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The Sulfur Microbial Diet and Risk of Colorectal Cancer by Molecular Subtypes and Intratumoral Microbial Species in Adult Men.
Clin Transl Gastroenterol. 2021 08 01; 12(8):e00338.CT

Abstract

INTRODUCTION

We recently described the sulfur microbial diet, a pattern of intake associated with increased gut sulfur-metabolizing bacteria and incidence of distal colorectal cancer (CRC). We assessed whether this risk differed by CRC molecular subtypes or presence of intratumoral microbes involved in CRC pathogenesis (Fusobacterium nucleatum and Bifidobacterium spp.).

METHODS

We performed Cox proportional hazards modeling to examine the association between the sulfur microbial diet and incidence of overall and distal CRC by molecular and microbial subtype in the Health Professionals Follow-Up Study (1986-2012).

RESULTS

We documented 1,264 incident CRC cases among 48,246 men, approximately 40% of whom had available tissue data. After accounting for multiple hypothesis testing, the relationship between the sulfur microbial diet and CRC incidence did not differ by subtype. However, there was a suggestion of an association by prostaglandin synthase 2 (PTGS2) status with a multivariable adjusted hazard ratio for highest vs lowest tertile of sulfur microbial diet scores of 1.31 (95% confidence interval: 0.99-1.74, Ptrend = 0.07, Pheterogeneity = 0.04) for PTGS2-high CRC. The association of the sulfur microbial diet with distal CRC seemed to differ by the presence of intratumoral Bifidobacterium spp. with an adjusted hazard ratio for highest vs lowest tertile of sulfur microbial diet scores of 1.65 (95% confidence interval: 1.14-2.39, Ptrend = 0.01, Pheterogeneity = 0.03) for Bifidobacterium-negative distal CRC. We observed no apparent heterogeneity by other tested molecular markers.

DISCUSSION

Greater long-term adherence to the sulfur microbial diet could be associated with PTGS2-high and Bifidobacterium-negative distal CRC in men. Additional studies are needed to further characterize the role of gut microbial sulfur metabolism and CRC.

Authors+Show Affiliations

Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA.Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA. Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA. Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA. Department of Medicine, Dana-Farber Cancer Institute, Boston, Massachusetts, USA.Department of Food Science and Technology, University of Nebraska, Lincoln, Nebraska, USA. Fred and Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, Nebraska, USA.Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, St Louis, Missouri, USA. Alvin J. Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri, USA.Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA. Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA. Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA. Department of Immunology and Infectious Disease, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA. Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA. Cancer Immunology and Cancer Epidemiology Programs, Dana-Farber Harvard Cancer Center, Boston, Massachusetts, USA.Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA. Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA. Department of Immunology and Infectious Disease, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.

Pub Type(s)

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.

