Are Host Genetics the Predominant Determinant of Persistent Nasal<i>Staphylococcus aureus</i>Carriage in Humans?

Ruimy, Raymond; Angebault, Cécile; Djossou, Félix; Dupont, Claire; Epelboin, Loïc; Jarraud, Sophie; Lefèvre, Lise; Bes, Michèle; Lixandru, Brânduşa Elena; Bertine, Mélanie; Miniai, Assiya El; Renard, Magaly; Bettinger, Régis Marc; Lescat, Mathilde; Clermont, Olivier; Peroz, Gilles; Lina, Gérard; Tavakol, Mehri; Vandenesch, François; Belkum, Alex van; Rousset, François; Andremont, Antoine

doi:10.1086/655901

Cited by 135 publications

(117 citation statements)

References 49 publications

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“…The volunteers enrolled in the study were healthy adult Wayampi Amerindians from the village of Trois-Sauts, in French Guyana, where huts with no modern facilities are disseminated over ϳ3 km along the Oyapok river. Their living conditions and microbiological follow-up since 2001 has been extensively described elsewhere (9)(10)(11)(12)(13). This is a genetically homogenous population of ϳ500 inhabitants, still living mostly in a traditional manner, including alimentation, which is provided by hunting, fishing, and raising crops.…”

Section: Methodsmentioning

confidence: 99%

“…However, a resident paramedic ensures fully free access to allopathic medicine and records all health care deliveries, including antibiotics. During the last sampling campaign, which took place in October 2010, we tested 151 individuals for E-ESBL intestinal carriage, as described previously (9,11,13). In addition, a fecal sample of about 5 g that had recently passed (less than 2 h earlier) was diluted 1:10 in RNAlater (Applied Biosystems, Villebon-sur-Yvette, France), thoroughly mixed, and immediately frozen at Ϫ20°C before being taken to the laboratory, without defrosting, and stored at Ϫ80°C until harvesting.…”

Section: Methodsmentioning

confidence: 99%

“…The data on antibiotic exposure during the year preceding sampling, demography, and living habits were collected as described previously (9,10,11,13). Epidemiological characteristics of carriers and noncarrier controls were compared using the permutation Student t test for quantitative variables and the binomial exact test for paired data in cases of qualitative variables (24).…”

Section: Methodsmentioning

confidence: 99%

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Carriage of Enterobacteria Producing Extended-Spectrum β-Lactamases and Composition of the Gut Microbiota in an Amerindian Community

Gosalbes

Angebault

Woerther

et al. 2016

Antimicrob Agents Chemother

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c Epidemiological and individual risk factors for colonization by enterobacteria producing extended-spectrum beta-lactamases (E-ESBL) have been studied extensively, but whether such colonization is associated with significant changes in the composition of the rest of the microbiota is still unknown. To address this issue, we assessed in an isolated Amerindian Guianese community whether intestinal carriage of E-ESBL was associated with specificities in gut microbiota using metagenomic and metatranscriptomic approaches. While the richness of taxa of the active microbiota of carriers was similar to that of noncarriers, the taxa were less homogeneous. In addition, species of four genera, Desulfovibrio, Oscillospira, Parabacteroides, and Coprococcus, were significantly more abundant in the active microbiota of noncarriers than in the active microbiota of carriers, whereas such was the case only for species of Desulfovibrio and Oscillospira in the total microbiota. Differential genera in noncarrier microbiota could either be associated with resistance to colonization or be the consequence of the colonization by E-ESBL.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Carriage of Enterobacteria Producing Extended-Spectrum β-Lactamases and Composition of the Gut Microbiota in an Amerindian Community

Gosalbes

Angebault

Woerther

et al. 2016

Antimicrob Agents Chemother

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“…While it is clear that host genetics, immune responses, and strain differences contribute (12)(13)(14)(15)(16)(17), there are likely other important factors. As the anterior nares appear to be a critical S. aureus reservoir (1,18,19) and because antecedent nasal carriage increases the risk for infection (1,20,21), a better understanding of nasal microbial ecology may yield valuable clues regarding SSTI susceptibility.…”

mentioning

confidence: 99%

Correlation between Nasal Microbiome Composition and Remote Purulent Skin and Soft Tissue Infections

