IL-13 and IL-13–induced periostin levels are specifically decreased in patients following endoscopic sinus surgery for chronic rhinosinusitis

Regan Harmon, Alexander L. Schneider, Junqin Bai, Samuel D. Racette, Abhita T. Reddy, Julia H. Huang, David S. Lehmann, Caroline P.E. Price, Samuel Rodeghiero, Aditi Agarwal, Jacob G. Eide, Siyuan Dong, David B. Conley, Kevin C. Welch, Robert C. Kern, Stephanie Shintani-Smith, Anju T. Peters, Atsushi Kato, Whitney W. Stevens, Lutfiyya N. MuhammadRobert P Schleimer, Bruce K. Tan*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Background: Type 2 (T2) inflammation plays a pathogenic role in chronic rhinosinusitis (CRS). The effects of endoscopic sinus surgery (ESS) on T2 inflammation are unknown. Objective: The aim of this study was to compare T2 inflammatory biomarkers from middle meatal (MM) mucus for distinguishing patients with CRS from CRS-free patients, identifying major phenotypes (CRS without nasal polyps [CRSsNP] and CRS with nasal polyps [CRSwNP]), assessing endotypic change, and establishing cross-sectional and longitudinal outcomes in patients undergoing ESS. Methods: MM mucus samples were collected from patients with CRSsNP and patients with CRSwNP before and 6 to 12 months after ESS and compared with samples from CRS-free control patients. T2 biomarkers were evaluated both continuously and using threshold-based definitions of T2 endotype to identify relationships with patient-reported (based on the 22-Item Sinonasal Outcomes Test and Chronic Rhinosinusitis Patient-Reported Outcomes Measure) and clinician-reported (radiographic and endoscopic) severity. Linear mixed models were developed to analyze clinical variables associated with T2 biomarker levels. Results: A total of 154 patients with CRS (89 with CRSsNP and 65 with CRSwNP) were enrolled, with a mean interval of 9 months between ESS and follow-up. An analysis of pre-ESS MM mucus samples revealed elevated levels of T2 mediators in patients with CRSwNP versus in patients with CRSsNP and CRS-free controls. Temporally stable correlations between levels of IL-13 and IL-5, levels of periostin and complement 5a, and levels of eosinophil cationic protein (ECP) and eotaxin-3 were observed. On this basis and on the basis of pathologic significance, levels of IL-13, periostin and ECP were further analyzed. After ESS, levels of IL-13 and periostin decreased significantly, whereas ECP levels remained unchanged. Across pre- and post-ESS evaluation, the T2 endotype was associated with radiographic severity but did not predict outcomes. CRSwNP status and African American race were associated with higher levels of IL-13 and periostin, whereas ECP level was higher in patients undergoing extensive surgery. Conclusion: ESS decreased levels of IL-13 and periostin in the middle meatus. T2 inflammation after ESS was correlated with patient- and clinician-reported severity across phenotypes. Pre-ESS T2 inflammation did not predict post-ESS outcomes.

Original languageEnglish (US)
Pages (from-to)1292-1305
Number of pages14
JournalJournal of Allergy and Clinical Immunology
Volume153
Issue number5
DOIs
StatePublished - May 2024

Funding

Supported by the National Institutes of Health (grants R01 AI134952, R01 DC016645, and T32 AI083216), the National Institutes of Health's National Center for Advancing Translational Sciences (grant UL1TR001422), and the Chronic Rhinosinusitis Integrative Studies Program 2 (grant P01 AI145818). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Keywords

  • CRSsNP
  • CRSwNP
  • Chronic rhinosinusitis
  • biomarker
  • endotype
  • nasal polyps
  • patient-reported outcome measures

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology

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