Association of dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue

Raaj S. Mehta, Reiko Nishihara, Yin Cao, Mingyang Song, Kosuke Mima, Zhi Rong Qian, Jonathan A. Nowak, Keisuke Kosumi, Tsuyoshi Hamada, Yohei Masugi, Susan Bullman, David A. Drew, Aleksandar D. Kostic, Teresa T. Fung, Wendy S. Garrett, Curtis Huttenhower, Kana Wu, Jeffrey A. Meyerhardt, Xuehong Zhang, Walter C. Willett & 4 others Edward L. Giovannucci, Charles S. Fuchs, Andrew T. Chan, Shuji Ogino

Research output: Contribution to journalArticle

62 Citations (Scopus)

Abstract

IMPORTANCE: Fusobacterium nucleatum appears to play a role in colorectal carcinogenesis through suppression of the hosts’ immune response to tumor. Evidence also suggests that diet influences intestinal F nucleatum. However, the role of F nucleatum in mediating the relationship between diet and the risk of colorectal cancer is unknown. OBJECTIVE: To test the hypothesis that the associations of prudent diets (rich in whole grains and dietary fiber) and Western diets (rich in red and processed meat, refined grains, and desserts) with colorectal cancer risk may differ according to the presence of F nucleatum in tumor tissue. DESIGN, SETTING, AND PARTICIPANTS: A prospective cohort study was conducted using data from the Nurses’ Health Study (June 1, 1980, to June 1, 2012) and the Health Professionals Follow-up Study (June 1, 1986, to June 1, 2012) on a total of 121 700 US female nurses and 51 529 US male health professionals aged 30 to 55 years and 40 to 75 years, respectively (both predominantly white individuals), at enrollment. Data analysis was performed from March 15, 2015, to August 10, 2016. EXPOSURES: Prudent and Western diets. MAIN OUTCOMES AND MEASURES: Incidence of colorectal carcinoma subclassified by F nucleatum status in tumor tissue, determined by quantitative polymerase chain reaction. RESULTS: Of the 173 229 individuals considered for the study, 137 217 were included in the analysis, 47 449 were male (34.6%), and mean (SD) baseline age for men was 54.0 (9.8) years and for women, 46.3 (7.2) years. A total of 1019 incident colon and rectal cancer cases with available F nucleatum data were documented over 26 to 32 years of follow-up, encompassing 3 643 562 person-years. The association of prudent diet with colorectal cancer significantly differed by tissue F nucleatum status (P = .01 for heterogeneity); prudent diet score was associated with a lower risk of F nucleatum–positive cancers (P = .003 for trend; multivariable hazard ratio of 0.43; 95% CI, 0.25-0.72, for the highest vs the lowest prudent score quartile) but not with F nucleatum–negative cancers (P = .47 for trend, the corresponding multivariable hazard ratio of 0.95; 95% CI, 0.77-1.17). There was no significant heterogeneity between the subgroups in relation to Western dietary pattern scores. CONCLUSIONS AND RELEVANCE: Prudent diets rich in whole grains and dietary fiber are associated with a lower risk for F nucleatum–positive colorectal cancer but not F nucleatum–negative cancer, supporting a potential role for intestinal microbiota in mediating the association between diet and colorectal neoplasms.

Original languageEnglish
Pages (from-to)921-927
Number of pages7
JournalJAMA oncology
Volume3
Issue number7
DOIs
Publication statusPublished - 2017 Jul 1
Externally publishedYes

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Fusobacterium nucleatum
Colorectal Neoplasms
Diet
Neoplasms
Dietary Fiber
Health
Nurses
Rectal Neoplasms
Colonic Neoplasms
Carcinogenesis
Cohort Studies
Prospective Studies
Polymerase Chain Reaction
Incidence

ASJC Scopus subject areas

  • Oncology
  • Cancer Research

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Association of dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue. / Mehta, Raaj S.; Nishihara, Reiko; Cao, Yin; Song, Mingyang; Mima, Kosuke; Qian, Zhi Rong; Nowak, Jonathan A.; Kosumi, Keisuke; Hamada, Tsuyoshi; Masugi, Yohei; Bullman, Susan; Drew, David A.; Kostic, Aleksandar D.; Fung, Teresa T.; Garrett, Wendy S.; Huttenhower, Curtis; Wu, Kana; Meyerhardt, Jeffrey A.; Zhang, Xuehong; Willett, Walter C.; Giovannucci, Edward L.; Fuchs, Charles S.; Chan, Andrew T.; Ogino, Shuji.

In: JAMA oncology, Vol. 3, No. 7, 01.07.2017, p. 921-927.