Language

eng

PubMed ID

34333506

Citation

Sikavi, Daniel R., et al. "The Sulfur Microbial Diet and Risk of Colorectal Cancer By Molecular Subtypes and Intratumoral Microbial Species in Adult Men." Clinical and Translational Gastroenterology, vol. 12, no. 8, 2021, pp. e00338.
Sikavi DR, Nguyen LH, Haruki K, et al. The Sulfur Microbial Diet and Risk of Colorectal Cancer by Molecular Subtypes and Intratumoral Microbial Species in Adult Men. Clin Transl Gastroenterol. 2021;12(8):e00338.
Sikavi, D. R., Nguyen, L. H., Haruki, K., Ugai, T., Ma, W., Wang, D. D., Thompson, K. N., Yan, Y., Branck, T., Wilkinson, J. E., Akimoto, N., Zhong, R., Lau, M. C., Mima, K., Kosumi, K., Morikawa, T., Rimm, E. B., Garrett, W. S., Izard, J., ... Chan, A. T. (2021). The Sulfur Microbial Diet and Risk of Colorectal Cancer by Molecular Subtypes and Intratumoral Microbial Species in Adult Men. Clinical and Translational Gastroenterology, 12(8), e00338. https://doi.org/10.14309/ctg.0000000000000338
Sikavi DR, et al. The Sulfur Microbial Diet and Risk of Colorectal Cancer By Molecular Subtypes and Intratumoral Microbial Species in Adult Men. Clin Transl Gastroenterol. 2021 08 1;12(8):e00338. PubMed PMID: 34333506.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The Sulfur Microbial Diet and Risk of Colorectal Cancer by Molecular Subtypes and Intratumoral Microbial Species in Adult Men. AU - Sikavi,Daniel R, AU - Nguyen,Long H, AU - Haruki,Koichiro, AU - Ugai,Tomotaka, AU - Ma,Wenjie, AU - Wang,Dong D, AU - Thompson,Kelsey N, AU - Yan,Yan, AU - Branck,Tobyn, AU - Wilkinson,Jeremy E, AU - Akimoto,Naohiko, AU - Zhong,Rong, AU - Lau,Mai Chan, AU - Mima,Kosuke, AU - Kosumi,Keisuke, AU - Morikawa,Teppei, AU - Rimm,Eric B, AU - Garrett,Wendy S, AU - Izard,Jacques, AU - Cao,Yin, AU - Song,Mingyang, AU - Huttenhower,Curtis, AU - Ogino,Shuji, AU - Chan,Andrew T, Y1 - 2021/08/01/ PY - 2020/11/06/received PY - 2021/03/05/accepted PY - 2021/8/1/entrez PY - 2021/8/2/pubmed PY - 2022/1/19/medline SP - e00338 EP - e00338 JF - Clinical and translational gastroenterology JO - Clin Transl Gastroenterol VL - 12 IS - 8 N2 - INTRODUCTION: We recently described the sulfur microbial diet, a pattern of intake associated with increased gut sulfur-metabolizing bacteria and incidence of distal colorectal cancer (CRC). We assessed whether this risk differed by CRC molecular subtypes or presence of intratumoral microbes involved in CRC pathogenesis (Fusobacterium nucleatum and Bifidobacterium spp.). METHODS: We performed Cox proportional hazards modeling to examine the association between the sulfur microbial diet and incidence of overall and distal CRC by molecular and microbial subtype in the Health Professionals Follow-Up Study (1986-2012). RESULTS: We documented 1,264 incident CRC cases among 48,246 men, approximately 40% of whom had available tissue data. After accounting for multiple hypothesis testing, the relationship between the sulfur microbial diet and CRC incidence did not differ by subtype. However, there was a suggestion of an association by prostaglandin synthase 2 (PTGS2) status with a multivariable adjusted hazard ratio for highest vs lowest tertile of sulfur microbial diet scores of 1.31 (95% confidence interval: 0.99-1.74, Ptrend = 0.07, Pheterogeneity = 0.04) for PTGS2-high CRC. The association of the sulfur microbial diet with distal CRC seemed to differ by the presence of intratumoral Bifidobacterium spp. with an adjusted hazard ratio for highest vs lowest tertile of sulfur microbial diet scores of 1.65 (95% confidence interval: 1.14-2.39, Ptrend = 0.01, Pheterogeneity = 0.03) for Bifidobacterium-negative distal CRC. We observed no apparent heterogeneity by other tested molecular markers. DISCUSSION: Greater long-term adherence to the sulfur microbial diet could be associated with PTGS2-high and Bifidobacterium-negative distal CRC in men. Additional studies are needed to further characterize the role of gut microbial sulfur metabolism and CRC. SN - 2155-384X UR - https://www.unboundmedicine.com/medline/citation/34333506/The_Sulfur_Microbial_Diet_and_Risk_of_Colorectal_Cancer_by_Molecular_Subtypes_and_Intratumoral_Microbial_Species_in_Adult_Men_ DB - PRIME DP - Unbound Medicine ER -