Butyricicoccus pullicaecorum in inflammatory bowel disease

Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum i...

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Veröffentlicht in:Gut 2013-12, Vol.62 (12), p.1745-1752
Hauptverfasser: Eeckhaut, Venessa, Machiels, Kathleen, Perrier, Clémentine, Romero, Carlos, Maes, Sofie, Flahou, Bram, Steppe, Marjan, Haesebrouck, Freddy, Sas, Benedikt, Ducatelle, Richard, Vermeire, Severine, Van Immerseel, Filip
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container_end_page 1752
container_issue 12
container_start_page 1745
container_title Gut
container_volume 62
creator Eeckhaut, Venessa
Machiels, Kathleen
Perrier, Clémentine
Romero, Carlos
Maes, Sofie
Flahou, Bram
Steppe, Marjan
Haesebrouck, Freddy
Sas, Benedikt
Ducatelle, Richard
Vermeire, Severine
Van Immerseel, Filip
description Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.
doi_str_mv 10.1136/gutjnl-2012-303611
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We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.</description><identifier>ISSN: 0017-5749</identifier><identifier>EISSN: 1468-3288</identifier><identifier>DOI: 10.1136/gutjnl-2012-303611</identifier><identifier>PMID: 23263527</identifier><identifier>CODEN: GUTTAK</identifier><language>eng</language><publisher>England: BMJ Publishing Group Ltd and British Society of Gastroenterology</publisher><subject>Adult ; Animals ; Bacteria ; Bacterial Load ; Biopsy ; Butyrate ; Case-Control Studies ; Colitis, Ulcerative - microbiology ; Colitis, Ulcerative - prevention &amp; control ; Crohn Disease - microbiology ; Crohn Disease - prevention &amp; control ; Cytokines ; Disease Models, Animal ; Epithelial Barrier ; Feces - microbiology ; Female ; Firmicutes ; Gram-Positive Endospore-Forming Rods - genetics ; Gram-Positive Endospore-Forming Rods - physiology ; Humans ; IBD ; Inflammation ; Inflammatory bowel disease ; Intestinal Mucosa - metabolism ; Male ; Permeability ; Prevention ; Probiotics ; Probiotics - pharmacology ; Rats ; Rats, Wistar ; Real-Time Polymerase Chain Reaction ; RNA, Ribosomal, 16S - genetics ; Rodents ; Studies ; Womens health</subject><ispartof>Gut, 2013-12, Vol.62 (12), p.1745-1752</ispartof><rights>Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions</rights><rights>Copyright: 2013 Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b489t-5cf2816d847714854a654de7c86ca4a4b835fb1dc36192d768378726ba4f5e923</citedby><cites>FETCH-LOGICAL-b489t-5cf2816d847714854a654de7c86ca4a4b835fb1dc36192d768378726ba4f5e923</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttp://gut.bmj.com/content/62/12/1745.full.pdf$$EPDF$$P50$$Gbmj$$H</linktopdf><linktohtml>$$Uhttp://gut.bmj.com/content/62/12/1745.full$$EHTML$$P50$$Gbmj$$H</linktohtml><link.rule.ids>114,115,314,780,784,3196,23571,27924,27925,77472,77503</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23263527$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Eeckhaut, Venessa</creatorcontrib><creatorcontrib>Machiels, Kathleen</creatorcontrib><creatorcontrib>Perrier, Clémentine</creatorcontrib><creatorcontrib>Romero, Carlos</creatorcontrib><creatorcontrib>Maes, Sofie</creatorcontrib><creatorcontrib>Flahou, Bram</creatorcontrib><creatorcontrib>Steppe, Marjan</creatorcontrib><creatorcontrib>Haesebrouck, Freddy</creatorcontrib><creatorcontrib>Sas, Benedikt</creatorcontrib><creatorcontrib>Ducatelle, Richard</creatorcontrib><creatorcontrib>Vermeire, Severine</creatorcontrib><creatorcontrib>Van Immerseel, Filip</creatorcontrib><title>Butyricicoccus pullicaecorum in inflammatory bowel disease</title><title>Gut</title><addtitle>Gut</addtitle><description>Objective Many species within the phylum Firmicutes are thought to exert anti-inflammatory effects. We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.