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Diets That Promote Colon Inflammation Associate With Risk of Colorectal Carcinomas That Contain Fusobacterium nucleatum.
Clin Gastroenterol Hepatol. 2018 10; 16(10):1622-1631.e3.CG

Abstract

BACKGROUND & AIMS

Specific nutritional components are likely to induce intestinal inflammation, which is characterized by increased levels of interleukin 6 (IL6), C-reactive protein (CRP), and tumor necrosis factor-receptor superfamily member 1B (TNFRSF1B) in the circulation and promotes colorectal carcinogenesis. The inflammatory effects of a diet can be estimated based on an empiric dietary inflammatory pattern (EDIP) score, calculated based on intake of 18 foods associated with plasma levels of IL6, CRP, and TNFRSF1B. An inflammatory environment in the colon (based on increased levels of IL6, CRP, and TNFRSF1B in peripheral blood) contributes to impairment of the mucosal barrier and altered immune cell responses, affecting the composition of the intestinal microbiota. Colonization by Fusobacterium nucleatum has been associated with the presence and features of colorectal adenocarcinoma. We investigated the association between diets that promote inflammation (based on EDIP score) and colorectal cancer subtypes classified by level of F nucleatum in the tumor microenvironment.

METHODS

We calculated EDIP scores based on answers to food frequency questionnaires collected from participants in the Nurses' Health Study (through June 1, 2012) and the Health Professionals Follow-up Study (through January 31, 2012). Participants in both cohorts reported diagnoses of rectal or colon cancer in biennial questionnaires; deaths from unreported colorectal cancer cases were identified through the National Death Index and next of kin. Colorectal tumor tissues were collected from hospitals where the patients underwent tumor resection and F nucleatum DNA was quantified by a polymerase chain reaction assay. We used multivariable duplication-method Cox proportional hazard regression to assess the associations of EDIP scores with risks of colorectal cancer subclassified by F nucleatum status.

RESULTS

During 28 years of follow-up evaluation of 124,433 participants, we documented 951 incident cases of colorectal carcinoma with tissue F nucleatum data. Higher EDIP scores were associated with increased risk of F nucleatum-positive colorectal tumors (Ptrend = .03); for subjects in the highest vs lowest EDIP score tertiles, the hazard ratio for F nucleatum-positive colorectal tumors was 1.63 (95% CI, 1.03-2.58). EDIP scores did not associate with F nucleatum-negative tumors (Ptrend = .44). High EDIP scores associated with proximal F nucleatum-positive colorectal tumors but not with proximal F nucleatum-negative colorectal tumors (Pheterogeneity = .003).

CONCLUSIONS

Diets that may promote intestinal inflammation, based on EDIP score, are associated with increased risk of F nucleatum-positive colorectal carcinomas, but not carcinomas that do not contain these bacteria. These findings indicate that diet-induced intestinal inflammation alters the gut microbiome to contribute to colorectal carcinogenesis; nutritional interventions might be used in precision medicine and cancer prevention.

