Alterations to the duodenal microbiota are linked to gastric emptying and symptoms in functional dyspepsia

ObjectiveFunctional dyspepsia (FD) is a complex disorder, with debilitating epigastric symptoms. Evidence suggests alterations in gastrointestinal (GI) motility, visceral hypersensitivity, permeability and low-level immune activation in the duodenum may play a role. However, we still have a relative...

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Veröffentlicht in:Gut 2023-05, Vol.72 (5), p.929-938
Hauptverfasser: Shanahan, Erin R, Kang, Seungha, Staudacher, Heidi, Shah, Ayesha, Do, Anh, Burns, Grace, Chachay, Veronique S, Koloski, Natasha A, Keely, Simon, Walker, Marjorie M, Talley, Nicholas J, Morrison, Mark, Holtmann, Gerald J
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container_end_page 938
container_issue 5
container_start_page 929
container_title Gut
container_volume 72
creator Shanahan, Erin R
Kang, Seungha
Staudacher, Heidi
Shah, Ayesha
Do, Anh
Burns, Grace
Chachay, Veronique S
Koloski, Natasha A
Keely, Simon
Walker, Marjorie M
Talley, Nicholas J
Morrison, Mark
Holtmann, Gerald J
description ObjectiveFunctional dyspepsia (FD) is a complex disorder, with debilitating epigastric symptoms. Evidence suggests alterations in gastrointestinal (GI) motility, visceral hypersensitivity, permeability and low-level immune activation in the duodenum may play a role. However, we still have a relatively poor understanding of how these factors interact to precipitate the onset of FD symptoms which are frequently meal related. The duodenal microbiota, in combination with specific dietary substrates, may be important mediators in disease pathophysiology; however, these interlinked factors have not been thoroughly investigated in FD.DesignEighty-six individuals (56 FD, 30 controls) undergoing endoscopy were consecutively recruited and underwent detailed clinical assessment, including upper GI symptoms, gastric emptying and dietary assessment. Duodenal biopsies were obtained aseptically, and the mucosa-associated microbiota (MAM) analysed via 16S rRNA gene amplicon sequencing.ResultsThe relative abundances of predominant members of the Firmicutes, Bacteroidota and Fusobacteriota phyla were linked to symptom burden in FD. Inverse relationships between the relative abundances of Streptococcus and Prevotella, and the relative abundance of Veillonella spp with gastric emptying time, were also observed. No significant differences in long-term nutrient intake or diet quality were found between FD and controls, and there appeared to be limited association between habitual diet and duodenal MAM profiles.ConclusionThis study suggests a link between the duodenal MAM, gastric emptying and FD symptoms, and this is largely independent of long-term dietary intake.
doi_str_mv 10.1136/gutjnl-2021-326158
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Evidence suggests alterations in gastrointestinal (GI) motility, visceral hypersensitivity, permeability and low-level immune activation in the duodenum may play a role. However, we still have a relatively poor understanding of how these factors interact to precipitate the onset of FD symptoms which are frequently meal related. The duodenal microbiota, in combination with specific dietary substrates, may be important mediators in disease pathophysiology; however, these interlinked factors have not been thoroughly investigated in FD.DesignEighty-six individuals (56 FD, 30 controls) undergoing endoscopy were consecutively recruited and underwent detailed clinical assessment, including upper GI symptoms, gastric emptying and dietary assessment. Duodenal biopsies were obtained aseptically, and the mucosa-associated microbiota (MAM) analysed via 16S rRNA gene amplicon sequencing.ResultsThe relative abundances of predominant members of the Firmicutes, Bacteroidota and Fusobacteriota phyla were linked to symptom burden in FD. Inverse relationships between the relative abundances of Streptococcus and Prevotella, and the relative abundance of Veillonella spp with gastric emptying time, were also observed. No significant differences in long-term nutrient intake or diet quality were found between FD and controls, and there appeared to be limited association between habitual diet and duodenal MAM profiles.ConclusionThis study suggests a link between the duodenal MAM, gastric emptying and FD symptoms, and this is largely independent of long-term dietary intake.