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      Airway Inflammation in Chronic Rhinosinusitis with Nasal Polyps and Asthma: The United Airways Concept Further Supported

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          Abstract

          Background

          It has been established that patients with chronic rhinosinusitis with nasal polyps (CRSwNP) often have co-existing asthma.

          Objective

          We aimed to test two hypotheses: (i) upper and lower airway inflammation in CRSwNP is uniform in agreement with the united airways concept; and (ii) bronchial inflammation exists in all CRSwNP patients irrespective of clinical asthma status.

          Methods

          We collected biopsies from nasal polyps, inferior turbinates and bronchi of 27 CRSwNP patients and 6 controls. All participants were evaluated for lower airway disease according to international guidelines. Inflammatory cytokines were investigated using a Th1/Th2 assay including 14 chemokines and cytokines; tissue concentrations were normalized according to tissue weight and total protein concentration. Individual cytokines and multivariate inflammatory profiles were compared between biopsy sites and between patients and controls.

          Results

          We found significantly higher concentrations of Th2 cytokines in nasal polyps compared to inferior turbinate and bronchial biopsies. In addition, we showed that the inflammatory profile of nasal polyps and bronchial biopsies correlated significantly (p<0.01). From the Th2 cytokines measured, IL-13 was significantly increased in bronchial biopsies from CRSwNP patients with, but not without asthma.

          Conclusion

          Our findings support the united airways concept; however, we did not find evidence for subclinical bronchial inflammation in CRSwNP patients without asthma. Finally, this study indicates for the first time that nasal polyps potentially play an important role in the airway inflammation rather than being a secondary phenomenon.

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          Most cited references25

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          European Position Paper on Rhinosinusitis and Nasal Polyps 2012.

          The European Position Paper on Rhinosinusitis and Nasal Polyps 2012 is the update of similar evidence based position papers published in 2005 and 2007.The document contains chapters on definitions and classification, we now also proposed definitions for difficult to treat rhinosinusitis, control of disease and better definitions for rhinosinusitis in children. More emphasis is placed on the diagnosis and treatment of acute rhinosinusitis. Throughout the document the terms chronic rhinosinusitis without nasal polyps and chronic rhinosinusitis with nasal polyps are used to further point out differences in pathophysiology and treatment of these two entities. There are extensive chapters on epidemiology and predisposing factors, inflammatory mechanisms, (differential) diagnosis of facial pain, genetics, cystic fibrosis, aspirin exacerbated respiratory disease, immunodeficiencies, allergic fungal rhinosinusitis and the relationship between upper and lower airways. The chapters on paediatric acute and chronic rhinosinusitis are totally rewritten. Last but not least all available evidence for management of acute rhinosinusitis and chronic rhinosinusitis with or without nasal polyps in adults and children is analyzed and presented and management schemes based on the evidence are proposed.
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            Different types of T-effector cells orchestrate mucosal inflammation in chronic sinus disease.

            Chronic rhinosinusitis with nasal polyps (CRSwNP) is characterized by the accumulation of inflammatory cells; however, an eosinophil predominance is seen in white (Belgian), but not Asian (south Chinese), patients with polyps. We sought to investigate the association of inflammatory cell predominance with regulatory T-cell and T-effector cell patterns. Nasal mucosal tissue was obtained from 26 consecutive Belgian patients with CRSwNP and 21 Belgian control subjects and 29 south Chinese patients with CRSwNP and 29 south Chinese control subjects, who all underwent phenotyping, including nasal endoscopy and computed tomographic scanning. Tissues were investigated for granulocytes and their products and T-effector/regulatory T cells and related cytokines. Both CRSwNP groups were comparable in terms of symptoms, computed tomographic scan results, and nasal endoscopy results, but asthma comorbidity was significantly higher in white patients. Tissue from white patients with CRSwNP was characterized by eosinophilic inflammation (eosinophil cationic protein/myeloperoxidase ratio > 2), whereas samples from Asian patients were biased toward neutrophilic inflammation (eosinophil cationic protein/myeloperoxidase ratio = 0.25). Both CRSwNP groups demonstrated significant upregulation of the T-cell activation marker soluble IL-2 receptor alpha and significant downregulation of Foxp3 expression and TGF-beta1 protein content versus their respective control groups. However, whereas white patients displayed a significant increase in T(H)2 cytokine and related marker levels versus control subjects and versus Asian patients, the latter showed a T(H)1/T(H)17 cell pattern versus control tissue. Nasal polyps (CRSwNP) from white and Asian patients are both characterized by T-cell activation and impaired regulatory T-cell function; however, T-effector cells in the samples from white patients were T(H)2-biased, whereas samples from their Asian counterparts demonstrated a T(H)1/T(H)17 polarization.
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              British Thoracic Society guidelines on diagnostic flexible bronchoscopy.

              (2001)
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 July 2015
                2015
                : 10
                : 7
                : e0127228
                Affiliations
                [1 ]Department of Otorhinolaryngology, Head & Neck Surgery and Audiology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
                [2 ]Upper Airways Research Laboratory, Ghent University Hospital, Ghent, Belgium, ENT-Department, Karolinska Institute, Stockholm, Sweden
                [3 ]Centre for Clinical Education, University of Copenhagen and the Capital Region of Denmark, Copenhagen, Denmark
                [4 ]Department of Respiratory Medicine L, Bispebjerg Hospital, University of Copenhagen, Copenhagen, Denmark
                [5 ]Department of International Health, Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
                [6 ]Department of Biomedical Sciences, Endocrinology Research Section, University of Copenhagen, Copenhagen, Denmark
                [7 ]The Bioinformatics Centre (BINF), Department of Biology and Biotech Research and Innovation Centre (BRIC), University of Copenhagen, Copenhagen, Denmark
                [8 ]Section for Cognitive Systems, DTU Compute Technical University of Denmark (DTU), Copenhagen, Denmark
                University of Tennessee Health Science Center, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: KH CB SFT LK VB CvB. Performed the experiments: KH LK VB CB AEP SSP. Analyzed the data: KH CB TM-B OW CvB. Contributed reagents/materials/analysis tools: KH CB AEP SSP VB. Wrote the paper: KH CB LK SFT AEP SSP TM-B OW VB CvB.

                Article
                PONE-D-14-48525
                10.1371/journal.pone.0127228
                4489400
                26132710
                da8a7b52-03ea-4d11-b1ab-549be0643280
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 28 October 2014
                : 12 April 2015
                Page count
                Figures: 2, Tables: 3, Pages: 11
                Funding
                The authors would like to gratefully acknowledge Candy Foundation and Ørelæge Hans Skouby's og Hustru Emma Skouby`s Foundation for supporting their work. Both of these are non-profit organisation and neither was involved in the conception, execution, and interpretation or publication strategy of this study.
                Categories
                Research Article
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                All relevant data are within the paper and its Supporting Information files.

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