Association Between Sulfur-Metabolizing Bacterial Communities in Stool and Risk of Distal Colorectal Cancer in Men.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
04 2020
Historique:
received: 30 09 2019
revised: 06 12 2019
accepted: 24 12 2019
pubmed: 24 1 2020
medline: 11 7 2020
entrez: 24 1 2020
Statut: ppublish

Résumé

Sulfur-metabolizing microbes, which convert dietary sources of sulfur into genotoxic hydrogen sulfide (H We collected data from 51,529 men enrolled in the Health Professionals Follow-up Study since 1986 to determine the association between sulfur-metabolizing bacteria in stool and risk of CRC over 26 years of follow-up. First, in a subcohort of 307 healthy men, we profiled serial stool metagenomes and metatranscriptomes and assessed diet using semiquantitative food frequency questionnaires to identify food groups associated with 43 bacterial species involved in sulfur metabolism. We used these data to develop a sulfur microbial dietary score. We then used Cox proportional hazards modeling to evaluate adherence to this pattern among eligible individuals (n = 48,246) from 1986 through 2012 with risk for incident CRC. Foods associated with higher sulfur microbial diet scores included increased consumption of processed meats and low-calorie drinks and lower consumption of vegetables and legumes. Increased sulfur microbial diet scores were associated with risk of distal colon and rectal cancers, after adjusting for other risk factors (multivariable relative risk, highest vs lowest quartile, 1.43; 95% confidence interval 1.14-1.81; P-trend = .002). In contrast, sulfur microbial diet scores were not associated with risk of proximal colon cancer (multivariable relative risk 0.86; 95% CI 0.65-1.14; P-trend = .31). In an analysis of participants in the Health Professionals Follow-up Study, we found that long-term adherence to a dietary pattern associated with sulfur-metabolizing bacteria in stool was associated with an increased risk of distal CRC. Further studies are needed to determine how sulfur-metabolizing bacteria might contribute to CRC pathogenesis.

Sections du résumé

BACKGROUND & AIMS
Sulfur-metabolizing microbes, which convert dietary sources of sulfur into genotoxic hydrogen sulfide (H
METHODS
We collected data from 51,529 men enrolled in the Health Professionals Follow-up Study since 1986 to determine the association between sulfur-metabolizing bacteria in stool and risk of CRC over 26 years of follow-up. First, in a subcohort of 307 healthy men, we profiled serial stool metagenomes and metatranscriptomes and assessed diet using semiquantitative food frequency questionnaires to identify food groups associated with 43 bacterial species involved in sulfur metabolism. We used these data to develop a sulfur microbial dietary score. We then used Cox proportional hazards modeling to evaluate adherence to this pattern among eligible individuals (n = 48,246) from 1986 through 2012 with risk for incident CRC.
RESULTS
Foods associated with higher sulfur microbial diet scores included increased consumption of processed meats and low-calorie drinks and lower consumption of vegetables and legumes. Increased sulfur microbial diet scores were associated with risk of distal colon and rectal cancers, after adjusting for other risk factors (multivariable relative risk, highest vs lowest quartile, 1.43; 95% confidence interval 1.14-1.81; P-trend = .002). In contrast, sulfur microbial diet scores were not associated with risk of proximal colon cancer (multivariable relative risk 0.86; 95% CI 0.65-1.14; P-trend = .31).
CONCLUSIONS
In an analysis of participants in the Health Professionals Follow-up Study, we found that long-term adherence to a dietary pattern associated with sulfur-metabolizing bacteria in stool was associated with an increased risk of distal CRC. Further studies are needed to determine how sulfur-metabolizing bacteria might contribute to CRC pathogenesis.

Identifiants

pubmed: 31972239
pii: S0016-5085(20)30009-3
doi: 10.1053/j.gastro.2019.12.029
pmc: PMC7384232
mid: NIHMS1607831
pii:
doi:

Substances chimiques

Sulfur 70FD1KFU70

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1313-1325

Subventions

Organisme : Cancer Research UK
ID : C10674/A27140
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : P30 DK043351
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA152904
Pays : United States
Organisme : NIDDK NIH HHS
ID : K24 DK098311
Pays : United States
Organisme : NCI NIH HHS
ID : K07 CA218377
Pays : United States
Organisme : NCI NIH HHS
ID : R00 CA215314
Pays : United States
Organisme : NIDDK NIH HHS
ID : K01 DK120742
Pays : United States
Organisme : NIDDK NIH HHS
ID : L30 DK118604
Pays : United States
Organisme : NIDDK NIH HHS
ID : K99 DK119412
Pays : United States
Organisme : NCI NIH HHS
ID : R35 CA197735
Pays : United States
Organisme : NIDDK NIH HHS
ID : K01 DK110267
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA202704
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA055075
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA151993
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA167552
Pays : United States
Organisme : NCI NIH HHS
ID : L30 CA209764
Pays : United States
Organisme : NIDDK NIH HHS
ID : K23 DK125838
Pays : United States
Organisme : NIDCR NIH HHS
ID : U54 DE023798
Pays : United States
Organisme : NCI NIH HHS
ID : T32 CA009001
Pays : United States
Organisme : NCI NIH HHS
ID : UM1 CA167552
Pays : United States

Informations de copyright

Copyright © 2020 AGA Institute. Published by Elsevier Inc. All rights reserved.

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Auteurs

Long H Nguyen (LH)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Wenjie Ma (W)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

Dong D Wang (DD)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Yin Cao (Y)

Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, St Louis, Missouri; Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri.

Himel Mallick (H)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Broad Institute of MIT and Harvard, Cambridge, Massachusetts.

Teklu K Gerbaba (TK)

Department of Food Science & Technology, University of Nebraska, Lincoln, Nebraska.

Jason Lloyd-Price (J)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Broad Institute of MIT and Harvard, Cambridge, Massachusetts.

Galeb Abu-Ali (G)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

A Brantley Hall (AB)

Broad Institute of MIT and Harvard, Cambridge, Massachusetts.

Daniel Sikavi (D)

Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

David A Drew (DA)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Raaj S Mehta (RS)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

Cesar Arze (C)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Amit D Joshi (AD)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.

Yan Yan (Y)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Tobyn Branck (T)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Casey DuLong (C)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Kerry L Ivey (KL)

Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; South Australian Health and Medical Research Institute, Microbiome & Host Health Programme, Precision Medicine Theme, South Australia, Australia.

Shuji Ogino (S)

Broad Institute of MIT and Harvard, Cambridge, Massachusetts; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Cancer Immunology and Cancer Epidemiology Programs, Dana-Farber Harvard Cancer Center, Boston, Massachusetts; Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.

Eric B Rimm (EB)

Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Mingyang Song (M)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Wendy S Garrett (WS)

Broad Institute of MIT and Harvard, Cambridge, Massachusetts; Department of Medicine, Dana-Farber Cancer Institute, Boston, Massachusetts; Department of Immunology and Infectious Disease, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.

Jacques Izard (J)

Department of Food Science & Technology, University of Nebraska, Lincoln, Nebraska; Fred and Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, Nebraska.

Curtis Huttenhower (C)

Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Broad Institute of MIT and Harvard, Cambridge, Massachusetts. Electronic address: chuttenh@hsph.harvard.edu.

Andrew T Chan (AT)

Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts; Broad Institute of MIT and Harvard, Cambridge, Massachusetts; Department of Immunology and Infectious Disease, Harvard T.H. Chan School of Public Health, Boston, Massachusetts. Electronic address: achan@partners.org.

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Classifications MeSH