Temporal and Racial Differences Associated with Atopic Dermatitis Staphylococcusaureus and Encoded Virulence Factors

Joseph A Merriman, Elizabeth A Mueller, Michael P Cahill, Lisa A Beck, Amy S Paller, Jon M Hanifin, Peck Y Ong, Lynda Schneider, Denise C Babineau, Gloria David, Alexandre Lockhart, Keli Artis, Donald Y M Leung, Patrick M Schlievert, Joseph A Merriman, Elizabeth A Mueller, Michael P Cahill, Lisa A Beck, Amy S Paller, Jon M Hanifin, Peck Y Ong, Lynda Schneider, Denise C Babineau, Gloria David, Alexandre Lockhart, Keli Artis, Donald Y M Leung, Patrick M Schlievert

Abstract

Atopic dermatitis (AD) is an inflammatory skin condition strongly associated with Staphylococcus aureus colonization and infection. S. aureus strains shift in populations in ~10-year intervals depending on virulence factors. Shifts in S. aureus virulence factors may in part explain the racial differences observed in the levels of prevalence and severity of AD. AD S. aureus isolates collected from 2011 to 2014 (103 isolates) and in 2008 (100 isolates) were examined for the prevalence of genes encoding superantigens (SAgs). The strains from 2011 to 2014 were obtained from AD patients as a part of the National Institute of Allergy and Infectious Diseases (NIAID) Atopic Dermatitis Research Network (ADRN). The prevalence of SAg genes was investigated temporally and racially. The enterotoxin gene cluster (EGC) was more prevalent in the 2011-2014 AD isolates than in the 2008 AD isolates. The prevalences of virulence factor genes were similar in European American (EA) and Mexican American (MA) patients but differed in 6 of 22 SAg genes between EA and African American (AA) or MA and AA isolates; notably, AA isolates lacked tstH, the gene encoding toxic shock syndrome toxin 1 (TSST-1). The presence of tstH and sel-p (enterotoxin-like P) was associated with decreased clinical severity and increased blood eosinophils, respectively. The EGC is becoming more prevalent, consistent with the previously observed 10 years of cycling of S. aureus strains. Race-specific S. aureus selection may account for differences in virulence factor profiles. The lack of TSST-1-positive (TSST-1+) AD S. aureus in AA is consistent with the lack of AAs acquiring TSST-1-associated menstrual toxic shock syndrome (TSS). IMPORTANCE Monitoring pathogen emergence provides insight into how pathogens adapt in the human population. Secreted virulence factors, important contributors to infections, may differ in a manner dependent on the strain and host. Temporal changes of Staphylococcus aureus toxigenic potential, for example, in encoding toxic shock syndrome toxin 1 (TSST-1), contributed to an epidemic of TSS with significant health impact. This study monitored changes in atopic dermatitis (AD) S. aureus isolates and demonstrated both temporal and host infection differences according to host race based on secreted superantigen potential. The current temporal increase in enterotoxin gene cluster superantigen prevalence and lack of the gene encoding TSST-1 in AAs predict differences in infection types and presentations.

Keywords: Staphylococcus aureus; atopic dermatitis; clonal groups; phenotype; race; superantigens.

Figures

FIG 1
FIG 1
Probability of superantigen for a given S. aureus genotype. The table component of the figure displays the probability of each S. aureus genotype within each racial group.
FIG 2
FIG 2
Prevalence of superantigen (SAg) genes in S. aureus isolates from 2011 to 2014 within each racial group. Horizontal lines indicate comparisons that are statistically significant at the 0.05 level.

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