Research output: Contribution to journalArticle

Mehta, RS, Nishihara, R, Cao, Y, Song, M, Mima, K, Qian, ZR, Nowak, JA, Kosumi, K, Hamada, T, Masugi, Y, Bullman, S, Drew, DA, Kostic, AD, Fung, TT, Garrett, WS, Huttenhower, C, Wu, K, Meyerhardt, JA, Zhang, X, Willett, WC, Giovannucci, EL, Fuchs, CS, Chan, AT & Ogino, S 2017, 'Association of dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue', JAMA oncology, vol. 3, no. 7, pp. 921-927. https://doi.org/10.1001/jamaoncol.2016.6374
Mehta, Raaj S. ; Nishihara, Reiko ; Cao, Yin ; Song, Mingyang ; Mima, Kosuke ; Qian, Zhi Rong ; Nowak, Jonathan A. ; Kosumi, Keisuke ; Hamada, Tsuyoshi ; Masugi, Yohei ; Bullman, Susan ; Drew, David A. ; Kostic, Aleksandar D. ; Fung, Teresa T. ; Garrett, Wendy S. ; Huttenhower, Curtis ; Wu, Kana ; Meyerhardt, Jeffrey A. ; Zhang, Xuehong ; Willett, Walter C. ; Giovannucci, Edward L. ; Fuchs, Charles S. ; Chan, Andrew T. ; Ogino, Shuji. / Association of dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue. In: JAMA oncology. 2017 ; Vol. 3, No. 7. pp. 921-927.
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abstract = "IMPORTANCE: Fusobacterium nucleatum appears to play a role in colorectal carcinogenesis through suppression of the hosts’ immune response to tumor. Evidence also suggests that diet influences intestinal F nucleatum. However, the role of F nucleatum in mediating the relationship between diet and the risk of colorectal cancer is unknown. OBJECTIVE: To test the hypothesis that the associations of prudent diets (rich in whole grains and dietary fiber) and Western diets (rich in red and processed meat, refined grains, and desserts) with colorectal cancer risk may differ according to the presence of F nucleatum in tumor tissue. DESIGN, SETTING, AND PARTICIPANTS: A prospective cohort study was conducted using data from the Nurses’ Health Study (June 1, 1980, to June 1, 2012) and the Health Professionals Follow-up Study (June 1, 1986, to June 1, 2012) on a total of 121 700 US female nurses and 51 529 US male health professionals aged 30 to 55 years and 40 to 75 years, respectively (both predominantly white individuals), at enrollment. Data analysis was performed from March 15, 2015, to August 10, 2016. EXPOSURES: Prudent and Western diets. MAIN OUTCOMES AND MEASURES: Incidence of colorectal carcinoma subclassified by F nucleatum status in tumor tissue, determined by quantitative polymerase chain reaction. RESULTS: Of the 173 229 individuals considered for the study, 137 217 were included in the analysis, 47 449 were male (34.6{\%}), and mean (SD) baseline age for men was 54.0 (9.8) years and for women, 46.3 (7.2) years. A total of 1019 incident colon and rectal cancer cases with available F nucleatum data were documented over 26 to 32 years of follow-up, encompassing 3 643 562 person-years. The association of prudent diet with colorectal cancer significantly differed by tissue F nucleatum status (P = .01 for heterogeneity); prudent diet score was associated with a lower risk of F nucleatum–positive cancers (P = .003 for trend; multivariable hazard ratio of 0.43; 95{\%} CI, 0.25-0.72, for the highest vs the lowest prudent score quartile) but not with F nucleatum–negative cancers (P = .47 for trend, the corresponding multivariable hazard ratio of 0.95; 95{\%} CI, 0.77-1.17). There was no significant heterogeneity between the subgroups in relation to Western dietary pattern scores. CONCLUSIONS AND RELEVANCE: Prudent diets rich in whole grains and dietary fiber are associated with a lower risk for F nucleatum–positive colorectal cancer but not F nucleatum–negative cancer, supporting a potential role for intestinal microbiota in mediating the association between diet and colorectal neoplasms.",
author = "Mehta, {Raaj S.} and Reiko Nishihara and Yin Cao and Mingyang Song and Kosuke Mima and Qian, {Zhi Rong} and Nowak, {Jonathan A.} and Keisuke Kosumi and Tsuyoshi Hamada and Yohei Masugi and Susan Bullman and Drew, {David A.} and Kostic, {Aleksandar D.} and Fung, {Teresa T.} and Garrett, {Wendy S.} and Curtis Huttenhower and Kana Wu and Meyerhardt, {Jeffrey A.} and Xuehong Zhang and Willett, {Walter C.} and Giovannucci, {Edward L.} and Fuchs, {Charles S.} and Chan, {Andrew T.} and Shuji Ogino",
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TY - JOUR

T1 - Association of dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue

AU - Mehta, Raaj S.

AU - Nishihara, Reiko

AU - Cao, Yin

AU - Song, Mingyang

AU - Mima, Kosuke

AU - Qian, Zhi Rong

AU - Nowak, Jonathan A.

AU - Kosumi, Keisuke

AU - Hamada, Tsuyoshi

AU - Masugi, Yohei

AU - Bullman, Susan

AU - Drew, David A.

AU - Kostic, Aleksandar D.

AU - Fung, Teresa T.

AU - Garrett, Wendy S.

AU - Huttenhower, Curtis

AU - Wu, Kana

AU - Meyerhardt, Jeffrey A.

AU - Zhang, Xuehong

AU - Willett, Walter C.

AU - Giovannucci, Edward L.

AU - Fuchs, Charles S.

AU - Chan, Andrew T.

