Kai Wang, Chun-Han Lo, Raaj S Mehta, Long H Nguyen, Yiqing Wang, Wenjie Ma, Tomotaka Ugai, Hidetaka Kawamura, Satoko Ugai, Yasutoshi Takashima, Kosuke Mima, Kota Arima, Kazuo Okadome, Marios Giannakis, Cynthia L Sears, Jeffrey A Meyerhardt, Kimmie Ng, Nicola Segata, Jacques Izard, Eric B Rimm, Wendy S Garrett, Curtis Huttenhower, Edward L Giovannucci, Andrew T Chan, Shuji Ogino, Mingyang Song
{"title":"与大肠癌风险相关的肠道微生物特征的经验饮食模式。","authors":"Kai Wang, Chun-Han Lo, Raaj S Mehta, Long H Nguyen, Yiqing Wang, Wenjie Ma, Tomotaka Ugai, Hidetaka Kawamura, Satoko Ugai, Yasutoshi Takashima, Kosuke Mima, Kota Arima, Kazuo Okadome, Marios Giannakis, Cynthia L Sears, Jeffrey A Meyerhardt, Kimmie Ng, Nicola Segata, Jacques Izard, Eric B Rimm, Wendy S Garrett, Curtis Huttenhower, Edward L Giovannucci, Andrew T Chan, Shuji Ogino, Mingyang Song","doi":"10.1053/j.gastro.2024.07.040","DOIUrl":null,"url":null,"abstract":"<p><strong>Background & aims: </strong>Epidemiologic evidence for dietary influence on colorectal cancer (CRC) risk through the gut microbiome remains limited.</p><p><strong>Methods: </strong>Leveraging 307 men and 212 women with stool metagenomes and dietary data, we characterized and validated a sex-specific dietary pattern associated with the CRC-related gut microbial signature (CRC Microbial Dietary Score [CMDS]). We evaluated the associations of CMDS with CRC risk according to Fusobacterium nucleatum, pks<sup>+</sup>Escherichia coli, and enterotoxigenic Bacteroides fragilis status in tumor tissue using Cox proportional hazards regression in the Health Professionals Follow-Up Study (1986-2018), Nurses' Health Study (1984-2020), and Nurses' Health Study II (1991-2019).</p><p><strong>Results: </strong>The CMDS was characterized by high industrially processed food and low unprocessed fiber-rich food intakes. In 259,200 participants, we documented 3854 incident CRC cases over 6,467,378 person-years of follow-up. CMDS was associated with a higher risk of CRC (P<sub>trend</sub> < .001), with a multivariable hazard ratio (HR<sub>Q5 vs Q1</sub>) of 1.25 (95% CI, 1.13-1.39). The association remained after adjusting for previously established dietary patterns, for example, the Western and prudent diets. Notably, the association was stronger for tumoral F nucleatum-positive (HR<sub>Q5 vs Q1</sub>, 2.51; 95% CI, 1.68-3.75; P<sub>trend</sub> < .001; P<sub>heterogeneity</sub> = .03, positivity vs negativity), pks<sup>+</sup>E coli-positive (HR<sub>Q5 vs Q1</sub>, 1.68; 95% CI, 0.84-3.38; P<sub>trend</sub> = .005; P<sub>heterogeneity</sub> = .01, positivity vs negativity), and enterotoxigenic Bacteroides fragilis-positive CRC (HR<sub>Q5 vs Q1</sub>, 2.06; 95% CI, 1.10-3.88; P<sub>trend</sub> = .016; P<sub>heterogeneity</sub> = .06, positivity vs negativity), compared with their negative counterparts.</p><p><strong>Conclusions: </strong>CMDS was associated with increased CRC risk, especially for tumors with detectable F nucleatum, pks<sup>+</sup>E coli, and enterotoxigenic Bacteroides fragilis in tissue. Our findings support a potential role of the gut microbiome underlying the dietary effects on CRC.</p>","PeriodicalId":12590,"journal":{"name":"Gastroenterology","volume":" ","pages":"1371-1383.e4"},"PeriodicalIF":25.7000,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11581916/pdf/","citationCount":"0","resultStr":"{\"title\":\"An Empirical Dietary Pattern Associated With the Gut Microbial Features in Relation to Colorectal Cancer Risk.\",\"authors\":\"Kai Wang, Chun-Han Lo, Raaj S Mehta, Long H Nguyen, Yiqing Wang, Wenjie Ma, Tomotaka Ugai, Hidetaka Kawamura, Satoko Ugai, Yasutoshi Takashima, Kosuke Mima, Kota Arima, Kazuo Okadome, Marios Giannakis, Cynthia L Sears, Jeffrey A Meyerhardt, Kimmie Ng, Nicola Segata, Jacques Izard, Eric B Rimm, Wendy S Garrett, Curtis Huttenhower, Edward L Giovannucci, Andrew T Chan, Shuji Ogino, Mingyang Song\",\"doi\":\"10.1053/j.gastro.2024.07.040\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background & aims: </strong>Epidemiologic evidence for dietary influence on colorectal cancer (CRC) risk through the gut microbiome remains limited.</p><p><strong>Methods: </strong>Leveraging 307 men and 212 women with stool metagenomes and dietary data, we characterized and validated a sex-specific dietary pattern associated with the CRC-related gut microbial signature (CRC Microbial Dietary Score [CMDS]). We evaluated the associations of CMDS with CRC risk according to Fusobacterium nucleatum, pks<sup>+</sup>Escherichia coli, and enterotoxigenic Bacteroides fragilis status in tumor tissue using Cox proportional hazards regression in the Health Professionals Follow-Up Study (1986-2018), Nurses' Health Study (1984-2020), and Nurses' Health Study II (1991-2019).