Doratha A Byrd, Maria Gomez, Stephanie Hogue, Yunhu Wan, Ana Ortega-Villa, Andrew Warner, Casey Dagnall, Kristine Jones, Belynda Hicks, Paul Albert, Gwen Murphy, Rashmi Sinha, Emily Vogtmann
{"title":"Effects of a high-fiber, high-fruit and high-vegetable, low-fat dietary intervention on the rectal tissue microbiome.","authors":"Doratha A Byrd, Maria Gomez, Stephanie Hogue, Yunhu Wan, Ana Ortega-Villa, Andrew Warner, Casey Dagnall, Kristine Jones, Belynda Hicks, Paul Albert, Gwen Murphy, Rashmi Sinha, Emily Vogtmann","doi":"10.1093/jnci/djaf034","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Emerging evidence suggests that bacteria residing in colorectal tissue are plausibly associated with colorectal cancer. Prior studies investigated the effects of dietary interventions on the fecal microbiome, but few assessed colorectal tissue microbiome endpoints. We investigated the effects of a high-fiber, high-fruit, high-vegetable, and low-fat dietary intervention on the rectal tissue microbiome in the Polyp Prevention Trial (PPT).</p><p><strong>Methods: </strong>PPT is a 4-year randomized clinical trial with intervention goals of consuming (1) at least 18 g of fiber per 1000 kcal/day; (2) at least 3.5 servings of fruits and vegetables per 1000 kcal/day; and (3) no more than 20% of kcal/day from fat. Using 16S ribosomal RNA gene sequencing, we characterized bacteria in rectal biopsies collected at baseline and the end of years 1 and 4 (n = 233 in intervention arm and n = 222 in control arm). We estimated effects of the intervention on alpha and beta diversity and relative abundance of a priori-selected bacteria using repeated-measures linear mixed-effects models.</p><p><strong>Results: </strong>The intervention did not statistically significantly modify rectal tissue alpha diversity. Compared with the control arm, relative abundance of a priori-selected Porphyromonas (absolute intervention effects [standard errors] at T1 vs T0 = -0.24 [0.07] and T4 vs T0 = -0.12 [0.07]; P = .004) and Prevotella (absolute intervention effects at T1 vs T0 = -0.40 [0.14] and at T4 vs T0 = -0.32 [0.15]; P = .01) were more strongly decreased in the intervention arm.</p><p><strong>Conclusion: </strong>The PPT intervention did not influence rectal tissue microbiome diversity or the relative abundance of most bacteria, except for 2 oral-originating bacteria that were previously associated with colorectal cancer presence.</p>","PeriodicalId":14809,"journal":{"name":"JNCI Journal of the National Cancer Institute","volume":" ","pages":"1237-1244"},"PeriodicalIF":7.2000,"publicationDate":"2025-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12145913/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"JNCI Journal of the National Cancer Institute","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1093/jnci/djaf034","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ONCOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Emerging evidence suggests that bacteria residing in colorectal tissue are plausibly associated with colorectal cancer. Prior studies investigated the effects of dietary interventions on the fecal microbiome, but few assessed colorectal tissue microbiome endpoints. We investigated the effects of a high-fiber, high-fruit, high-vegetable, and low-fat dietary intervention on the rectal tissue microbiome in the Polyp Prevention Trial (PPT).
Methods: PPT is a 4-year randomized clinical trial with intervention goals of consuming (1) at least 18 g of fiber per 1000 kcal/day; (2) at least 3.5 servings of fruits and vegetables per 1000 kcal/day; and (3) no more than 20% of kcal/day from fat. Using 16S ribosomal RNA gene sequencing, we characterized bacteria in rectal biopsies collected at baseline and the end of years 1 and 4 (n = 233 in intervention arm and n = 222 in control arm). We estimated effects of the intervention on alpha and beta diversity and relative abundance of a priori-selected bacteria using repeated-measures linear mixed-effects models.
Results: The intervention did not statistically significantly modify rectal tissue alpha diversity. Compared with the control arm, relative abundance of a priori-selected Porphyromonas (absolute intervention effects [standard errors] at T1 vs T0 = -0.24 [0.07] and T4 vs T0 = -0.12 [0.07]; P = .004) and Prevotella (absolute intervention effects at T1 vs T0 = -0.40 [0.14] and at T4 vs T0 = -0.32 [0.15]; P = .01) were more strongly decreased in the intervention arm.
Conclusion: The PPT intervention did not influence rectal tissue microbiome diversity or the relative abundance of most bacteria, except for 2 oral-originating bacteria that were previously associated with colorectal cancer presence.
背景:越来越多的证据表明,居住在结直肠组织中的细菌可能与结直肠癌(CRC)有关。先前的研究调查了饮食干预对粪便微生物组的影响,但很少评估结直肠组织微生物组的终点。在息肉预防试验(PPT)中,我们研究了高纤维、高水果和蔬菜、低脂肪饮食干预对直肠组织微生物组的影响。方法:PPT是一项为期4年的随机临床试验,干预目标为:1)每1000千卡/天摄入≥18克纤维;2)每1000千卡/天≥3.5份水果和蔬菜;3)结果:干预对直肠组织α多样性的影响无统计学意义。与对照组相比,优先选择的卟啉单胞菌的相对丰度(T1 vs T0的绝对干预效应[标准误差]=-0.24 [0.07],T4 vs T0=-0.12 [0.07];P = 0.004)和普雷沃氏菌(T1 vs T0=-0.40[0.14]和T4 vs T0=-0.32[0.15]的绝对干预效应;P = 0.01),在干预组下降更为明显。结论:PPT干预不影响直肠组织微生物组的多样性,也不影响大多数细菌的相对丰度,除了两种先前与结直肠癌存在相关的口腔起源细菌。原始临床试验注册号:NCT00339625。
期刊介绍:
The Journal of the National Cancer Institute is a reputable publication that undergoes a peer-review process. It is available in both print (ISSN: 0027-8874) and online (ISSN: 1460-2105) formats, with 12 issues released annually. The journal's primary aim is to disseminate innovative and important discoveries in the field of cancer research, with specific emphasis on clinical, epidemiologic, behavioral, and health outcomes studies. Authors are encouraged to submit reviews, minireviews, and commentaries. The journal ensures that submitted manuscripts undergo a rigorous and expedited review to publish scientifically and medically significant findings in a timely manner.