Microbiome of Affected and Unaffected Skin of Patients With Atopic Dermatitis Before and After Emollient Treatment

November 2014 | Volume 13 | Issue 11 | Original Article | 1365 | Copyright © November 2014


Gilberto E. Flores PhD,a Sophie Seité PhD,b Jessica B. Henley MS,c Richard Martin MS Ing,d
Hana Zelenkova MD,e Luc Aguilar PhD,f Noah Fierer PhDa,c

aDepartment of Biology, California State University, Northridge, CA,USA
bLa Roche-Posay Pharmaceutical Laboratories, Asnières, France
cCooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, USA
dL’Oréal Research and Innovation, Tours, France
eDOST, Private Clinic of Dermatovenerology, Svidnik, Slovakia
fL’Oréal Research and Innovation, Aulnay-sous-Bois, France

Abstract
Atopic dermatitis (AD) is a chronic inflammatory skin disorder that results in areas of dry, itchy skin. Several cultivation-dependent and –independent studies have identified changes in the composition of microbial communities in these affected areas over time and when compared to healthy control individuals. However, how these communities vary on affected and unaffected skin of the same individual, and how these communities respond to emollient treatment, remains poorly understood. Here we characterized the microbial communities associated with affected and unaffected skin of 49 patients with AD before and after emollient treatment using high-throughput sequencing of the 16S rRNA gene. We found that microbial diversity and community composition was different between affected and unaffected skin of AD patients prior to treatment. Differences were driven primarily by the overabundance of Staphylococcus species on affected skin and a corresponding decrease in bacterial diversity. After 84-days of emollient treatment, the clinical symptoms of AD improved in 72% of the study population. Microbial communities associated with affected skin of these treatment responders more closely resembled unaffected skin after treatment as indicated by increased overall diversity and a decrease in the abundance of Staphylococcus species. Interestingly, Stenotrophomonas species were significantly more abundant in the communities of ‘responders’, suggesting a possible role in restoration of the skin microbiome in patients with AD. We demonstrated that the comparison of affected and unaffected skin from the same individual provides deeper insight into the bacterial communities involved in the skin dysbiosis associated with AD. These data support the importance of emollients in the management of AD although future studies should explore how emollients and other treatments help to restore skin dysbioses.

J Drugs Dermatol. 2014;13(11):1365-1372.

INTRODUCTION

Human skin hosts complex microbial communities whose diversity and composition vary by skin region1 and between individuals.2,3 Compositional differences between skin regions arise largely from contrasting environmental conditions of skin sites.4 Inter-individual differences in microbiome composition have been attributed to a number of factors including host demographics, host genetics, and host behavior.5 For example, the diversity of palm bacterial communities differs between genders.6 These inter- and intra-individual differences in skin bacterial communities may contribute to differences in disease susceptibility and quantifying such differences may aid in efforts to monitor changes in skin health status.7,8
Atopic dermatitis (AD) is a multifactorial, chronic inflammatory skin disorder with several genetic risk factors and environmental triggers.9,10 One of the hallmark symptoms of AD is dry skin (xerosis), which affects not only lesional (affected) skin, but also non-lesional (unaffected) skin.11 Xerosis is linked to skin barrier dysfunction and is usually accompanied by pruritus (itching), which may favor the penetration of allergens, bacteria, and/or viruses.12 Indeed, AD patients experience a higher frequency of bacterial skin infections with Staphylococcus aureus being the most commonly cultured organism.12,13,14
A recent cultivation-independent study confirmed the association of S. aureus with AD lesions but also revealed dramatic, community-level changes within patients over time, with treatment, and when compared to healthy individuals.15 For example, disease exacerbations were associated with a decrease in microbial diversity on lesional skin due to Staphylococcus blooms, with this genus accounting for up to 90% of the bacteria detected. In contrast, another study using both cultivation-dependent and cultivation-independent techniques found a gammaproteobacterial species, Stenotrophomonas maltophilia, to be significantly more abundant on AD patients than on other healthy individuals.16 Given these conflicting results and that each individual