Shared signatures and divergence in skin microbiomes of children with atopic dermatitis and their caregivers

Abstract

Background: Atopic dermatitis (AD) is a common chronic skin condition in children (15-20%) that can significantly impair their quality of life. Due to its relapsing nature and enrichment of Staphylococcus aureus during flares, clinical management can include eradicating S. aureus from the skin of children, however this does not extend to their healthy caregivers who are potential reservoirs. Objective: Our aim was to understand skin microbiome sharing and microbial features in children with AD and their healthy adult caregivers. Methods: We utilized whole metagenome profiling at 4 body sites (volar forearm, antecubital fossae, cheeks and lesions) in combination with sequencing of S. aureus isolates to characterize a cohort of children with AD and their healthy caregivers (n = 30 families), in comparison to matched pairs from control households (n = 30 families). Results: Metagenome analysis revealed distinct microbiome configurations in the non-lesional skin of AD children and their healthy caregivers versus controls, which were sufficient to accurately predict case-control status (AUC > 0.8). These differences were accompanied by significant microbiome similarity between children and their caregivers, indicating that microbiome sharing may play a role in recurrent disease flares. Whole genome comparisons with high quality S. aureus isolate genomes (n = 55) confirmed significant strain sharing between AD children and their caregivers and AD-specific enrichment of strains expressing enterotoxins Q and K/K2. Conclusion: Our results highlight the distinctive skin microbiome features of healthy caregivers for children with AD, and support their inclusion in strategies for the treatment of recurrent paediatric AD.