</p><p><strong>Results: </strong>The CMDS was characterized by high industrially processed food and low unprocessed fiber-rich food intakes. In 259,200 participants, we documented 3854 incident CRC cases over 6,467,378 person-years of follow-up. CMDS was associated with a higher risk of CRC (P<sub>trend</sub> < .001), with a multivariable hazard ratio (HR<sub>Q5 vs Q1</sub>) of 1.25 (95% CI, 1.13-1.39). The association remained after adjusting for previously established dietary patterns, for example, the Western and prudent diets. Notably, the association was stronger for tumoral F nucleatum-positive (HR<sub>Q5 vs Q1</sub>, 2.51; 95% CI, 1.68-3.75; P<sub>trend</sub> < .001; P<sub>heterogeneity</sub> = .03, positivity vs negativity), pks<sup>+</sup>E coli-positive (HR<sub>Q5 vs Q1</sub>, 1.68; 95% CI, 0.84-3.38; P<sub>trend</sub> = .005; P<sub>heterogeneity</sub> = .01, positivity vs negativity), and enterotoxigenic Bacteroides fragilis-positive CRC (HR<sub>Q5 vs Q1</sub>, 2.06; 95% CI, 1.10-3.88; P<sub>trend</sub> = .016; P<sub>heterogeneity</sub> = .06, positivity vs negativity), compared with their negative counterparts.</p><p><strong>Conclusions: </strong>CMDS was associated with increased CRC risk, especially for tumors with detectable F nucleatum, pks<sup>+</sup>E coli, and enterotoxigenic Bacteroides fragilis in tissue. Our findings support a potential role of the gut microbiome underlying the dietary effects on CRC.</p>\",\"PeriodicalId\":12590,\"journal\":{\"name\":\"Gastroenterology\",\"volume\":\" \",\"pages\":\"1371-1383.e4\"},\"PeriodicalIF\":25.7000,\"publicationDate\":\"2024-12-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11581916/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Gastroenterology\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1053/j.gastro.2024.07.040\",\"RegionNum\":1,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/8/6 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"GASTROENTEROLOGY & HEPATOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Gastroenterology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1053/j.gastro.2024.07.040","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/8/6 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"GASTROENTEROLOGY & HEPATOLOGY","Score":null,"Total":0}
An Empirical Dietary Pattern Associated With the Gut Microbial Features in Relation to Colorectal Cancer Risk.
Background & aims: Epidemiologic evidence for dietary influence on colorectal cancer (CRC) risk through the gut microbiome remains limited.
Methods: Leveraging 307 men and 212 women with stool metagenomes and dietary data, we characterized and validated a sex-specific dietary pattern associated with the CRC-related gut microbial signature (CRC Microbial Dietary Score [CMDS]). We evaluated the associations of CMDS with CRC risk according to Fusobacterium nucleatum, pks+Escherichia coli, and enterotoxigenic Bacteroides fragilis status in tumor tissue using Cox proportional hazards regression in the Health Professionals Follow-Up Study (1986-2018), Nurses' Health Study (1984-2020), and Nurses' Health Study II (1991-2019).
Results: The CMDS was characterized by high industrially processed food and low unprocessed fiber-rich food intakes. In 259,200 participants, we documented 3854 incident CRC cases over 6,467,378 person-years of follow-up. CMDS was associated with a higher risk of CRC (Ptrend < .001), with a multivariable hazard ratio (HRQ5 vs Q1) of 1.25 (95% CI, 1.13-1.39). The association remained after adjusting for previously established dietary patterns, for example, the Western and prudent diets. Notably, the association was stronger for tumoral F nucleatum-positive (HRQ5 vs Q1, 2.51; 95% CI, 1.68-3.75; Ptrend < .001; Pheterogeneity = .03, positivity vs negativity), pks+E coli-positive (HRQ5 vs Q1, 1.68; 95% CI, 0.84-3.38; Ptrend = .005; Pheterogeneity = .01, positivity vs negativity), and enterotoxigenic Bacteroides fragilis-positive CRC (HRQ5 vs Q1, 2.06; 95% CI, 1.10-3.88; Ptrend = .016; Pheterogeneity = .06, positivity vs negativity), compared with their negative counterparts.
Conclusions: CMDS was associated with increased CRC risk, especially for tumors with detectable F nucleatum, pks+E coli, and enterotoxigenic Bacteroides fragilis in tissue. Our findings support a potential role of the gut microbiome underlying the dietary effects on CRC.
期刊介绍：
Gastroenterology is the most prominent journal in the field of gastrointestinal disease. It is the flagship journal of the American Gastroenterological Association and delivers authoritative coverage of clinical, translational, and basic studies of all aspects of the digestive system, including the liver and pancreas, as well as nutrition.
Some regular features of Gastroenterology include original research studies by leading authorities, comprehensive reviews and perspectives on important topics in adult and pediatric gastroenterology and hepatology. The journal also includes features such as editorials, correspondence, and commentaries, as well as special sections like "Mentoring, Education and Training Corner," "Diversity, Equity and Inclusion in GI," "Gastro Digest," "Gastro Curbside Consult," and "Gastro Grand Rounds."
Gastroenterology also provides digital media materials such as videos and "GI Rapid Reel" animations. It is abstracted and indexed in various databases including Scopus, Biological Abstracts, Current Contents, Embase, Nutrition Abstracts, Chemical Abstracts, Current Awareness in Biological Sciences, PubMed/Medline, and the Science Citation Index.
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