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Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home

BACKGROUND: Nursing home residents have increased rates of intestinal colonisation with multidrug-resistant organisms (MDROs). We assessed the colonisation and spread of MDROs among this population, determined clinical risk factors for MDRO colonisation and investigated the role of the gut microbiot...

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Autores principales: Ducarmon, Quinten R., Terveer, Elisabeth M., Nooij, Sam, Bloem, Michelle N., Vendrik, Karuna E. W., Caljouw, Monique A. A., Sanders, Ingrid M. J. G., van Dorp, Sofie M., Wong, Man C., Zwittink, Romy D., Kuijper, Ed J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8028076/
https://www.ncbi.nlm.nih.gov/pubmed/33827686
http://dx.doi.org/10.1186/s13073-021-00869-z
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author Ducarmon, Quinten R.
Terveer, Elisabeth M.
Nooij, Sam
Bloem, Michelle N.
Vendrik, Karuna E. W.
Caljouw, Monique A. A.
Sanders, Ingrid M. J. G.
van Dorp, Sofie M.
Wong, Man C.
Zwittink, Romy D.
Kuijper, Ed J.
author_facet Ducarmon, Quinten R.
Terveer, Elisabeth M.
Nooij, Sam
Bloem, Michelle N.
Vendrik, Karuna E. W.
Caljouw, Monique A. A.
Sanders, Ingrid M. J. G.
van Dorp, Sofie M.
Wong, Man C.
Zwittink, Romy D.
Kuijper, Ed J.
author_sort Ducarmon, Quinten R.
collection PubMed
description BACKGROUND: Nursing home residents have increased rates of intestinal colonisation with multidrug-resistant organisms (MDROs). We assessed the colonisation and spread of MDROs among this population, determined clinical risk factors for MDRO colonisation and investigated the role of the gut microbiota in providing colonisation resistance against MDROs. METHODS: We conducted a prospective cohort study in a Dutch nursing home. Demographical, epidemiological and clinical data were collected at four time points with 2-month intervals (October 2016–April 2017). To obtain longitudinal data, faecal samples from residents were collected for at least two time points. Ultimately, twenty-seven residents were included in the study and 93 faecal samples were analysed, of which 27 (29.0%) were MDRO-positive. Twelve residents (44.4%) were colonised with an MDRO at at least one time point throughout the 6-month study. RESULTS: Univariable generalised estimating equation logistic regression indicated that antibiotic use in the previous 2 months and hospital admittance in the previous year were associated with MDRO colonisation. Characterisation of MDRO isolates through whole-genome sequencing revealed Escherichia coli sequence type (ST)131 to be the most prevalent MDRO and ward-specific clusters of E. coli ST131 were identified. Microbiota analysis by 16S rRNA gene amplicon sequencing revealed no differences in alpha or beta diversity between MDRO-positive and negative samples, nor between residents who were ever or never colonised. Three bacterial taxa (Dorea, Atopobiaceae and Lachnospiraceae ND3007 group) were more abundant in residents never colonised with an MDRO throughout the 6-month study. An unexpectedly high abundance of Bifidobacterium was observed in several residents. Further investigation of a subset of samples with metagenomics showed that various Bifidobacterium species were highly abundant, of which B. longum strains remained identical within residents over time, but were different between residents. CONCLUSIONS: Our study provides new evidence for the role of the gut microbiota in colonisation resistance against MDROs in the elderly living in a nursing home setting. Dorea, Atopobiaceae and Lachnospiraceae ND3007 group may be associated with protection against MDRO colonisation. Furthermore, we report a uniquely high abundance of several Bifidobacterium species in multiple residents and excluded the possibility that this was due to probiotic supplementation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13073-021-00869-z.
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spelling pubmed-80280762021-04-08 Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home Ducarmon, Quinten R. Terveer, Elisabeth M. Nooij, Sam Bloem, Michelle N. Vendrik, Karuna E. W. Caljouw, Monique A. A. Sanders, Ingrid M. J. G. van Dorp, Sofie M. Wong, Man C. Zwittink, Romy D. Kuijper, Ed J. Genome Med Research BACKGROUND: Nursing home residents have increased rates of intestinal colonisation with multidrug-resistant organisms (MDROs). We assessed the colonisation and spread of MDROs among this population, determined clinical risk factors for MDRO colonisation and investigated the role of the gut microbiota in providing colonisation resistance against MDROs. METHODS: We conducted a prospective cohort study in a Dutch nursing home. Demographical, epidemiological and clinical data were collected at four time points with 2-month intervals (October 2016–April 2017). To obtain longitudinal data, faecal samples from residents were collected for at least two time points. Ultimately, twenty-seven residents were included in the study and 93 faecal samples were analysed, of which 27 (29.0%) were MDRO-positive. Twelve residents (44.4%) were colonised with an MDRO at at least one time point throughout the 6-month study. RESULTS: Univariable generalised estimating equation logistic regression indicated that antibiotic use in the previous 2 months and hospital admittance in the previous year were associated with MDRO colonisation. Characterisation of MDRO isolates through whole-genome sequencing revealed Escherichia coli sequence type (ST)131 to be the most prevalent MDRO and ward-specific clusters of E. coli ST131 were identified. Microbiota analysis by 16S rRNA gene amplicon sequencing revealed no differences in alpha or beta diversity between MDRO-positive and negative samples, nor between residents who were ever or never colonised. Three bacterial taxa (Dorea, Atopobiaceae and Lachnospiraceae ND3007 group) were more abundant in residents never colonised with an MDRO throughout the 6-month study. An unexpectedly high abundance of Bifidobacterium was observed in several residents. Further investigation of a subset of samples with metagenomics showed that various Bifidobacterium species were highly abundant, of which B. longum strains remained identical within residents over time, but were different between residents. CONCLUSIONS: Our study provides new evidence for the role of the gut microbiota in colonisation resistance against MDROs in the elderly living in a nursing home setting. Dorea, Atopobiaceae and Lachnospiraceae ND3007 group may be associated with protection against MDRO colonisation. Furthermore, we report a uniquely high abundance of several Bifidobacterium species in multiple residents and excluded the possibility that this was due to probiotic supplementation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13073-021-00869-z. BioMed Central 2021-04-07 /pmc/articles/PMC8028076/ /pubmed/33827686 http://dx.doi.org/10.1186/s13073-021-00869-z Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ducarmon, Quinten R.
Terveer, Elisabeth M.
Nooij, Sam
Bloem, Michelle N.
Vendrik, Karuna E. W.
Caljouw, Monique A. A.
Sanders, Ingrid M. J. G.
van Dorp, Sofie M.
Wong, Man C.
Zwittink, Romy D.
Kuijper, Ed J.
Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home
title Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home
title_full Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home
title_fullStr Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home
title_full_unstemmed Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home
title_short Microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a Dutch nursing home
title_sort microbiota-associated risk factors for asymptomatic gut colonisation with multi-drug-resistant organisms in a dutch nursing home
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8028076/
https://www.ncbi.nlm.nih.gov/pubmed/33827686
http://dx.doi.org/10.1186/s13073-021-00869-z
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