肠道微生物群特征和循环代谢物与儿童全身性炎症的关系。

IF 3.3 Q2 GASTROENTEROLOGY & HEPATOLOGY
Bruno Bohn, Curtis Tilves, Yingan Chen, Myriam Doyon, Luigi Bouchard, Patrice Perron, Renée Guérin, Éric Massé, Marie-France Hivert, Noel T Mueller
{"title":"肠道微生物群特征和循环代谢物与儿童全身性炎症的关系。","authors":"Bruno Bohn, Curtis Tilves, Yingan Chen, Myriam Doyon, Luigi Bouchard, Patrice Perron, Renée Guérin, Éric Massé, Marie-France Hivert, Noel T Mueller","doi":"10.1136/bmjgast-2024-001470","DOIUrl":null,"url":null,"abstract":"<p><strong>Objective: </strong>Gut microbes and microbe-dependent metabolites (eg, tryptophan-kynurenine-serotonin pathway metabolites) have been linked to systemic inflammation, but the microbiota-metabolite-inflammation axis remains uncharacterised in children. Here we investigated whether gut microbiota features and circulating metabolites (both microbe-dependent and non-microbe-dependent metabolites) associated with circulating inflammation markers in children.</p><p><strong>Methods: </strong>We studied children from the prospective Gen3G birth cohort who had data on untargeted plasma metabolome (n=321 children; Metabolon platform), gut microbiota (n=147; 16S rRNA sequencing), and inflammation markers (plasminogen activator inhibitor-1 (PAI-1), monocyte chemoattractant protein-1, and tumour necrosis factor-α) measured at 5-7 years. We examined associations of microbial taxa and metabolites-examining microbe-dependent and non-microbe-dependent metabolites separately-with each inflammatory marker and with an overall inflammation score (InfSc), adjusting for key confounders and correcting for multiple comparisons. We also compared the proportion of significantly associated microbe-dependent versus non-microbe-dependent metabolites, identified a priori (Human Microbial Metabolome Database), with each inflammation marker.</p><p><strong>Results: </strong>Of 335 taxa tested, 149 were associated (q<sub>FDR</sub><0.05) with at least one inflammatory marker; 10 of these were robust to pseudocount choice. Several bacterial taxa involved in tryptophan metabolism were associated with inflammation, including kynurenine-degrading <i>Ruminococcus</i>, which was inversely associated with all inflammation markers. Of 1037 metabolites tested, 315 were previously identified as microbe dependent and were more frequently associated with PAI-1 and the InfSc than non-microbe dependent metabolites. In total, 87 metabolites were associated (q<sub>FDR</sub><0.05) with at least one inflammation marker, including kynurenine (positively), serotonin (positively), and tryptophan (inversely).</p><p><strong>Conclusion: </strong>A distinct set of gut microbes and microbe-dependent metabolites, including those involved in the tryptophan-kynurenine-serotonin pathway, may be implicated in inflammatory pathways in childhood.</p>","PeriodicalId":9235,"journal":{"name":"BMJ Open Gastroenterology","volume":null,"pages":null},"PeriodicalIF":3.3000,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11367355/pdf/","citationCount":"0","resultStr":"{\"title\":\"Associations of gut microbiota features and circulating metabolites with systemic inflammation in children.\",\"authors\":\"Bruno Bohn, Curtis Tilves, Yingan Chen, Myriam Doyon, Luigi Bouchard, Patrice Perron, Renée Guérin, Éric Massé, Marie-France Hivert, Noel T Mueller\",\"doi\":\"10.1136/bmjgast-2024-001470\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Objective: </strong>Gut microbes and microbe-dependent metabolites (eg, tryptophan-kynurenine-serotonin pathway metabolites) have been linked to systemic inflammation, but the microbiota-metabolite-inflammation axis remains uncharacterised in children. Here we investigated whether gut microbiota features and circulating metabolites (both microbe-dependent and non-microbe-dependent metabolites) associated with circulating inflammation markers in children.</p><p><strong>Methods: </strong>We studied children from the prospective Gen3G birth cohort who had data on untargeted plasma metabolome (n=321 children; Metabolon platform), gut microbiota (n=147; 16S rRNA sequencing), and inflammation markers (plasminogen activator inhibitor-1 (PAI-1), monocyte chemoattractant protein-1, and tumour necrosis factor-α) measured at 5-7 years. We examined associations of microbial taxa and metabolites-examining microbe-dependent and non-microbe-dependent metabolites separately-with each inflammatory marker and with an overall inflammation score (InfSc), adjusting for key confounders and correcting for multiple comparisons. We also compared the proportion of significantly associated microbe-dependent versus non-microbe-dependent metabolites, identified a priori (Human Microbial Metabolome Database), with each inflammation marker.</p><p><strong>Results: </strong>Of 335 taxa tested, 149 were associated (q<sub>FDR</sub><0.05) with at least one inflammatory marker; 10 of these were robust to pseudocount choice. Several bacterial taxa involved in tryptophan metabolism were associated with inflammation, including kynurenine-degrading <i>Ruminococcus</i>, which was inversely associated with all inflammation markers. Of 1037 metabolites tested, 315 were previously identified as microbe dependent and were more frequently associated with PAI-1 and the InfSc than non-microbe dependent metabolites. In total, 87 metabolites were associated (q<sub>FDR</sub><0.05) with at least one inflammation marker, including kynurenine (positively), serotonin (positively), and tryptophan (inversely).</p><p><strong>Conclusion: </strong>A distinct set of gut microbes and microbe-dependent metabolites, including those involved in the tryptophan-kynurenine-serotonin pathway, may be implicated in inflammatory pathways in childhood.</p>\",\"PeriodicalId\":9235,\"journal\":{\"name\":\"BMJ Open Gastroenterology\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":3.3000,\"publicationDate\":\"2024-08-29\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11367355/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"BMJ Open Gastroenterology\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1136/bmjgast-2024-001470\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"GASTROENTEROLOGY & HEPATOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"BMJ Open Gastroenterology","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1136/bmjgast-2024-001470","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"GASTROENTEROLOGY & HEPATOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

