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Original Investigation |

The Presence and Impact of Biofilm-Producing Staphylococci in Atopic Dermatitis

Herbert B. Allen, MD1; Nachiket D. Vaze, BS2; Catherine Choi, MD1; Tesfu Hailu, MD1; Brittain H. Tulbert, MD1; Carrie A. Cusack, MD1; Suresh G. Joshi, MD, PhD1,2
[+] Author Affiliations
1Department of Dermatology, Drexel University College of Medicine, Philadelphia, Pennsylvania
2Surgical Infections Research and Bacterial Pathogenesis Program, Drexel University College of Medicine, Philadelphia, Pennsylvania
JAMA Dermatol. 2014;150(3):260-265. doi:10.1001/jamadermatol.2013.8627.
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Importance  Atopic dermatitis (AD) is thought to be a double-hit phenomenon with an unknown environmental component and a genetic abnormality likely centered on the filaggrin gene. Biologically, the presence of Staphylococcus aureus in AD was reported more than 2 decades ago, but the relationship to AD has been elusive.

Objective  To explore the bacteria that produce the biofilms in the lesions of AD and the response of the innate immune system to these biofilm occlusions of the sweat ducts by specifically evaluating Toll-like receptor 2.

Design, Setting, and Participants  University hospital dermatologic clinic study involving the environmental component related to the characterization, correlation, and impact of staphylococci and their biofilms in AD. We processed routine skin swabs from lesional and nonlesional skin from 40 patients with AD and performed scrapings and biopsies. We also obtained 20 samples from controls (10 inflamed skin samples and 10 normal skin samples).

Exposures  Gram staining, bright-field microscopy, hematoxylin and eosin, periodic acid–Schiff, Congo red, and light microscopy.

Main Outcomes and Measures  Association of staphylococcal biofilms with AD pathogenesis.

Results  All AD-affected samples contained multidrug-resistant staphylococci, with S aureus (42.0%) and Staphylococcus epidermidis (20.0%) as the predominant species. All isolates were positive for extracellular polysaccharide and biofilm (85.0% strong biofilm producers and 15.0% moderately to weakly positive). Polymerase chain reaction revealed the biofilm-mediating icaD (93.0%) and aap (12.5%) genes in the isolates (some contained both). We also examined tissues for microbial identification, extracellular biomass formation, biofilm formation, and staphylococcal biofilm in skin tissues. Occlusion of sweat ducts with periodic acid–Schiff–positive and Congo red–positive material was noted on microscopic tissue examination. Toll-like receptor 2 was shown to be activated in AD lesional skin (immediately proximal to the sweat ducts), which likely led to the initiation of proteinase-activated receptor 2–mediated pruritus and MyD88-mediated spongiosis.

Conclusions and Relevance  Biofilm formation by AD-associated staphylococci almost certainly plays a major role in the occlusion of sweat ducts and leads to inflammation and pruritus. We believe the environmental hit in AD relates to staphylococci and their biofilms, which occlude sweat ducts.

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Figures

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Figure 1.
Flexural Eczema

Eczema may present in the antecubitals.

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Figure 2.
Blood Agar Plate

Almost uniform and pure growth of coagulase-negative staphylococci was seen when a swab from the area affected by atopic dermatitis was cultured.

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Figure 3.
Biopsy Specimen

Specimen shows an occlusion that stained positively for Congo red in the acrosyringium, along with spongiosis and early vesicle formation. Thirty-six of 36 lesional specimens showed Congo red within the ducts (original magnification ×40).

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Figure 4.
Skin Biopsy Specimen Stained for Immunopathologic Analysis

A, Activation of Toll-like receptor 2 (TLR2) in the stratum corneum adjacent to occluded sweat ducts. B, Control location for TLR2 is in the basal layer of the epidermis. Both immunostained with CD 282 immunoperoxidase for TLR2 (original magnification ×40).

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