</description><subject>Adult</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacterial Load</subject><subject>Biopsy</subject><subject>Butyrate</subject><subject>Case-Control Studies</subject><subject>Colitis, Ulcerative - microbiology</subject><subject>Colitis, Ulcerative - prevention &amp; control</subject><subject>Crohn Disease - microbiology</subject><subject>Crohn Disease - prevention &amp; control</subject><subject>Cytokines</subject><subject>Disease Models, Animal</subject><subject>Epithelial Barrier</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Firmicutes</subject><subject>Gram-Positive Endospore-Forming Rods - genetics</subject><subject>Gram-Positive Endospore-Forming Rods - physiology</subject><subject>Humans</subject><subject>IBD</subject><subject>Inflammation</subject><subject>Inflammatory bowel disease</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Male</subject><subject>Permeability</subject><subject>Prevention</subject><subject>Probiotics</subject><subject>Probiotics - pharmacology</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Rodents</subject><subject>Studies</subject><subject>Womens health</subject><issn>0017-5749</issn><issn>1468-3288</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkUtLw0AQxxdRtD6-gAcpePES3dl3vGmxPlEK1euy2WwkNWnqbhbttzclPsCLwsAc5jf_efwR2gd8DEDFyXNsZ_MqIRhIQjEVAGtoAEyohBKl1tEAY5AJlyzdQtshzDDGSqWwibYIJYJyIgfo9Dy2S1_a0jbWxjBcxKoqrXG28bEelvMuisrUtWkbvxxmzZurhnkZnAluF20Upgpu7zPvoMfxxXR0ldw9XF6Pzu6SjKm0TbgtiAKRKyYlMMWZEZzlTlolrGGGZYryIoPcdgekJJdCUakkEZlhBXcpoTvoqNdd-OY1utDqugzWVZWZuyYGDZJTxgVN5d8oY2m3BYDo0MNf6KyJft4d0gnKlAkQajWb9JT1TQjeFXrhy9r4pQasVybo3gS9MkH3JnRNB5_SMatd_t3y9fUOSHqgDK17_64b_6KFpJLr-6eRHt3cjCfTW6onP3xWz_6zwAd4Wp-X</recordid><startdate>20131201</startdate><enddate>20131201</enddate><creator>Eeckhaut, Venessa</creator><creator>Machiels, Kathleen</creator><creator>Perrier, Clémentine</creator><creator>Romero, Carlos</creator><creator>Maes, Sofie</creator><creator>Flahou, Bram</creator><creator>Steppe, Marjan</creator><creator>Haesebrouck, Freddy</creator><creator>Sas, Benedikt</creator><creator>Ducatelle, Richard</creator><creator>Vermeire, Severine</creator><creator>Van Immerseel, Filip</creator><general>BMJ Publishing Group Ltd and British Society of Gastroenterology</general><general>BMJ Publishing Group LTD</general><scope>BSCLL</scope><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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AF</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BTHHO</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>7T5</scope><scope>H94</scope></search><sort><creationdate>20131201</creationdate><title>Butyricicoccus pullicaecorum in inflammatory bowel disease</title><author>Eeckhaut, Venessa ; Machiels, Kathleen ; Perrier, Clémentine ; Romero, Carlos ; Maes, Sofie ; Flahou, Bram ; Steppe, Marjan ; Haesebrouck, Freddy ; Sas, Benedikt ; Ducatelle, Richard ; Vermeire, Severine ; Van Immerseel, Filip</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b489t-5cf2816d847714854a654de7c86ca4a4b835fb1dc36192d768378726ba4f5e923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adult</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacterial Load</topic><topic>Biopsy</topic><topic>Butyrate</topic><topic>Case-Control Studies</topic><topic>Colitis, Ulcerative - microbiology</topic><topic>Colitis, Ulcerative - prevention &amp; control</topic><topic>Crohn Disease - microbiology</topic><topic>Crohn Disease - prevention &amp; control</topic><topic>Cytokines</topic><topic>Disease Models, Animal</topic><topic>Epithelial Barrier</topic><topic>Feces - microbiology</topic><topic>Female</topic><topic>Firmicutes</topic><topic>Gram-Positive Endospore-Forming Rods - genetics</topic><topic>Gram-Positive Endospore-Forming Rods - physiology</topic><topic>Humans</topic><topic>IBD</topic><topic>Inflammation</topic><topic>Inflammatory