</description><identifier>ISSN: 0017-5749</identifier><identifier>EISSN: 1468-3288</identifier><identifier>DOI: 10.1136/gutjnl-2021-326158</identifier><identifier>PMID: 36167662</identifier><language>eng</language><publisher>England: BMJ Publishing Group Ltd and British Society of Gastroenterology</publisher><subject>Anemia ; Biopsy ; Body mass index ; Brain research ; DIET ; Dietary intake ; DUODENAL MUCOSA ; Duodenum ; Dyspepsia ; Endoscopy ; GASTRIC EMPTYING ; Gastric Emptying - physiology ; Humans ; Hypersensitivity ; Immune response ; Infections ; Inflammation ; INTESTINAL MICROBIOLOGY ; Microbiota ; Motility ; Neurogastroenterology ; Patients ; Permeability ; Quality of life ; Relative abundance ; RNA, Ribosomal, 16S - genetics ; rRNA 16S</subject><ispartof>Gut, 2023-05, Vol.72 (5), p.929-938</ispartof><rights>Author(s) (or their employer(s)) 2023. No commercial re-use. See rights and permissions. Published by BMJ.</rights><rights>2022 Author(s) (or their employer(s)) 2022. No commercial re-use. See rights and permissions. Published by BMJ.</rights><rights>2023 Author(s) (or their employer(s)) 2023. No commercial re-use. See rights and permissions. 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Evidence suggests alterations in gastrointestinal (GI) motility, visceral hypersensitivity, permeability and low-level immune activation in the duodenum may play a role. However, we still have a relatively poor understanding of how these factors interact to precipitate the onset of FD symptoms which are frequently meal related. The duodenal microbiota, in combination with specific dietary substrates, may be important mediators in disease pathophysiology; however, these interlinked factors have not been thoroughly investigated in FD.DesignEighty-six individuals (56 FD, 30 controls) undergoing endoscopy were consecutively recruited and underwent detailed clinical assessment, including upper GI symptoms, gastric emptying and dietary assessment. Duodenal biopsies were obtained aseptically, and the mucosa-associated microbiota (MAM) analysed via 16S rRNA gene amplicon sequencing.ResultsThe relative abundances of predominant members of the Firmicutes, Bacteroidota and Fusobacteriota phyla were linked to symptom burden in FD. Inverse relationships between the relative abundances of Streptococcus and Prevotella, and the relative abundance of Veillonella spp with gastric emptying time, were also observed. No significant differences in long-term nutrient intake or diet quality were found between FD and controls, and there appeared to be limited association between habitual diet and duodenal MAM profiles.ConclusionThis study suggests a link between the duodenal MAM, gastric emptying and FD symptoms, and this is largely independent of long-term dietary intake.</description><subject>Anemia</subject><subject>Biopsy</subject><subject>Body mass index</subject><subject>Brain research</subject><subject>DIET</subject><subject>Dietary intake</subject><subject>DUODENAL MUCOSA</subject><subject>Duodenum</subject><subject>Dyspepsia</subject><subject>Endoscopy</subject><subject>GASTRIC EMPTYING</subject><subject>Gastric Emptying - physiology</subject><subject>Humans</subject><subject>Hypersensitivity</subject><subject>Immune response</subject><subject>Infections</subject><subject>Inflammation</subject><subject>INTESTINAL MICROBIOLOGY</subject><subject>Microbiota</subject><subject>Motility</subject><subject>Neurogastroenterology</subject><subject>Patients</subject><subject>Permeability</subject><subject>Quality of life</subject><subject>Relative abundance</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>rRNA 16S</subject><issn>0017-5749</issn><issn>1468-3288</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</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>eNp9kU2L1TAUQIMoznP0D7iQgBs3HXPz1WQ5DH7BgBtdl7RJn6ltUpN08f69KR0VXMwqXDj3JOQg9BrIDQCT789bmcLcUEKhYVSCUE_QCbhUdVLqKToRAm0jWq6v0IucJ0KIUhqeoysmQbZS0hOabufikik-hoxLxOWHw3aL1gUz48UPKfY-FoNNcnj24aezO3U2uSQ_YLes5eLDGZtgcb7UKS4Z-4DHLQy7s0rsJa9uzd68RM9GM2f36uG8Rt8_fvh297m5__rpy93tfdMzrUpDB2F7YKwdgXMjBuMYHYFaRzh3QmgjjJKag7WSW-tEP5qe2GGQBsjIiGHX6N3hXVP8tblcusXnwc2zCS5uuaMtKC0JKF7Rt_-hU9xSffVOaS651lI8TlGmWCVVpehB1T_LObmxW5NfTLp0QLq9V3f06vZe3dGrLr15UG_94uzflT-BKnBzAP0y_bv2EeNvbZSiSQ</recordid><startdate>20230501</startdate><enddate>20230501</enddate><creator>Shanahan, Erin