Gut microbiome diversity and composition in individuals with and without extended-spectrum β-lactamase-producing Enterobacterales carriage: a matched case–control study in infectious diseases department

Boyd, Anders; El Dani, Mariam; Ajrouche, Roula; Demontant, Vanessa; Cheval, Justine; Lacombe, Karine; Cosson, Guillaume; Rodriguez, Christophe; Pawlotsky, Jean-Michel; Woerther, Paul-Louis; Surgers, Laure

doi:10.1016/j.cmi.2024.03.016

Cited by 4 publications

(2 citation statements)

References 37 publications

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“…Therefore, sampling quality and strategy are key in conducting studies aiming to investigate the gut microbiome. In a study performed by Boid et al [25], only swabs with visible fecal matter were included, and their results showed that ESBL acquisition did not affect the diversity or overall structure of the microbiome, which is consistent with our results in which we did not observe a major impact of MDRO acquisition or loss on the microbiome.…”

Section: Discussionsupporting

confidence: 92%

Towards unraveling antimicrobial resistance dynamics: A longitudinal exploration of rectal swab metagenomes

Boutin,

Käding,

Belheouane

et al. 2024

Preprint

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The increasing prevalence of antimicrobial resistance (AMR) poses significant challenges in clinical settings. In particular, early screening and detection of colonization by multidrug-resistant organisms (MDROs) in patients at admission is crucial. In this context, the clinical use of metagenomics (mNGS) holds promise for fast and untargeted diagnostic methods. Here, we aimed to evaluate the long-term stability of the rectal microbiome and the diagnostic accuracy of mNGS in comparison to culture and whole-genome sequencing (WGS) of MDROs. We analyzed rectal swabs from 26 patients with two consecutive admissions over a four-year period. The detected antimicrobial resistance genes and assembled metagenomes were compared to those obtained via classical culture-based antimicrobial susceptibility testing and WGS of isolated MDROs. Our results showed that the rectal microbiome is variable during the two timepoints, with a β-diversity greater in magnitude than what is currently known for the gut microbiome, highlighting the variability in the niche. Nevertheless, we also observed strong co-occurrence of taxa, suggesting that the rectal swab microbiome is also a regulated niche with cooperative biotic interactions. In total, we isolated and sequenced 6 MDROs from 6 patients at individual timepoints. Almost all AMR genes from the genomes of the isolates (median: 100%, range: 84.6-100%) could be detected by mNGS of the rectal swabs. Thus, in patients with positive cultures, we could not detect the isolated MDRO species or associated AMR genes at all screening visits. In addition, we detected AMR genes and pathogenic species in patients with negative cultures. In conclusion, our study showed that, in principle, mNGS of rectal swabs can detect clinically relevant AMR profiles. However, the cooccurrence of AMR genes and pathogenic species does not always correlate with culture-based diagnostic results but rather indicates a potential risk of horizontal AMR gene transfer. However, it is unclear whether the observed discrepancies are due to transient or locally confined colonization of MDROs, limits of detection, or variability of the sampling method and specimens.

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Section: Discussionsupporting

confidence: 92%

Towards unraveling antimicrobial resistance dynamics: A longitudinal exploration of rectal swab metagenomes

Boutin,

Käding,

Belheouane

et al. 2024

Preprint

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“…Davies et al conducted a point-prevalence metagenomics study on fecal samples from international travelers before and after travel, observed changes in the microbiome composition during travel, and found that these changes were primarily associated with the development of travelers' diarrhea rather than the acquisition of ESBL-producing E. coli [33]. In another study, no differences were found in the diversity parameters or relative abundance of bacterial species in the gut microbiome between healthy individuals, who were colonized or not colonized with ESBL-producing E. coli [34]. Recently, Ducarmon et al analyzed the potential role of the gut microbiome in controlling the colonization of ESBL-producing E. coli, and no differences in the diversity parameters or in the relative abundance were observed between ESBL-producing E. coli and the negative groups [35].…”

Section: Discussionmentioning

confidence: 97%

The Roles of a Multidrug-Resistant Klebsiella pneumoniae High-Risk Clone and Its Resistance Plasmids on the Gastrointestinal Colonization and Host-Defense Effectors in the Gut

Stercz,

Domokos,

Dunai

et al. 2024

Antibiotics

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The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing Klebsiella pneumoniae ST15 (MDR-KP) strain, as well as Escherichia coli J53 (EC) and E. coli transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the Bacteroidota phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas Proteobacteria was dominant in EC. The Muribaculaceae family was significantly more common in the MDR-KP and EC-OXA groups, while the Lachnospiraceae family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the Muribaculaceae family members exhibited a correlation with the IncL plasmid. The detected amounts of the Lachnospiraceae family indicated the protective role against the high-risk clone and the resistance plasmids’ dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut.

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Gut microbiome and its role in the acquisition of extended-spectrum β-lactamase-producing Enterobacterales

Denkel,

Gastmeier

2024

Clinical Microbiology and Infection

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Gut microbiome diversity and composition in individuals with and without extended-spectrum β-lactamase-producing Enterobacterales carriage: a matched case–control study in infectious diseases department

Cited by 4 publications

References 37 publications

Towards unraveling antimicrobial resistance dynamics: A longitudinal exploration of rectal swab metagenomes

Towards unraveling antimicrobial resistance dynamics: A longitudinal exploration of rectal swab metagenomes

The Roles of a Multidrug-Resistant Klebsiella pneumoniae High-Risk Clone and Its Resistance Plasmids on the Gastrointestinal Colonization and Host-Defense Effectors in the Gut

Gut microbiome and its role in the acquisition of extended-spectrum β-lactamase-producing Enterobacterales

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