Biofilm propensity of Staphylococcus aureus skin isolates is associated with increased atopic dermatitis severity and barrier dysfunction in the MPAACH pediatric cohort

• Published in: Allergy (Copenhagen) Vol. 76; no. 1; pp. 302 - 313
• Main Authors: Gonzalez, Tammy, Stevens, Mariana L., Baatyrbek kyzy, Asel, Alarcon, Rosario, He, Hua, Kroner, John W., Spagna, Daniel, Grashel, Brittany, Sidler, Elaine, Martin, Lisa J., Biagini Myers, Jocelyn M., Khurana Hershey, Gurjit K., Herr, Andrew B.
• Format: Journal Article
• Language: English
• Published: Denmark Blackwell Publishing Ltd 01.01.2021
• Subjects: Adult; Asthma; Atopic dermatitis; biofilm; Biofilms; Child; Children; Colonization; Dermatitis; Dermatitis, Atopic; Eczema; Filaggrin; Filaggrin Proteins; Gene expression; Humans; Pediatrics; Ribonucleic acid; RNA; S100A8/S100A9; Scanning electron microscopy; Skin; Skin diseases; Skin lesions; Species; Staphylococcal Infections; Staphylococcus aureus; Staphylococcus epidermidis - genetics; atopic dermatitis; S100A8/S100A9; filaggrin; Staphylococcus aureus; biofilm
• ISSN: 0105-4538; 1398-9995; 1398-9995
• DOI: 10.1111/all.14489

Background Atopic dermatitis (AD) patients are often colonized with Staphylococcus aureus, and staphylococcal biofilms have been reported on adult AD skin lesions. The commensal S epidermidis can antagonize S aureus, although its role in AD is unclear. We sought to characterize S aureus and S epidermidis colonization and biofilm propensity and determine their associations with AD severity, barrier function, and epidermal gene expression in the first US early‐life cohort of children with AD, the Mechanisms of Progression of Atopic Dermatitis to Asthma in Children (MPAACH). Methods The biofilm propensity of staphylococcal isolates was assessed by crystal violet assays. Gene expression of filaggrin and antimicrobial alarmins S100A8 and S100A9 was measured in keratinocyte RNA extracted from skin tape strips. Staphylococcal biofilms sampled from MPAACH skin were visualized using scanning electron microscopy. Results Sixty‐two percent of staphylococcal isolates (sampled from 400 subjects) formed moderate/strong biofilms. Sixty‐eight percent of subjects co‐colonized with both staphylococcal species exhibited strains that formed cooperative mixed‐species biofilms. Scanning electron microscopy verified the presence of staphylococcal biofilms on the skin of MPAACH children. Staphylococcus aureus strains showing higher relative biofilm propensity compared with S epidermidis were associated with increased AD severity (P = .03) and increased lesional and nonlesional transepidermal water loss (P = .01, P = .03). Conclusions Our data suggest a pathogenic role for S aureus biofilms in AD. We found that strain‐level variation in staphylococcal isolates governs the interactions between S epidermidis and S aureus and that the balance between these two species, and their biofilm propensity, has important implications for AD. Staphylococcal biofilms are observed on the skin of children with AD in the MPAACH cohort. Staphylococcus aureus strains showing higher relative biofilm propensity (compared with S epidermidis from the same subject) are associated with increased AD severity. Staphylococcus aureus strains showing higher relative biofilm propensity are associated with increased lesional and nonlesional transepidermal water loss. Abbreviations: AD, atopic dermatitis; FLG, filaggrin; MPAACH, Mechanisms of Progression of Atopic Dermatitis to Asthma in Children; SCORAD, scoring atopic dermatitis index; S100A8, S100 Calcium‐Binding Protein A8; S100A9, Calcium‐Binding Protein A9; TEWL, transepidermal water loss.