AU - Ogino, Shuji

PY - 2017/7/1

Y1 - 2017/7/1

N2 - IMPORTANCE: Fusobacterium nucleatum appears to play a role in colorectal carcinogenesis through suppression of the hosts’ immune response to tumor. Evidence also suggests that diet influences intestinal F nucleatum. However, the role of F nucleatum in mediating the relationship between diet and the risk of colorectal cancer is unknown. OBJECTIVE: To test the hypothesis that the associations of prudent diets (rich in whole grains and dietary fiber) and Western diets (rich in red and processed meat, refined grains, and desserts) with colorectal cancer risk may differ according to the presence of F nucleatum in tumor tissue. DESIGN, SETTING, AND PARTICIPANTS: A prospective cohort study was conducted using data from the Nurses’ Health Study (June 1, 1980, to June 1, 2012) and the Health Professionals Follow-up Study (June 1, 1986, to June 1, 2012) on a total of 121 700 US female nurses and 51 529 US male health professionals aged 30 to 55 years and 40 to 75 years, respectively (both predominantly white individuals), at enrollment. Data analysis was performed from March 15, 2015, to August 10, 2016. EXPOSURES: Prudent and Western diets. MAIN OUTCOMES AND MEASURES: Incidence of colorectal carcinoma subclassified by F nucleatum status in tumor tissue, determined by quantitative polymerase chain reaction. RESULTS: Of the 173 229 individuals considered for the study, 137 217 were included in the analysis, 47 449 were male (34.6%), and mean (SD) baseline age for men was 54.0 (9.8) years and for women, 46.3 (7.2) years. A total of 1019 incident colon and rectal cancer cases with available F nucleatum data were documented over 26 to 32 years of follow-up, encompassing 3 643 562 person-years. The association of prudent diet with colorectal cancer significantly differed by tissue F nucleatum status (P = .01 for heterogeneity); prudent diet score was associated with a lower risk of F nucleatum–positive cancers (P = .003 for trend; multivariable hazard ratio of 0.43; 95% CI, 0.25-0.72, for the highest vs the lowest prudent score quartile) but not with F nucleatum–negative cancers (P = .47 for trend, the corresponding multivariable hazard ratio of 0.95; 95% CI, 0.77-1.17). There was no significant heterogeneity between the subgroups in relation to Western dietary pattern scores. CONCLUSIONS AND RELEVANCE: Prudent diets rich in whole grains and dietary fiber are associated with a lower risk for F nucleatum–positive colorectal cancer but not F nucleatum–negative cancer, supporting a potential role for intestinal microbiota in mediating the association between diet and colorectal neoplasms.

AB - IMPORTANCE: Fusobacterium nucleatum appears to play a role in colorectal carcinogenesis through suppression of the hosts’ immune response to tumor. Evidence also suggests that diet influences intestinal F nucleatum. However, the role of F nucleatum in mediating the relationship between diet and the risk of colorectal cancer is unknown. OBJECTIVE: To test the hypothesis that the associations of prudent diets (rich in whole grains and dietary fiber) and Western diets (rich in red and processed meat, refined grains, and desserts) with colorectal cancer risk may differ according to the presence of F nucleatum in tumor tissue. DESIGN, SETTING, AND PARTICIPANTS: A prospective cohort study was conducted using data from the Nurses’ Health Study (June 1, 1980, to June 1, 2012) and the Health Professionals Follow-up Study (June 1, 1986, to June 1, 2012) on a total of 121 700 US female nurses and 51 529 US male health professionals aged 30 to 55 years and 40 to 75 years, respectively (both predominantly white individuals), at enrollment. Data analysis was performed from March 15, 2015, to August 10, 2016. EXPOSURES: Prudent and Western diets. MAIN OUTCOMES AND MEASURES: Incidence of colorectal carcinoma subclassified by F nucleatum status in tumor tissue, determined by quantitative polymerase chain reaction. RESULTS: Of the 173 229 individuals considered for the study, 137 217 were included in the analysis, 47 449 were male (34.6%), and mean (SD) baseline age for men was 54.0 (9.8) years and for women, 46.3 (7.2) years. A total of 1019 incident colon and rectal cancer cases with available F nucleatum data were documented over 26 to 32 years of follow-up, encompassing 3 643 562 person-years. The association of prudent diet with colorectal cancer significantly differed by tissue F nucleatum status (P = .01 for heterogeneity); prudent diet score was associated with a lower risk of F nucleatum–positive cancers (P = .003 for trend; multivariable hazard ratio of 0.43; 95% CI, 0.25-0.72, for the highest vs the lowest prudent score quartile) but not with F nucleatum–negative cancers (P = .47 for trend, the corresponding multivariable hazard ratio of 0.95; 95% CI, 0.77-1.17). There was no significant heterogeneity between the subgroups in relation to Western dietary pattern scores. CONCLUSIONS AND RELEVANCE: Prudent diets rich in whole grains and dietary fiber are associated with a lower risk for F nucleatum–positive colorectal cancer but not F nucleatum–negative cancer, supporting a potential role for intestinal microbiota in mediating the association between diet and colorectal neoplasms.

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