of manuscript, approval of final manuscript.

Financial support: This work was supported by the National Institutes of Health (5T32DK063922-12 to BC; PI: David Whitcomb, MD, PhD); sabbatical salary of Medical Faculty University of Crete, Greece (to IEK); the University of Pittsburgh Clinical and Translational Science Institute (5TL1TR000145-09 to AMA; PI: Steven Reiss, MD); and the United States Army Medical Research and Materiel Command (W81XWH-11-2-0133 to DGB and MAD).

Potential competing interests: None.

SUPPLEMENTARY MATERIAL is linked to the online version of the paper at http://www.nature.com/ajg

© The American College of Gastroenterology 2017. All Rights Reserved.
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