Gut and oral microbial compositional differences in women with breast cancer, women with ductal carcinoma in situ, and healthy women.

IF 5 2区 生物学 Q1 MICROBIOLOGY
mSystems Pub Date : 2024-11-19 Epub Date: 2024-10-29 DOI:10.1128/msystems.01237-24
Emma McCune, Anukriti Sharma, Breanna Johnson, Tess O'Meara, Sarah Theiner, Maribel Campos, Diane Heditsian, Susie Brain, Jack A Gilbert, Laura Esserman, Michael J Campbell
{"title":"Gut and oral microbial compositional differences in women with breast cancer, women with ductal carcinoma <i>in situ</i>, and healthy women.","authors":"Emma McCune, Anukriti Sharma, Breanna Johnson, Tess O'Meara, Sarah Theiner, Maribel Campos, Diane Heditsian, Susie Brain, Jack A Gilbert, Laura Esserman, Michael J Campbell","doi":"10.1128/msystems.01237-24","DOIUrl":null,"url":null,"abstract":"<p><p>This study characterized and compared the fecal and oral microbiota from women with early-stage breast cancer (BC), women with ductal carcinoma <i>in situ</i> (DCIS), and healthy women. Fecal and oral samples were collected from newly diagnosed patients prior to any therapy and characterized using 16S rRNA sequencing. Measures of gut microbial alpha diversity were significantly lower in the BC vs healthy cohort. Beta diversity differed significantly between the BC or DCIS and healthy groups, and several differentially abundant taxa were identified. Clustering (non-negative matrix factorization) of the gut microbiota identified five bacterial guilds dominated by <i>Prevotella</i>, Enterobacteriaceae, <i>Akkermansia</i>, Clostridiales, or <i>Bacteroides</i>. The <i>Bacteroides</i> and Enterobacteriaceae guilds were significantly more abundant in the BC cohort compared to healthy controls, whereas the Clostridiales guild was more abundant in the healthy group. Finally, prediction of functional pathways identified 23 pathways that differed between the BC and healthy gut microbiota including lipopolysaccharide biosynthesis, glycan biosynthesis and metabolism, lipid metabolism, and sphingolipid metabolism. In contrast to the gut microbiomes, there were no significant differences in alpha or beta diversity in the oral microbiomes, and very few differentially abundant taxa were observed. Non-negative matrix factorization analysis of the oral microbiota samples identified seven guilds dominated by <i>Veillonella</i>, <i>Prevotella</i>, Gemellaceae, <i>Haemophilus</i>, <i>Neisseria</i>, <i>Propionibacterium</i>, and <i>Streptococcus</i>; however, none of these guilds were differentially associated with the different cohorts. Our results suggest that alterations in the gut microbiota may provide the basis for interventions targeting the gut microbiome to improve treatment outcomes and long-term prognosis.</p><p><strong>Importance: </strong>Emerging evidence suggests that the gut microbiota may play a role in breast cancer. Few studies have evaluated both the gut and oral microbiomes in women with breast cancer (BC), and none have characterized these microbiomes in women with ductal carcinoma <i>in situ</i> (DCIS). We surveyed the gut and oral microbiomes from women with BC or DCIS and healthy women and identified compositional and functional features of the gut microbiota that differed between these cohorts. In contrast, very few differential features were identified in the oral microbiota. Understanding the role of gut bacteria in BC and DCIS may open up new opportunities for the development of novel markers for early detection (or markers of susceptibility) as well as new strategies for prevention and/or treatment.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0123724"},"PeriodicalIF":5.0000,"publicationDate":"2024-11-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11575313/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSystems","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msystems.01237-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/29 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

