Chronic rhinosinusitis patients display an aberrant immune cell localization with enhanced S aureus biofilm metabolic activity and biomass

Date

2023

Authors

Shaghayegh, G.
Cooksley, C.
Bouras, G.S.
Panchatcharam, B.S.
Idrizi, R.
Jana, M.
Ellis, S.
Psaltis, A.J.
Wormald, P.J.
Vreugde, S.

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Journal article

Citation

Journal of Allergy and Clinical Immunology, 2023; 151(3):723-736.e16

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Gohar Shaghayegh, Clare Cooksley, George Spyro Bouras, Beula Subashini Panchatcharam, Rejhan Idrizi, Metta Jana, Sarah Ellis, Alkis James Psaltis, Peter-John Wormald, and Sarah Vreugde

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Abstract

Background: Chronic rhinosinusitis (CRS) is a persistent inflammation of the sinus mucosa associated with dysfunction of the sinuses’ natural defense mechanism and induction of different inflammatory clusters. Severe recalcitrant CRS is unresponsive to medical and surgical interventions and often has Staphylococcus aureus–dominant mucosal biofilms. Objectives: This study aimed to characterize in vitro grown S aureus biofilm properties in relation to inflammation and CRS severity. The spatial pattern of inflammatory cells in patients’ sinonasal tissue was also examined. Methods: S aureus isolated from the nasal swabs of patients with CRS with nasal polyps (CRSwNP), those with CRS without nasal polyps, and controls (n 5 72) were grown into biofilm in vitro, and their metabolic activity, biomass, colony-forming units, and exoprotein production were quantified. S aureus virulence genes were evaluated using whole-genome sequencing. Patients’ matched sinonasal tissue blocks (n 5 57) were analyzed using Opal multiplex immunostaining, and their disease severity was determined using the Lund-Mackay computed tomography score. Correlations among S aureus biofilm properties, the frequency and localization of key immune cells in corresponding sinonasal mucosa, and the disease severity were investigated. Results: Increased infiltration of CD31, CD681, CD201, and CD1381 cells was observed in tissue of patients with CRSwNP compared to tissue from controls. CD31, CD1381, and MBP1 cells diffused deeper into the tissue in CRSwNP but clustered close to the epithelium in controls. This study also found CRSwNP–derived S aureus biofilms showed thicker biomass, higher colony-forming units, and higher exoprotein production than those from controls did (P < .05). S aureus biofilm properties, inflammatory cell numbers, and CRS severity scores were positively correlated. Conclusions: These findings support the notion of an aberrant immunolocalization of key immune cells in CRSwNP with a critical role of S aureus biofilms in CRS etiopathogenesis.

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Available online October 28, 2022.

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© 2022 American Academy of Allergy, Asthma & Immunology

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