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. 2024 Dec;167(7):1371-1383.e4.
doi: 10.1053/j.gastro.2024.07.040. Epub 2024 Aug 6.

An Empirical Dietary Pattern Associated With the Gut Microbial Features in Relation to Colorectal Cancer Risk

Kai Wang  1 , Chun-Han Lo  2 , Raaj S Mehta  3 , Long H Nguyen  4 , Yiqing Wang  3 , Wenjie Ma  3 , Tomotaka Ugai  5 , Hidetaka Kawamura  5 , Satoko Ugai  5 , Yasutoshi Takashima  5 , Kosuke Mima  5 , Kota Arima  5 , Kazuo Okadome  5 , Marios Giannakis  6 , Cynthia L Sears  7 , Jeffrey A Meyerhardt  6 , Kimmie Ng  6 , Nicola Segata  8 , Jacques Izard  9 , Eric B Rimm  10 , Wendy S Garrett  11 , Curtis Huttenhower  12 , Edward L Giovannucci  13 , Andrew T Chan  14 , Shuji Ogino  15 , Mingyang Song  16
Affiliations

An Empirical Dietary Pattern Associated With the Gut Microbial Features in Relation to Colorectal Cancer Risk

Kai Wang et al. Gastroenterology. 2024 Dec.

Abstract

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.

Keywords: Cohort Study; Colorectal Cancer; Dietary Pattern; Gut Microbiome.

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Conflict of interest statement

Competing interests

All authors have completed the ICMJE uniform disclosure form at http://www.icmje.org/coi_disclosure.pdf. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Andrew T. Chan previously served as a consultant for Bayer Pharma AG, Pfizer Inc., and Boeheringer Ingelheim for work unrelated to the topic of this manuscript. Cynthia L. Sears has grant funding from Bristol Myers Squibb and Janssen for work unrelated to the topic of this manuscript. This study was not funded by Bayer Pharma AG, Pfizer Inc., Boeheringer Ingelheim, Bristol Myers Squibb, or Janssen. No other conflict of interest exists.

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