Race-dependent association of sulfidogenic bacteria with colorectal cancer

Cemal Yazici, Patricia G. Wolf, Hajwa Kim, Tzu Wen L. Cross, Karin Vermillion, Timothy Carroll, Gaius J. Augustus, Ece Mutlu, Lisa Tussing-Humphreys, Carol Braunschweig, Rosa M. Xicola, Barbara Jung, Xavier Llor, Nathan A. Ellis, H Rex Gaskins

Research output: Contribution to journalArticle

Abstract

Objective Colorectal cancer (CRC) incidence is higher in African Americans (AAs) compared with non-Hispanic whites (NHWs). A diet high in animal protein and fat is an environmental risk factor for CRC development. The intestinal microbiota is postulated to modulate the effects of diet in promoting or preventing CRC. Hydrogen sulfide, produced by autochthonous sulfidogenic bacteria, triggers proinflammatory pathways and hyperproliferation, and is genotoxic. We hypothesised that sulfidogenic bacterial abundance in colonic mucosa may be an environmental CRC risk factor that distinguishes AA and NHW. Design Colonic biopsies from uninvolved or healthy mucosa from CRC cases and tumour-free controls were collected prospectively from five medical centres in Chicago for association studies. Sulfidogenic bacterial abundance in uninvolved colonic mucosa of AA and NHW CRC cases was compared with normal mucosa of AA and NHW controls. In addition, 16S rDNA sequencing was performed in AA cases and controls. Correlations were examined among bacterial targets, race, disease status and dietary intake. Results AAs harboured a greater abundance of sulfidogenic bacteria compared with NHWs regardless of disease status. Bilophila wadsworthia-specific dsrA was more abundant in AA cases than controls. Linear discriminant analysis of 16S rRNA gene sequences revealed five sulfidogenic genera that were more abundant in AA cases. Fat and protein intake and daily servings of meat were significantly higher in AAs compared with NHWs, and multiple dietary components correlated with a higher abundance of sulfidogenic bacteria. Conclusions These results implicate sulfidogenic bacteria as a potential environmental risk factor contributing to CRC development in AAs.

Original languageEnglish (US)
Pages (from-to)1983-1994
Number of pages12
JournalGut
Volume66
Issue number11
DOIs
StatePublished - Nov 1 2017

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African Americans
Colorectal Neoplasms
Bacteria
Mucous Membrane
Bilophila
Fats
Diet
Hydrogen Sulfide
Discriminant Analysis
Ribosomal DNA
rRNA Genes
Meat
Proteins
Biopsy
Incidence

Keywords

  • COLONIC MICROFLORA
  • COLORECTAL CANCER
  • HYDROGEN SULPHIDE

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Yazici, C., Wolf, P. G., Kim, H., Cross, T. W. L., Vermillion, K., Carroll, T., ... Gaskins, H. R. (2017). Race-dependent association of sulfidogenic bacteria with colorectal cancer. Gut, 66(11), 1983-1994. https://doi.org/10.1136/gutjnl-2016-313321

Race-dependent association of sulfidogenic bacteria with colorectal cancer. / Yazici, Cemal; Wolf, Patricia G.; Kim, Hajwa; Cross, Tzu Wen L.; Vermillion, Karin; Carroll, Timothy; Augustus, Gaius J.; Mutlu, Ece; Tussing-Humphreys, Lisa; Braunschweig, Carol; Xicola, Rosa M.; Jung, Barbara; Llor, Xavier; Ellis, Nathan A.; Gaskins, H Rex.

In: Gut, Vol. 66, No. 11, 01.11.2017, p. 1983-1994.

