Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients
Among long-stay critically ill patients in the adult intensive care unit (ICU), there are often marked changes in the complexity of the gut microbiota. However, it remains unclear whether such patients might benefit from enhanced surveillance or from interventions targeting the gut microbiota or the...
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| Veröffentlicht in: | Microbial genomics 2019-09, Vol.5 (9) |
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| creator | Ravi, Anuradha Halstead, Fenella D Bamford, Amy Casey, Anna Thomson, Nicholas M van Schaik, Willem Snelson, Catherine Goulden, Robert Foster-Nyarko, Ebenezer Savva, George M Whitehouse, Tony Pallen, Mark J Oppenheim, Beryl A |
| description | Among long-stay critically ill patients in the adult intensive care unit (ICU), there are often marked changes in the complexity of the gut microbiota. However, it remains unclear whether such patients might benefit from enhanced surveillance or from interventions targeting the gut microbiota or the pathogens therein. We therefore undertook a prospective observational study of 24 ICU patients, in which serial faecal samples were subjected to shotgun metagenomic sequencing, phylogenetic profiling and microbial genome analyses. Two-thirds of the patients experienced a marked drop in gut microbial diversity (to an inverse Simpson's index of |
| doi_str_mv | 10.1099/mgen.0.000293 |
| format | Article |
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. In some patients, we also saw an increase in the relative abundance of apparent commensal organisms in the gut microbiome, including the archaeal species
. In conclusion, we have documented a dramatic absence of microbial diversity and pathogen domination of the gut microbiota in a high proportion of critically ill patients using shotgun metagenomics.</description><identifier>ISSN: 2057-5858</identifier><identifier>EISSN: 2057-5858</identifier><identifier>DOI: 10.1099/mgen.0.000293</identifier><identifier>PMID: 31526447</identifier><language>eng</language><publisher>England: Microbiology Society</publisher><subject>Adult ; Aged ; Aged, 80 and over ; Anti-Bacterial Agents - pharmacology ; Anti-Bacterial Agents - therapeutic use ; Biodiversity ; Critical Illness ; Enterococcus faecium - isolation & purification ; Enterococcus faecium - physiology ; Feces - microbiology ; Female ; Gastrointestinal Microbiome - drug effects ; Humans ; Intensive Care Units ; Male ; Meropenem - pharmacology ; Meropenem - therapeutic use ; Metagenomics ; Middle Aged ; Prospective Studies</subject><ispartof>Microbial genomics, 2019-09, Vol.5 (9)</ispartof><rights>2019 The Authors 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c387t-4fa7351273c0b9b6363f1f5c084709e025faf5c18ce67e54b91791a12e8f92493</citedby><cites>FETCH-LOGICAL-c387t-4fa7351273c0b9b6363f1f5c084709e025faf5c18ce67e54b91791a12e8f92493</cites><orcidid>0000-0002-2833-2926 ; 0000-0002-4387-3421 ; 0000-0001-5832-0988 ; 0000-0003-1168-9010 ; 0000-0003-1807-3657</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6807385/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6807385/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31526447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ravi, Anuradha</creatorcontrib><creatorcontrib>Halstead, Fenella D</creatorcontrib><creatorcontrib>Bamford, Amy</creatorcontrib><creatorcontrib>Casey, Anna</creatorcontrib><creatorcontrib>Thomson, Nicholas M</creatorcontrib><creatorcontrib>van Schaik, Willem</creatorcontrib><creatorcontrib>Snelson, Catherine</creatorcontrib><creatorcontrib>Goulden, Robert</creatorcontrib><creatorcontrib>Foster-Nyarko, Ebenezer</creatorcontrib><creatorcontrib>Savva, George M</creatorcontrib><creatorcontrib>Whitehouse, Tony</creatorcontrib><creatorcontrib>Pallen, Mark J</creatorcontrib><creatorcontrib>Oppenheim, Beryl A</creatorcontrib><title>Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients</title><title>Microbial genomics</title><addtitle>Microb Genom</addtitle><description>Among long-stay critically ill patients in the adult intensive care unit (ICU), there are often marked changes in the complexity of the gut