目的:肠道微生物和微生物依赖性代谢物(如色氨酸-犬尿氨酸-羟色胺通路代谢物)与全身炎症有关,但在儿童中,微生物群-代谢物-炎症轴仍未被描述。在此,我们研究了肠道微生物群特征和循环代谢物(包括依赖微生物和不依赖微生物的代谢物)是否与儿童循环炎症指标相关:我们研究了前瞻性Gen3G出生队列中的儿童,他们在5-7岁时测量了非靶向血浆代谢组(321名儿童;Metabolon平台)、肠道微生物群(147名儿童;16S rRNA测序)和炎症标志物(纤溶酶原激活物抑制剂-1(PAI-1)、单核细胞趋化蛋白-1和肿瘤坏死因子-α)。我们研究了微生物类群和代谢物--分别研究了依赖微生物和不依赖微生物的代谢物--与每种炎症标记物和总体炎症评分(InfSc)的关系,调整了主要混杂因素并校正了多重比较。我们还比较了先验鉴定(人类微生物代谢组数据库)发现的与每种炎症标记物明显相关的微生物依赖性代谢物和非微生物依赖性代谢物的比例:在检测的 335 个类群中,149 个类群与所有炎症标志物相关(qFDRR为反刍球菌,与所有炎症标志物成反比)。在检测的 1037 种代谢物中,有 315 种先前被确定为依赖微生物,与非依赖微生物的代谢物相比,它们与 PAI-1 和 InfSc 的相关性更高。共有 87 种代谢物与 PAI-1 和 InfSc 相关(qFDRC 结论:一组独特的肠道微生物与 PAI-1 和 InfSc 相关:一组不同的肠道微生物和微生物依赖性代谢物,包括色氨酸-犬尿氨酸-羟色胺通路中的代谢物,可能与儿童期的炎症通路有关。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Associations of gut microbiota features and circulating metabolites with systemic inflammation in children.

Objective: Gut microbes and microbe-dependent metabolites (eg, tryptophan-kynurenine-serotonin pathway metabolites) have been linked to systemic inflammation, but the microbiota-metabolite-inflammation axis remains uncharacterised in children. Here we investigated whether gut microbiota features and circulating metabolites (both microbe-dependent and non-microbe-dependent metabolites) associated with circulating inflammation markers in children.

Methods: We studied children from the prospective Gen3G birth cohort who had data on untargeted plasma metabolome (n=321 children; Metabolon platform), gut microbiota (n=147; 16S rRNA sequencing), and inflammation markers (plasminogen activator inhibitor-1 (PAI-1), monocyte chemoattractant protein-1, and tumour necrosis factor-α) measured at 5-7 years. We examined associations of microbial taxa and metabolites-examining microbe-dependent and non-microbe-dependent metabolites separately-with each inflammatory marker and with an overall inflammation score (InfSc), adjusting for key confounders and correcting for multiple comparisons. We also compared the proportion of significantly associated microbe-dependent versus non-microbe-dependent metabolites, identified a priori (Human Microbial Metabolome Database), with each inflammation marker.

Results: Of 335 taxa tested, 149 were associated (qFDR<0.05) with at least one inflammatory marker; 10 of these were robust to pseudocount choice. Several bacterial taxa involved in tryptophan metabolism were associated with inflammation, including kynurenine-degrading Ruminococcus, which was inversely associated with all inflammation markers. Of 1037 metabolites tested, 315 were previously identified as microbe dependent and were more frequently associated with PAI-1 and the InfSc than non-microbe dependent metabolites. In total, 87 metabolites were associated (qFDR<0.05) with at least one inflammation marker, including kynurenine (positively), serotonin (positively), and tryptophan (inversely).

Conclusion: A distinct set of gut microbes and microbe-dependent metabolites, including those involved in the tryptophan-kynurenine-serotonin pathway, may be implicated in inflammatory pathways in childhood.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
BMJ Open Gastroenterology
BMJ Open Gastroenterology GASTROENTEROLOGY & HEPATOLOGY-
CiteScore
5.90
自引率
3.20%
发文量
68
审稿时长
2 weeks
期刊介绍: BMJ Open Gastroenterology is an online-only, peer-reviewed, open access gastroenterology journal, dedicated to publishing high-quality medical research from all disciplines and therapeutic areas of gastroenterology. It is the open access companion journal of Gut and is co-owned by the British Society of Gastroenterology. The journal publishes all research study types, from study protocols to phase I trials to meta-analyses, including small or specialist studies. Publishing procedures are built around continuous publication, publishing research online as soon as the article is ready.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信