Research output: Contribution to journalArticle

Yazici, C, Wolf, PG, Kim, H, Cross, TWL, Vermillion, K, Carroll, T, Augustus, GJ, Mutlu, E, Tussing-Humphreys, L, Braunschweig, C, Xicola, RM, Jung, B, Llor, X, Ellis, NA & Gaskins, HR 2017, 'Race-dependent association of sulfidogenic bacteria with colorectal cancer', Gut, vol. 66, no. 11, pp. 1983-1994. https://doi.org/10.1136/gutjnl-2016-313321
Yazici C, Wolf PG, Kim H, Cross TWL, Vermillion K, Carroll T et al. Race-dependent association of sulfidogenic bacteria with colorectal cancer. Gut. 2017 Nov 1;66(11):1983-1994. https://doi.org/10.1136/gutjnl-2016-313321
Yazici, Cemal ; Wolf, Patricia G. ; Kim, Hajwa ; Cross, Tzu Wen L. ; Vermillion, Karin ; Carroll, Timothy ; Augustus, Gaius J. ; Mutlu, Ece ; Tussing-Humphreys, Lisa ; Braunschweig, Carol ; Xicola, Rosa M. ; Jung, Barbara ; Llor, Xavier ; Ellis, Nathan A. ; Gaskins, H Rex. / Race-dependent association of sulfidogenic bacteria with colorectal cancer. In: Gut. 2017 ; Vol. 66, No. 11. pp. 1983-1994.
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abstract = "Objective Colorectal cancer (CRC) incidence is higher in African Americans (AAs) compared with non-Hispanic whites (NHWs). A diet high in animal protein and fat is an environmental risk factor for CRC development. The intestinal microbiota is postulated to modulate the effects of diet in promoting or preventing CRC. Hydrogen sulfide, produced by autochthonous sulfidogenic bacteria, triggers proinflammatory pathways and hyperproliferation, and is genotoxic. We hypothesised that sulfidogenic bacterial abundance in colonic mucosa may be an environmental CRC risk factor that distinguishes AA and NHW. Design Colonic biopsies from uninvolved or healthy mucosa from CRC cases and tumour-free controls were collected prospectively from five medical centres in Chicago for association studies. Sulfidogenic bacterial abundance in uninvolved colonic mucosa of AA and NHW CRC cases was compared with normal mucosa of AA and NHW controls. In addition, 16S rDNA sequencing was performed in AA cases and controls. Correlations were examined among bacterial targets, race, disease status and dietary intake. Results AAs harboured a greater abundance of sulfidogenic bacteria compared with NHWs regardless of disease status. Bilophila wadsworthia-specific dsrA was more abundant in AA cases than controls. Linear discriminant analysis of 16S rRNA gene sequences revealed five sulfidogenic genera that were more abundant in AA cases. Fat and protein intake and daily servings of meat were significantly higher in AAs compared with NHWs, and multiple dietary components correlated with a higher abundance of sulfidogenic bacteria. Conclusions These results implicate sulfidogenic bacteria as a potential environmental risk factor contributing to CRC development in AAs.",
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AU - Carroll, Timothy

AU - Augustus, Gaius J.

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AU - Braunschweig, Carol

AU - Xicola, Rosa M.

AU - Jung, Barbara

AU - Llor, Xavier

AU - Ellis, Nathan A.

AU - Gaskins, H Rex

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N2 - Objective Colorectal cancer (CRC) incidence is higher in African Americans (AAs) compared with non-Hispanic whites (NHWs). A diet high in animal protein and fat is an environmental risk factor for CRC development. The intestinal microbiota is postulated to modulate the effects of diet in promoting or preventing CRC. Hydrogen sulfide, produced by autochthonous sulfidogenic bacteria, triggers proinflammatory pathways and hyperproliferation, and is genotoxic. We hypothesised that sulfidogenic bacterial abundance in colonic mucosa may be an environmental CRC risk factor that distinguishes AA and NHW. Design Colonic biopsies from uninvolved or healthy mucosa from CRC cases and tumour-free controls were collected prospectively from five medical centres in Chicago for association studies. Sulfidogenic bacterial abundance in uninvolved colonic mucosa of AA and NHW CRC cases was compared with normal mucosa of AA and NHW controls. In addition, 16S rDNA sequencing was performed in AA cases and controls. Correlations were examined among bacterial targets, race, disease status and dietary intake. Results AAs harboured a greater abundance of sulfidogenic bacteria compared with NHWs regardless of disease status. Bilophila wadsworthia-specific dsrA was more abundant in AA cases than controls. Linear discriminant analysis of 16S rRNA gene sequences revealed five sulfidogenic genera that were more abundant in AA cases. Fat and protein intake and daily servings of meat were significantly higher in AAs compared with NHWs, and multiple dietary components correlated with a higher abundance of sulfidogenic bacteria. Conclusions These results implicate sulfidogenic bacteria as a potential environmental risk factor contributing to CRC development in AAs.

AB - Objective Colorectal cancer (CRC) incidence is higher in African Americans (AAs) compared with non-Hispanic whites (NHWs). A diet high in animal protein and fat is an environmental risk factor for CRC development. The intestinal microbiota is postulated to modulate the effects of diet in promoting or preventing CRC. Hydrogen sulfide, produced by autochthonous sulfidogenic bacteria, triggers proinflammatory pathways and hyperproliferation, and is genotoxic. We hypothesised that sulfidogenic bacterial abundance in colonic mucosa may be an environmental CRC risk factor that distinguishes AA and NHW. Design Colonic biopsies from uninvolved or healthy mucosa from CRC cases and tumour-free controls were collected prospectively from five medical centres in Chicago for association studies. Sulfidogenic bacterial abundance in uninvolved colonic mucosa of AA and NHW CRC cases was compared with normal mucosa of AA and NHW controls. In addition, 16S rDNA sequencing was performed in AA cases and controls. Correlations were examined among bacterial targets, race, disease status and dietary intake. Results AAs harboured a greater abundance of sulfidogenic bacteria compared with NHWs regardless of disease status. Bilophila wadsworthia-specific dsrA was more abundant in AA cases than controls. Linear discriminant analysis of 16S rRNA gene sequences revealed five sulfidogenic genera that were more abundant in AA cases. Fat and protein intake and daily servings of meat were significantly higher in AAs compared with NHWs, and multiple dietary components correlated with a higher abundance of sulfidogenic bacteria. Conclusions These results implicate sulfidogenic bacteria as a potential environmental risk factor contributing to CRC development in AAs.

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