This study characterized and compared the fecal and oral microbiota from women with early-stage breast cancer (BC), women with ductal carcinoma in situ (DCIS), and healthy women. Fecal and oral samples were collected from newly diagnosed patients prior to any therapy and characterized using 16S rRNA sequencing. Measures of gut microbial alpha diversity were significantly lower in the BC vs healthy cohort. Beta diversity differed significantly between the BC or DCIS and healthy groups, and several differentially abundant taxa were identified. Clustering (non-negative matrix factorization) of the gut microbiota identified five bacterial guilds dominated by Prevotella, Enterobacteriaceae, Akkermansia, Clostridiales, or Bacteroides. The Bacteroides and Enterobacteriaceae guilds were significantly more abundant in the BC cohort compared to healthy controls, whereas the Clostridiales guild was more abundant in the healthy group. Finally, prediction of functional pathways identified 23 pathways that differed between the BC and healthy gut microbiota including lipopolysaccharide biosynthesis, glycan biosynthesis and metabolism, lipid metabolism, and sphingolipid metabolism. In contrast to the gut microbiomes, there were no significant differences in alpha or beta diversity in the oral microbiomes, and very few differentially abundant taxa were observed. Non-negative matrix factorization analysis of the oral microbiota samples identified seven guilds dominated by Veillonella, Prevotella, Gemellaceae, Haemophilus, Neisseria, Propionibacterium, and Streptococcus; however, none of these guilds were differentially associated with the different cohorts. Our results suggest that alterations in the gut microbiota may provide the basis for interventions targeting the gut microbiome to improve treatment outcomes and long-term prognosis.

Importance: Emerging evidence suggests that the gut microbiota may play a role in breast cancer. Few studies have evaluated both the gut and oral microbiomes in women with breast cancer (BC), and none have characterized these microbiomes in women with ductal carcinoma in situ (DCIS). We surveyed the gut and oral microbiomes from women with BC or DCIS and healthy women and identified compositional and functional features of the gut microbiota that differed between these cohorts. In contrast, very few differential features were identified in the oral microbiota. Understanding the role of gut bacteria in BC and DCIS may open up new opportunities for the development of novel markers for early detection (or markers of susceptibility) as well as new strategies for prevention and/or treatment.

乳腺癌妇女、乳腺导管原位癌妇女和健康妇女的肠道和口腔微生物组成差异。
这项研究对患有早期乳腺癌(BC)的妇女、患有导管原位癌(DCIS)的妇女以及健康妇女的粪便和口腔微生物群进行了特征描述和比较。新诊断的患者在接受任何治疗前采集了粪便和口腔样本,并使用 16S rRNA 测序对其进行了表征。与健康人群相比,乳腺癌患者的肠道微生物α多样性明显较低。BC或DCIS组与健康组之间的β多样性差异明显,并发现了几个不同的丰富类群。肠道微生物群的聚类(非负矩阵因式分解)确定了以前驱菌属、肠杆菌科、Akkermansia、梭状芽孢杆菌属或Bacteroides为主的五个细菌行会。与健康对照组相比,Bacteroides 和肠杆菌科细菌群在 BC 组群中明显更多,而梭状芽孢杆菌群在健康组群中更多。最后,对功能通路的预测确定了 BC 组和健康组肠道微生物群之间存在差异的 23 条通路,包括脂多糖生物合成、糖类生物合成和代谢、脂质代谢和鞘脂代谢。与肠道微生物组不同的是,口腔微生物组中的α或β多样性没有显著差异,而且很少观察到差异丰富的类群。对口腔微生物群样本进行的非负矩阵因式分解分析确定了以 Veillonella、Prevotella、Gemellaceae、Haemophilus、Neisseria、Propionibacterium 和 Streptococcus 为主的七个类群;然而,这些类群与不同队列的关联性均不相同。我们的研究结果表明,肠道微生物群的改变可为针对肠道微生物群的干预措施提供依据,从而改善治疗效果和长期预后:新的证据表明,肠道微生物群可能在乳腺癌中发挥作用。很少有研究对乳腺癌(BC)女性患者的肠道和口腔微生物组进行评估,也没有研究对乳腺导管原位癌(DCIS)女性患者的这些微生物组进行特征描述。我们调查了患有乳腺癌或乳腺导管原位癌(DCIS)的女性和健康女性的肠道和口腔微生物组,发现了这些组群之间存在差异的肠道微生物组的组成和功能特征。相比之下,在口腔微生物群中却很少发现差异特征。了解肠道细菌在BC和DCIS中的作用可能会为开发用于早期检测的新型标记物(或易感性标记物)以及新的预防和/或治疗策略带来新的机遇。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
mSystems
mSystems Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍: mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.
×
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