et al. 2015

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The incidence of skin and soft tissue infections (SSTIs) has increased dramatically over the past decade, resulting in significant morbidity in millions of otherwise healthy individuals worldwide. Certain groups, like military personnel, are at increased risk for SSTI development. Although nasal colonization with Staphylococcus aureus is an important risk factor for the development of SSTIs, it is not clear why some colonized individuals develop disease while others do not. Recent studies have revealed the importance of microbial diversity in human health. Therefore, we hypothesized that the nasal microbiome may provide valuable insight into SSTI development. To examine this hypothesis, we obtained anterior-naris samples from military trainees with cutaneous abscesses and from asymptomatic (non-SSTI) participants. We also obtained samples from within abscess cavities. Specimens were analyzed by culture, and the microbial community within each sample was characterized using a 16S sequencingbased approach. We collected specimens from 46 non-SSTI participants and from 40 participants with abscesses. We observed a significantly higher abundance of Proteobacteria in the anterior nares in non-SSTI participants (P < 0.0001) than in participants with abscesses. Additionally, we noted a significant inverse correlation between Corynebacterium spp. and S. aureus (P ‫؍‬ 0.0001). The sensitivity of standard microbiological culture for abscesses was 71.4%. These data expand our knowledge of the complexity of the nasal and abscess microbiomes and potentially pave the way for novel therapeutic and prophylactic countermeasures against SSTI. Staphylococcus aureus is a leading pathogen in both community and hospital settings. Infections with S. aureus range from invasive disease such as bacteremia and pneumonia to generally less severe skin and soft tissue infections (SSTIs) (1-3). SSTIs, especially those caused by USA300 methicillin-resistant Staphylococcus aureus (MRSA), have emerged as a common, burdensome, and costly disease (4-6). Individuals in congregate settings (e.g., members of athletic teams, prison inmates, and military trainees) are at increased risk for SSTI (7-10).Given that approximately one-third of people may exhibit S. aureus carriage, it is unclear why some develop SSTI while others do not (11). While it is clear that host genetics, immune responses, and strain differences contribute (12-17), there are likely other important factors. As the anterior nares appear to be a critical S. aureus reservoir (1, 18, 19) and because antecedent nasal carriage increases the risk for infection (1, 20, 21), a better understanding of nasal microbial ecology may yield valuable clues regarding SSTI susceptibility.The anterior nares are a dynamic microbial battleground between pathogens and commensals (22,23). The concept that changes in the host microbiome may influence human health is well documented (24); however, few studies have investigated how the nasal microbiome is altered in response to human disease (25,26). Importantl...

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“…In addition, patients colonized with Esp-secreting S. epidermidis correlated with absence of S. aureus in the nasal cavity (7). One study observed that single nucleotide polymorphisms (SNPs) in C-reactive protein and interleukin 4 (IL-4) genes correlated with S. aureus nasal colonization (8), whereas another found a correlation with SNPs in the glucocorticoid receptor gene (9).…”

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confidence: 99%

Clearance of Staphylococcus aureus Nasal Carriage Is T Cell Dependent and Mediated through Interleukin-17A Expression and Neutrophil Influx

2013

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The anterior nares of humans are the major reservoir for Staphylococcus aureus colonization. Approximately 20% of the healthy human population is persistently and 80% is intermittently colonized with S. aureus in the nasal cavity. Previous studies have shown a strong causal connection between S. aureus nasal carriage and increased risk of nosocomial infection, as well as increased carriage due to immune dysfunction. However, the immune responses that permit persistence or mediate clearance of S. aureus on the nasal mucosa are fundamentally undefined. In this study, we developed a carriage model in C57BL/6J mice and showed that clearance begins 14 days postinoculation. In contrast, SCID mice that have a deficient adaptive immune response are unable to eliminate S. aureus even after 28 days postinoculation. Furthermore, decolonization was found to be T cell mediated but B cell independent by evaluating carriage clearance in T-cell receptor ␤/␦ (TCR-␤/␦) knockout (KO) and IgH-KO mice, respectively. Upregulation of the cytokines interleukin 1␤ (IL-1␤), KC (also termed CXC ligand 1 [CXCL1]), and IL-17A occurred following inoculation with intranasal S. aureus. IL-17A production was crucial for clearance, since IL-17A-deficient mice were unable to effectively eliminate S. aureus carriage. Subsequently, cell differential counts were evaluated from nasal lavage fluid obtained from wild-type and IL-17A-deficient colonized mice. These counts displayed IL-17A-dependent neutrophil migration. Antibody-mediated depletion of neutrophils in colonized mice caused reduced clearance compared to that in isotypetreated controls. Our data suggest that the Th17-associated immune response is required for nasal decolonization. This response is T cell dependent and mediated via IL-17A production and neutrophil influx. Th17-associated immune responses may be targeted for strategies to mitigate distal infections originating from persistent S. aureus carriage in humans.

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Are Host Genetics the Predominant Determinant of Persistent NasalStaphylococcus aureusCarriage in Humans?

Abstract: Host genetic factors appeared to be the predominant determinant for S. aureus persistent nasal carriage in humans.

Cited by 135 publications

References 49 publications

Carriage of Enterobacteria Producing Extended-Spectrum β-Lactamases and Composition of the Gut Microbiota in an Amerindian Community

Carriage of Enterobacteria Producing Extended-Spectrum β-Lactamases and Composition of the Gut Microbiota in an Amerindian Community

Correlation between Nasal Microbiome Composition and Remote Purulent Skin and Soft Tissue Infections

Clearance of Staphylococcus aureus Nasal Carriage Is T Cell Dependent and Mediated through Interleukin-17A Expression and Neutrophil Influx

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