Nasal microbiome disruption and recovery after mupirocin treatment in Staphylococcus aureus carriers and noncarriers

Abstract

Nasal decolonization procedures against the opportunistic pathogen Staphylococcus aureus rely on topical antimicrobial drug usage, whose impact on the nasal microbiota is poorly understood. We examined this impact in healthy S. aureus carriers and noncarriers. This is a prospective interventional cohort study of 8 S. aureus carriers and 8 noncarriers treated with nasal mupirocin and chlorhexidine baths. Sequential nasal swabs were taken over 6 months. S. aureus was detected by quantitative culture and genotyped using spa typing. RNA-based 16S species-level metabarcoding was used to assess the living microbial diversity. The species Dolosigranulum pigrum, Moraxella nonliquefaciens and Corynebacterium propinquum correlated negatively with S. aureus carriage. Mupirocin treatment effectively eliminated S. aureus, D. pigrum and M. nonliquefaciens, but not corynebacteria. S. aureus recolonization in carriers occurred more rapidly than recolonization by the dominant species in noncarriers (median 3 vs. 6 months, respectively). Most recolonizing S. aureus isolates had the same spa type as the initial isolate. The impact of mupirocin-chlorhexidine treatment on the nasal microbiota was still detectable after 6 months. S. aureus recolonization predated microbiota recovery, emphasizing the strong adaptation of this pathogen to the nasal niche and the transient efficacy of the decolonization procedure.

Dolosigranulum pigrum: A promising nasal probiotic candidate

“…Deriving its name from the Latin words dolosus (“crafty, deceitful”), granulum (“a small grain”), and pigrum (“lazy”), D. pigrum (phylum: Firmicutes, class: Bacilli, order: Lactobacillales, family: Carnobacteriaceae) is a gram-positive, lactic acid bacterium that was first described by Aguirre and colleagues in 1993 [ 3 ]. It is non-spore-forming, facultatively anaerobic, catalase-negative, and generally susceptible to beta-lactams, clindamycin, and other commonly used antibiotics [ 4 , 5 ]. D. pigrum is the only recognized species within the genus Dolosigranulum .…”

“…D. pigrum may also influence the outcome of efforts to decolonize Staphylococcus aureus carriers. Use of nasal mupirocin can eliminate both Staphylococcus aureus and D. pigrum from the nasal microbiota, while recolonization with Staphylococcus aureus after stopping mupirocin is associated with delayed recolonization by D. pigrum [ 4 ]. Several cross-sectional studies also reported lower relative abundances of D. pigrum among children colonized by Streptococcus pneumoniae , a bacterial pathobiont that is among the most common bacterial causes of pneumonia, acute otitis media, and acute bacterial rhinosinusitis [ 20 , 29 ].…”

“…Moreover, D. pigrum has been associated with the absence of URT colonization by bacterial respiratory pathobionts. Most notably, lower relative abundances of D. pigrum are found in the nasal cavities of AU : PleasenotethatgenusStaphylococcushasbeenaddedtoStaphylococcusaureusasitsbinomial Staphylococcus aureus carriers [4,[24][25][26][27], and a prospective study found that higher nasal abundances of D. pigrum were associated with a lower risk of Staphylococcus aureus acquisition during infancy [28]. D. pigrum may also influence the outcome of efforts to decolonize Staphylococcus aureus carriers.…”