bowel disease</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Male</topic><topic>Permeability</topic><topic>Prevention</topic><topic>Probiotics</topic><topic>Probiotics - pharmacology</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Rodents</topic><topic>Studies</topic><topic>Womens health</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Eeckhaut, Venessa</creatorcontrib><creatorcontrib>Machiels, Kathleen</creatorcontrib><creatorcontrib>Perrier, Clémentine</creatorcontrib><creatorcontrib>Romero, Carlos</creatorcontrib><creatorcontrib>Maes, Sofie</creatorcontrib><creatorcontrib>Flahou, Bram</creatorcontrib><creatorcontrib>Steppe, Marjan</creatorcontrib><creatorcontrib>Haesebrouck, Freddy</creatorcontrib><creatorcontrib>Sas, Benedikt</creatorcontrib><creatorcontrib>Ducatelle, Richard</creatorcontrib><creatorcontrib>Vermeire, Severine</creatorcontrib><creatorcontrib>Van Immerseel, Filip</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health &amp; 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We quantified bacteria belonging to the genus Butyricicoccus in stools of patients with ulcerative colitis (UC) and Crohn's disease (CD). We evaluated the effect of Butyricicoccus pullicaecorum in a rat colitis model and analysed the ability to prevent cytokine-induced increases in epithelial permeability. Design A genus-specific quantitative PCR was used for quantification of Butyricicoccus in stools from patients with UC or CD and healthy subjects. The effect of B pullicaecorum on trinitrobenzenesulfonic (TNBS)-induced colitis was assessed and the effect of B pullicaecorum culture supernatant on epithelial barrier function was investigated in vitro. Results The average number of Butyricicoccus in stools from patients with UC and CD in active (UC: 8.61 log10/g stool; CD: 6.58 log10/g stool) and remission phase (UC: 8.69 log10/g stool; CD: 8.38 log10/g stool) was significantly lower compared with healthy subjects (9.32 log10/g stool) and correlated with disease activity in CD. Oral administration of B pullicaecorum resulted in a significant protective effect based on macroscopic and histological criteria and decreased intestinal myeloperoxidase (MPO), tumour necrosis factor α (TNFα) and interleukin (IL)-12 levels. Supernatant of B pullicaecorum prevented the loss of transepithelial resistance (TER) and the increase in IL-8 secretion induced by TNFα and interferon γ (IFN gamma) in a Caco-2 cell model. Conclusions Patients with inflammatory bowel disease have lower numbers of Butyricicoccus bacteria in their stools. Administration of B pullicaecorum attenuates TNBS-induced colitis in rats and supernatant of B pullicaecorum cultures strengthens the epithelial barrier function by increasing the TER.</abstract><cop>England</cop><pub>BMJ Publishing Group Ltd and British Society of Gastroenterology</pub><pmid>23263527</pmid><doi>10.1136/gutjnl-2012-303611</doi><tpages>8</tpages></addata></record>
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subjects Adult
Animals
Bacteria
Bacterial Load
Biopsy
Butyrate
Case-Control Studies
Colitis, Ulcerative - microbiology
Colitis, Ulcerative - prevention & control
Crohn Disease - microbiology
Crohn Disease - prevention & control
Cytokines
Disease Models, Animal
Epithelial Barrier
Feces - microbiology
Female
Firmicutes
Gram-Positive Endospore-Forming Rods - genetics
Gram-Positive Endospore-Forming Rods - physiology
Humans
IBD
Inflammation
Inflammatory bowel disease
Intestinal Mucosa - metabolism
Male
Permeability
Prevention
Probiotics
Probiotics - pharmacology
Rats
Rats, Wistar
Real-Time Polymerase Chain Reaction
RNA, Ribosomal, 16S - genetics
Rodents
Studies
Womens health
title Butyricicoccus pullicaecorum in inflammatory bowel disease
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