Butyrylated starch intake can prevent red meat induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue

a randomised clinical trial

Richard K Le Leu, Jean M Winter, Claus T Christophersen, Graeme P Young, Karen J Humphreys, Ying Hu, Silvia W Gratz, Rosalind B Miller, David L Topping, Anthony R Bird, Michael A Conlon

Research output: Contribution to journalArticle

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Abstract

Epidemiological studies have identified increased colorectal cancer (CRC) risk with high red meat (HRM) intakes, whereas dietary fibre intake appears to be protective. In the present study, we examined whether a HRM diet increased rectal O6-methyl-2-deoxyguanosine (O6MeG) adduct levels in healthy human subjects, and whether butyrylated high-amylose maize starch (HAMSB) was protective. A group of twenty-three individuals consumed 300 g/d of cooked red meat without (HRM diet) or with 40 g/d of HAMSB (HRM+HAMSB diet) over 4-week periods separated by a 4-week washout in a randomised cross-over design. Stool and rectal biopsy samples were collected for biochemical, microbial and immunohistochemical analyses at baseline and at the end of each 4-week intervention period. The HRM diet increased rectal O6MeG adducts relative to its baseline by 21 % (P< 0·01), whereas the addition of HAMSB to the HRM diet prevented this increase. Epithelial proliferation increased with both the HRM (P< 0·001) and HRM+HAMSB (P< 0·05) diets when compared with their respective baseline levels, but was lower following the HRM+HAMSB diet compared with the HRM diet (P< 0·05). Relative to its baseline, the HRM+HAMSB diet increased the excretion of SCFA by over 20 % (P< 0·05) and increased the absolute abundances of the Clostridium coccoides group (P< 0·05), the Clostridiumleptum group (P< 0·05), Lactobacillus spp. (P< 0·01), Parabacteroides distasonis (P< 0·001) and Ruminococcus bromii (P< 0·05), but lowered Ruminococcus torques (P< 0·05) and the proportions of Ruminococcus gnavus, Ruminococcus torques and Escherichia coli (P< 0·01). HRM consumption could increase the risk of CRC through increased formation of colorectal epithelial O6MeG adducts. HAMSB consumption prevented red meat-induced adduct formation, which may be associated with increased stool SCFA levels and/or changes in the microbiota composition.
Original languageEnglish
Pages (from-to)220-230
Number of pages11
JournalBritish Journal of Nutrition
Volume114
Issue number02
Early online date17 Jun 2015
DOIs
Publication statusPublished - Jul 2015

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Deoxyguanosine
Starch
Randomized Controlled Trials
Diet
Ruminococcus
Torque
Red Meat
Colorectal Neoplasms
Amylose
Clostridium
Microbiota
Dietary Fiber
Lactobacillus
Cross-Over Studies
Zea mays
Epidemiologic Studies

Keywords

  • SCFA
  • butyrate
  • DNA adducts
  • resistant starch
  • red meat
  • fermentation
  • microbiota

Cite this

Le Leu, R. K., Winter, J. M., Christophersen, C. T., Young, G. P., Humphreys, K. J., Hu, Y., ... Conlon, M. A. (2015). Butyrylated starch intake can prevent red meat induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue: a randomised clinical trial. British Journal of Nutrition, 114(02), 220-230. https://doi.org/10.1017/S0007114515001750

Butyrylated starch intake can prevent red meat induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue : a randomised clinical trial. / Le Leu, Richard K; Winter, Jean M; Christophersen, Claus T ; Young, Graeme P; Humphreys, Karen J ; Hu, Ying; Gratz, Silvia W; Miller, Rosalind B ; Topping, David L ; Bird, Anthony R; Conlon, Michael A.

In: British Journal of Nutrition, Vol. 114, No. 02, 07.2015, p. 220-230.

Research output: Contribution to journalArticle

Le Leu, RK, Winter, JM, Christophersen, CT, Young, GP, Humphreys, KJ, Hu, Y, Gratz, SW, Miller, RB, Topping, DL, Bird, AR & Conlon, MA 2015, 'Butyrylated starch intake can prevent red meat induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue: a randomised clinical trial', British Journal of Nutrition, vol. 114, no. 02, pp. 220-230. https://doi.org/10.1017/S0007114515001750
Le Leu, Richard K ; Winter, Jean M ; Christophersen, Claus T ; Young, Graeme P ; Humphreys, Karen J ; Hu, Ying ; Gratz, Silvia W ; Miller, Rosalind B ; Topping, David L ; Bird, Anthony R ; Conlon, Michael A. / Butyrylated starch intake can prevent red meat induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue : a randomised clinical trial. In: British Journal of Nutrition. 2015 ; Vol. 114, No. 02. pp. 220-230.
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N2 - Epidemiological studies have identified increased colorectal cancer (CRC) risk with high red meat (HRM) intakes, whereas dietary fibre intake appears to be protective. In the present study, we examined whether a HRM diet increased rectal O6-methyl-2-deoxyguanosine (O6MeG) adduct levels in healthy human subjects, and whether butyrylated high-amylose maize starch (HAMSB) was protective. A group of twenty-three individuals consumed 300 g/d of cooked red meat without (HRM diet) or with 40 g/d of HAMSB (HRM+HAMSB diet) over 4-week periods separated by a 4-week washout in a randomised cross-over design. Stool and rectal biopsy samples were collected for biochemical, microbial and immunohistochemical analyses at baseline and at the end of each 4-week intervention period. The HRM diet increased rectal O6MeG adducts relative to its baseline by 21 % (P< 0·01), whereas the addition of HAMSB to the HRM diet prevented this increase. Epithelial proliferation increased with both the HRM (P< 0·001) and HRM+HAMSB (P< 0·05) diets when compared with their respective baseline levels, but was lower following the HRM+HAMSB diet compared with the HRM diet (P< 0·05). Relative to its baseline, the HRM+HAMSB diet increased the excretion of SCFA by over 20 % (P< 0·05) and increased the absolute abundances of the Clostridium coccoides group (P< 0·05), the Clostridiumleptum group (P< 0·05), Lactobacillus spp. (P< 0·01), Parabacteroides distasonis (P< 0·001) and Ruminococcus bromii (P< 0·05), but lowered Ruminococcus torques (P< 0·05) and the proportions of Ruminococcus gnavus, Ruminococcus torques and Escherichia coli (P< 0·01). HRM consumption could increase the risk of CRC through increased formation of colorectal epithelial O6MeG adducts. HAMSB consumption prevented red meat-induced adduct formation, which may be associated with increased stool SCFA levels and/or changes in the microbiota composition.

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KW - butyrate

KW - DNA adducts

KW - resistant starch

KW - red meat

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KW - microbiota

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