microbiota. However, it remains unclear whether such patients might benefit from enhanced surveillance or from interventions targeting the gut microbiota or the pathogens therein. We therefore undertook a prospective observational study of 24 ICU patients, in which serial faecal samples were subjected to shotgun metagenomic sequencing, phylogenetic profiling and microbial genome analyses. Two-thirds of the patients experienced a marked drop in gut microbial diversity (to an inverse Simpson's index of <4) at some stage during their stay in the ICU, often accompanied by the absence or loss of potentially beneficial bacteria. Intravenous administration of the broad-spectrum antimicrobial agent meropenem was significantly associated with loss of gut microbial diversity, but the administration of other antibiotics, including piperacillin/tazobactam, failed to trigger statistically detectable changes in microbial diversity. In three-quarters of ICU patients, we documented episodes of gut domination by pathogenic strains, with evidence of cryptic nosocomial transmission of
. In some patients, we also saw an increase in the relative abundance of apparent commensal organisms in the gut microbiome, including the archaeal species
. In conclusion, we have documented a dramatic absence of microbial diversity and pathogen domination of the gut microbiota in a high proportion of critically ill patients using shotgun metagenomics.</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Anti-Bacterial Agents - therapeutic use</subject><subject>Biodiversity</subject><subject>Critical Illness</subject><subject>Enterococcus faecium - isolation & purification</subject><subject>Enterococcus faecium - physiology</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Gastrointestinal Microbiome - drug effects</subject><subject>Humans</subject><subject>Intensive Care Units</subject><subject>Male</subject><subject>Meropenem - pharmacology</subject><subject>Meropenem - therapeutic use</subject><subject>Metagenomics</subject><subject>Middle Aged</subject><subject>Prospective Studies</subject><issn>2057-5858</issn><issn>2057-5858</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkM1qAyEUhaW0NCHNstviC0yq4zjqplBC_yDQTbsWx9HE4oxhNIG8fR3ShHR1vfidc7gHgHuMFhgJ8ditTb9AC4RQKcgVmJaIsoJyyq8v3hMwj_EnM5jyWjB6CyYE07KuKjYF7SrECIOFndNDaJzysHV7M0SXDlD1LdyqtAk5Brahc71KLvQjnjYGrnfpJAtJQddDPbjktPL-AJ33o9aZPsU7cGOVj2b-N2fg-_Xla_lerD7fPpbPq0ITzlJRWcUIxSUjGjWiqUlNLLZUI14xJAwqqVV5xVybmhlaNQIzgRUuDbeirASZgaej73bXdKbVOXtQXm4H16nhIINy8v9P7zZyHfay5ogRTrNBcTTIR8U4GHvWYiTHxuXYuETy2HjmHy4Dz_SpX_ILadd_JQ</recordid><startdate>20190901</startdate><enddate>20190901</enddate><creator>Ravi, Anuradha</creator><creator>Halstead, Fenella D</creator><creator>Bamford, Amy</creator><creator>Casey, Anna</creator><creator>Thomson, Nicholas M</creator><creator>van Schaik, Willem</creator><creator>Snelson, Catherine</creator><creator>Goulden, Robert</creator><creator>Foster-Nyarko, Ebenezer</creator><creator>Savva, George M</creator><creator>Whitehouse, Tony</creator><creator>Pallen, Mark J</creator><creator>Oppenheim, Beryl A</creator><general>Microbiology Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2833-2926</orcidid><orcidid>https://orcid.org/0000-0002-4387-3421</orcidid><orcidid>https://orcid.org/0000-0001-5832-0988</orcidid><orcidid>https://orcid.org/0000-0003-1168-9010</orcidid><orcidid>https://orcid.org/0000-0003-1807-3657</orcidid></search><sort><creationdate>20190901</creationdate><title>Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients</title><author>Ravi, Anuradha ; Halstead, Fenella D ; Bamford, Amy ; Casey, Anna ; Thomson, Nicholas M ; van Schaik, Willem ; Snelson, Catherine ; Goulden, Robert ; Foster-Nyarko, Ebenezer ; Savva, George M ; Whitehouse, Tony ; Pallen, Mark J ; Oppenheim, Beryl A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c387t-4fa7351273c0b9b6363f1f5c084709e025faf5c18ce67e54b91791a12e8f92493</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Anti-Bacterial Agents - therapeutic use</topic><topic>Biodiversity</topic><topic>Critical Illness</topic><topic>Enterococcus faecium - isolation & purification</topic><topic>Enterococcus faecium - physiology</topic><topic>Feces - microbiology</topic><topic>Female</topic><topic>Gastrointestinal Microbiome - drug effects</topic><topic>Humans</topic><topic>Intensive Care Units</topic><topic>Male</topic><topic>Meropenem - pharmacology</topic><topic>Meropenem - therapeutic use</topic><topic>Metagenomics</topic><topic>Middle Aged</topic><topic>Prospective Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ravi, Anuradha</creatorcontrib><creatorcontrib>Halstead, Fenella D</creatorcontrib><creatorcontrib>Bamford, Amy</creatorcontrib><creatorcontrib>Casey, Anna</creatorcontrib><creatorcontrib>Thomson, Nicholas M</creatorcontrib><creatorcontrib>van Schaik, Willem</creatorcontrib><creatorcontrib>Snelson, Catherine</creatorcontrib><creatorcontrib>Goulden, Robert</creatorcontrib><creatorcontrib>Foster-Nyarko, Ebenezer</creatorcontrib><creatorcontrib>Savva, George M</creatorcontrib><creatorcontrib>Whitehouse, Tony</creatorcontrib><creatorcontrib>Pallen, Mark J</creatorcontrib><creatorcontrib>Oppenheim, Beryl A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Microbial genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ravi, Anuradha</au><au>Halstead, Fenella D</au><au>Bamford, Amy</au><au>Casey, Anna</au><au>Thomson, Nicholas M</au><au>van Schaik, Willem</au><au>Snelson, Catherine</au><au>Goulden, Robert</au><au>Foster-Nyarko, Ebenezer</au><au>Savva, George M</au><au>Whitehouse, Tony</au><au>Pallen, Mark J</au><au>Oppenheim, Beryl A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients</atitle><jtitle>Microbial genomics</jtitle><addtitle>Microb Genom</addtitle><date>2019-09-01</date><risdate>2019</risdate><volume>5</volume><issue>9</issue><issn>2057-5858</issn><eissn>2057-5858</eissn><abstract>Among long-stay critically ill patients in the adult intensive care unit (ICU), there are often marked changes in the complexity of the gut microbiota. However, it remains unclear whether such patients might benefit from enhanced surveillance or from interventions targeting the gut microbiota or the pathogens therein. We therefore undertook a prospective observational study of 24 ICU patients, in which serial faecal samples were subjected to shotgun metagenomic sequencing, phylogenetic profiling and microbial genome analyses. Two-thirds of the patients experienced a marked drop in gut microbial diversity (to an inverse Simpson's index of <4) at some stage during their stay in the ICU, often accompanied by the absence or loss of potentially beneficial bacteria. Intravenous administration of the broad-spectrum antimicrobial agent meropenem was significantly associated with loss of gut microbial diversity, but the administration of other antibiotics, including piperacillin/tazobactam, failed to trigger statistically detectable changes in microbial diversity. In three-quarters of ICU patients, we documented episodes of gut domination by pathogenic strains, with evidence of cryptic nosocomial transmission of
. In some patients, we also saw an increase in the relative abundance of apparent commensal organisms in the gut microbiome, including the archaeal species
. In conclusion, we have documented a dramatic absence of microbial diversity and pathogen domination of the gut microbiota in a high proportion of critically ill patients using shotgun metagenomics.</abstract><cop>England</cop><pub>Microbiology Society</pub><pmid>31526447</pmid><doi>10.1099/mgen.0.000293</doi><orcidid>https://orcid.org/0000-0002-2833-2926</orcidid><orcidid>https://orcid.org/0000-0002-4387-3421</orcidid><orcidid>https://orcid.org/0000-0001-5832-0988</orcidid><orcidid>https://orcid.org/0000-0003-1168-9010</orcidid><orcidid>https://orcid.org/0000-0003-1807-3657</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Adult Aged Aged, 80 and over Anti-Bacterial Agents - pharmacology Anti-Bacterial Agents - therapeutic use Biodiversity Critical Illness Enterococcus faecium - isolation & purification Enterococcus faecium - physiology Feces - microbiology Female Gastrointestinal Microbiome - drug effects Humans Intensive Care Units Male Meropenem - pharmacology Meropenem - therapeutic use Metagenomics Middle Aged Prospective Studies |
| title | Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients |
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