R</creator><creator>Kang, Seungha</creator><creator>Staudacher, Heidi</creator><creator>Shah, Ayesha</creator><creator>Do, Anh</creator><creator>Burns, Grace</creator><creator>Chachay, Veronique S</creator><creator>Koloski, Natasha A</creator><creator>Keely, Simon</creator><creator>Walker, Marjorie M</creator><creator>Talley, Nicholas J</creator><creator>Morrison, Mark</creator><creator>Holtmann, Gerald J</creator><general>BMJ Publishing Group Ltd and British Society of Gastroenterology</general><general>BMJ Publishing Group LTD</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>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><orcidid>https://orcid.org/0000-0003-2537-3092</orcidid><orcidid>https://orcid.org/0000-0002-1248-9590</orcidid><orcidid>https://orcid.org/0000-0002-8647-5933</orcidid><orcidid>https://orcid.org/0000-0001-9257-9133</orcidid><orcidid>https://orcid.org/0000-0002-0206-2358</orcidid><orcidid>https://orcid.org/0000-0001-6704-2131</orcidid></search><sort><creationdate>20230501</creationdate><title>Alterations to the duodenal microbiota are linked to gastric emptying and symptoms in functional dyspepsia</title><author>Shanahan, Erin R ; 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Evidence suggests alterations in gastrointestinal (GI) motility, visceral hypersensitivity, permeability and low-level immune activation in the duodenum may play a role. However, we still have a relatively poor understanding of how these factors interact to precipitate the onset of FD symptoms which are frequently meal related. The duodenal microbiota, in combination with specific dietary substrates, may be important mediators in disease pathophysiology; however, these interlinked factors have not been thoroughly investigated in FD.DesignEighty-six individuals (56 FD, 30 controls) undergoing endoscopy were consecutively recruited and underwent detailed clinical assessment, including upper GI symptoms, gastric emptying and dietary assessment. Duodenal biopsies were obtained aseptically, and the mucosa-associated microbiota (MAM) analysed via 16S rRNA gene amplicon sequencing.ResultsThe relative abundances of predominant members of the Firmicutes, Bacteroidota and Fusobacteriota phyla were linked to symptom burden in FD. Inverse relationships between the relative abundances of Streptococcus and Prevotella, and the relative abundance of Veillonella spp with gastric emptying time, were also observed. No significant differences in long-term nutrient intake or diet quality were found between FD and controls, and there appeared to be limited association between habitual diet and duodenal MAM profiles.ConclusionThis study suggests a link between the duodenal MAM, gastric emptying and FD symptoms, and this is largely independent of long-term dietary intake.</abstract><cop>England</cop><pub>BMJ Publishing Group Ltd and British Society of Gastroenterology</pub><pmid>36167662</pmid><doi>10.1136/gutjnl-2021-326158</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-2537-3092</orcidid><orcidid>https://orcid.org/0000-0002-1248-9590</orcidid><orcidid>https://orcid.org/0000-0002-8647-5933</orcidid><orcidid>https://orcid.org/0000-0001-9257-9133</orcidid><orcidid>https://orcid.org/0000-0002-0206-2358</orcidid><orcidid>https://orcid.org/0000-0001-6704-2131</orcidid></addata></record>
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language eng
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source MEDLINE; PubMed Central
subjects Anemia
Biopsy
Body mass index
Brain research
DIET
Dietary intake
DUODENAL MUCOSA
Duodenum
Dyspepsia
Endoscopy
GASTRIC EMPTYING
Gastric Emptying - physiology
Humans
Hypersensitivity
Immune response
Infections
Inflammation
INTESTINAL MICROBIOLOGY
Microbiota
Motility
Neurogastroenterology
Patients
Permeability
Quality of life
Relative abundance
RNA, Ribosomal, 16S - genetics
rRNA 16S
title Alterations to the duodenal microbiota are linked to gastric emptying and symptoms in functional dyspepsia
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