Authors+Show Affiliations

Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Department of Epidemiology and Biostatistics, Ministry of Education Key Lab of Environment and Health, School of Public Health, Huazhong University of Science and Technology, Wuhan, People's Republic of China.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.Channing Division of Network Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.The 7th Affiliated Hospital of Sun Yat-Sen University, Sun Yat-Sen University, Shenzhen, People's Republic of China.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts; Division of Gastroenterology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts.Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, St. Louis, Missouri.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; Medical Oncology Department 2, Chinese People's Liberation Army General Hospital, Beijing, People's Republic of China.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; Cancer Center, Wuhan Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, People's Republic of China.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; College of Pharmacy, Zhejiang Chinese Medical University, Hangzhou, People's Republic of China.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; Oncology Department, The First Affiliated Hospital of Chinese People's Liberation Army General Hospital, Beijing, People's Republic of China.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts; Division of Gastroenterology, Massachusetts General Hospital, 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; Channing Division of Network Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.Section on Pathophysiology and Molecular Pharmacology, Joslin Diabetes Center, Boston, Massachusetts; Section on Islet Cell and Regenerative Biology, Joslin Diabetes Center, Boston, Massachusetts; Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts.Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; Broad Institute of Massachusetts Institute of Technology, Harvard, Cambridge, Massachusetts.Broad Institute of Massachusetts Institute of Technology, Harvard, Cambridge, Massachusetts; Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Broad Institute of Massachusetts Institute of Technology, Harvard, Cambridge, Massachusetts.Channing Division of Network Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts; Division of Gastroenterology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts; Broad Institute of Massachusetts Institute of Technology, Harvard, Cambridge, Massachusetts.Yale Cancer Center, New Haven, Connecticut; Department of Medicine, Yale School of Medicine, New Haven, Connecticut; Smilow Cancer Hospital, New Haven, Connecticut.Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; Broad Institute of Massachusetts Institute of Technology, Harvard, Cambridge, Massachusetts; Program in MPE Molecular Pathological Epidemiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts; Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts; Broad Institute of Massachusetts Institute of Technology, Harvard, Cambridge, Massachusetts; Program in MPE Molecular Pathological Epidemiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts. Electronic address: shuji_ogino@dfci.harvard.edu.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; Channing Division of Network Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.

Pub Type(s)

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

Language

eng

PubMed ID

29702299

Citation

Liu, Li, et al. "Diets That Promote Colon Inflammation Associate With Risk of Colorectal Carcinomas That Contain Fusobacterium Nucleatum." Clinical Gastroenterology and Hepatology : the Official Clinical Practice Journal of the American Gastroenterological Association, vol. 16, no. 10, 2018, pp. 1622-1631.e3.
Liu L, Tabung FK, Zhang X, et al. Diets That Promote Colon Inflammation Associate With Risk of Colorectal Carcinomas That Contain Fusobacterium nucleatum. Clin Gastroenterol Hepatol. 2018;16(10):1622-1631.e3.
Liu, L., Tabung, F. K., Zhang, X., Nowak, J. A., Qian, Z. R., Hamada, T., Nevo, D., Bullman, S., Mima, K., Kosumi, K., da Silva, A., Song, M., Cao, Y., Twombly, T. S., Shi, Y., Liu, H., Gu, M., Koh, H., Li, W., ... Giovannucci, E. L. (2018). Diets That Promote Colon Inflammation Associate With Risk of Colorectal Carcinomas That Contain Fusobacterium nucleatum. Clinical Gastroenterology and Hepatology : the Official Clinical Practice Journal of the American Gastroenterological Association, 16(10), 1622-e3. https://doi.org/10.1016/j.cgh.2018.04.030
Liu L, et al. Diets That Promote Colon Inflammation Associate With Risk of Colorectal Carcinomas That Contain Fusobacterium Nucleatum. Clin Gastroenterol Hepatol. 2018;16(10):1622-1631.e3. PubMed PMID: 29702299.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Diets That Promote Colon Inflammation Associate With Risk of Colorectal Carcinomas That Contain Fusobacterium nucleatum. AU - Liu,Li, AU - Tabung,Fred K, AU - Zhang,Xuehong, AU - Nowak,Jonathan A, AU - Qian,Zhi Rong, AU - Hamada,Tsuyoshi, AU - Nevo,Daniel, AU - Bullman,Susan, AU - Mima,Kosuke, AU - Kosumi,Keisuke, AU - da Silva,Annacarolina, AU - Song,Mingyang, AU - Cao,Yin, AU - Twombly,Tyler S, AU - Shi,Yan, AU - Liu,Hongli, AU - Gu,Mancang, AU - Koh,Hideo, AU - Li,Wanwan, AU - Du,Chunxia, AU - Chen,Yang, AU - Li,Chenxi, AU - Li,Wenbin, AU - Mehta,Raaj S, AU - Wu,Kana, AU - Wang,Molin, AU - Kostic,Aleksander D, AU - Giannakis,Marios, AU - Garrett,Wendy S, AU - Hutthenhower,Curtis, AU - Chan,Andrew T, AU - Fuchs,Charles S, AU - Nishihara,Reiko, AU - Ogino,Shuji, AU - Giovannucci,Edward L, Y1 - 2018/04/24/ PY - 2017/11/20/received PY - 2018/02/28/revised PY - 2018/04/15/accepted PY - 2018/4/28/pubmed PY - 2019/11/15/medline PY - 2018/4/28/entrez KW - Immunity KW - Microsatellite Instability KW - Nutrition KW - Red Meat SP - 1622 EP - 1631.e3 JF - Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association JO - Clin. Gastroenterol. Hepatol. VL - 16 IS - 10 N2 - BACKGROUND & AIMS: Specific nutritional components are likely to induce intestinal inflammation, which is characterized by increased levels of interleukin 6 (IL6), C-reactive protein (CRP), and tumor necrosis factor-receptor superfamily member 1B (TNFRSF1B) in the circulation and promotes colorectal carcinogenesis. The inflammatory effects of a diet can be estimated based on an empiric dietary inflammatory pattern (EDIP) score, calculated based on intake of 18 foods associated with plasma levels of IL6, CRP, and TNFRSF1B. An inflammatory environment in the colon (based on increased levels of IL6, CRP, and TNFRSF1B in peripheral blood) contributes to impairment of the mucosal barrier and altered immune cell responses, affecting the composition of the intestinal microbiota. Colonization by Fusobacterium nucleatum has been associated with the presence and features of colorectal adenocarcinoma. We investigated the association between diets that promote inflammation (based on EDIP score) and colorectal cancer subtypes classified by level of F nucleatum in the tumor microenvironment. METHODS: We calculated EDIP scores based on answers to food frequency questionnaires collected from participants in the Nurses' Health Study (through June 1, 2012) and the Health Professionals Follow-up Study (through January 31, 2012). Participants in both cohorts reported diagnoses of rectal or colon cancer in biennial questionnaires; deaths from unreported colorectal cancer cases were identified through the National Death Index and next of kin. Colorectal tumor tissues were collected from hospitals where the patients underwent tumor resection and F nucleatum DNA was quantified by a polymerase chain reaction assay. We used multivariable duplication-method Cox proportional hazard regression to assess the associations of EDIP scores with risks of colorectal cancer subclassified by F nucleatum status. RESULTS: During 28 years of follow-up evaluation of 124,433 participants, we documented 951 incident cases of colorectal carcinoma with tissue F nucleatum data. Higher EDIP scores were associated with increased risk of F nucleatum-positive colorectal tumors (Ptrend = .03); for subjects in the highest vs lowest EDIP score tertiles, the hazard ratio for F nucleatum-positive colorectal tumors was 1.63 (95% CI, 1.03-2.58). EDIP scores did not associate with F nucleatum-negative tumors (Ptrend = .44). High EDIP scores associated with proximal F nucleatum-positive colorectal tumors but not with proximal F nucleatum-negative colorectal tumors (Pheterogeneity = .003). CONCLUSIONS: Diets that may promote intestinal inflammation, based on EDIP score, are associated with increased risk of F nucleatum-positive colorectal carcinomas, but not carcinomas that do not contain these bacteria. These findings indicate that diet-induced intestinal inflammation alters the gut microbiome to contribute to colorectal carcinogenesis; nutritional interventions might be used in precision medicine and cancer prevention. SN - 1542-7714 UR - https://www.unboundmedicine.com/medline/citation/29702299/Diets_That_Promote_Colon_Inflammation_Associate_With_Risk_of_Colorectal_Carcinomas_That_Contain_Fusobacterium_nucleatum_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1542-3565(18)30389-6 DB - PRIME DP - Unbound Medicine ER -