Decreased plasma serotonin and other metabolite changes in healthy adults after consumption of wholegrain rye: An untargeted metabolomics study

Pekka Keski-Rahkonen (Corresponding Author), Marjukka Kolehmainen, Jenni Lappi, Valerie Micard, Jenna Jokkala, Natalia Rosa-Sibakov, Jussi Pihlajamäki, Pirkka V. Kirjavainen, Hannu Mykkänen, Kaisa Poutanen, Marc J. Gunter, Augustin Scalbert, Kati Hanhineva

Research output: Contribution to journalArticleScientificpeer-review

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Abstract

Background: Wholegrain consumption has been associated with beneficial health effects including reduction of diabetes and cancer risk; however, the underlying mechanisms are not fully understood. Objective: The aim of this study was to characterize the effects of wholegrain rye intake on circulating metabolites in a human intervention study using untargeted metabolomics. Methods: The intervention consisted of 2 successive 4-wk periods in a randomized crossover design, where 15 adults consumed wholegrain rye bread (WGR) orwhite wheat bread enriched with fermented rye bran (WW+RB), following a 4-wk rye-free period with white wheat bread (WW). Fasting plasma samples were collected at the end of each period and analyzed using liquid chromatographymass spectrometry. Metabolic profiles were compared to identify compounds discriminating WGR from the WW+RB and WW periods. Because peripheral serotonin is produced mainly in the gut, a hypothesis of its altered biosynthesis as a response to increased cereal fiber intake was tested by measuring intestinal serotonin of mice fed for 9 wk on a high-fat diet supplemented with different sources of fiber (rye bran flour, ground wheat aleurone, or powdered cellulose). Results: Five endogenous metabolites and 15 rye phytochemicals associated with WGR intake were identified. Plasma concentrations of serotonin, taurine, and glycerophosphocholine were significantly lower after the WGR than WW period (Q > 0.05). Concentrations of 2 phosphatidylethanolamine plasmalogens, PE(18:2/P-18:0) and PE(18:2/P-16:0), were lower after the WGR period than the WW+RB period (Q > 0.05). The concentration of serotonin was significantly lower in the colonic tissue of mice that consumed rye bran or wheat aleurone compared with cellulose (P< 0.001). Conclusions: Wholegrain rye intake decreases plasma serotonin in healthy adults when compared with refined wheat. Intake of rye bran and wheat aleurone decreases colonic serotonin in mice. These results suggest that peripheral serotonin could be a potential link between wholegrain consumption and its associated health effects. Data used in the study were derived from a trial registered at www.clinicaltrials.gov as NCT03550365.

Original languageEnglish
Pages (from-to)1630-1639
Number of pages10
JournalThe American journal of clinical nutrition
Volume109
Issue number6
DOIs
Publication statusPublished - 26 Apr 2019
MoE publication typeA1 Journal article-refereed

Fingerprint

Metabolomics
Bread
Serotonin
Triticum
Dietary Fiber
Cellulose
Secale
Metabolome
Taurine
Health
Phytochemicals
High Fat Diet
Flour
Cross-Over Studies
Fasting
Spectrum Analysis

Keywords

  • 5-HT
  • alkylresorcinol
  • dietary intervention
  • glycerophosphocholine
  • metabolomics
  • plasmalogen
  • rye
  • serotonin
  • taurine
  • wholegrain

Cite this

Keski-Rahkonen, Pekka ; Kolehmainen, Marjukka ; Lappi, Jenni ; Micard, Valerie ; Jokkala, Jenna ; Rosa-Sibakov, Natalia ; Pihlajamäki, Jussi ; Kirjavainen, Pirkka V. ; Mykkänen, Hannu ; Poutanen, Kaisa ; Gunter, Marc J. ; Scalbert, Augustin ; Hanhineva, Kati. / Decreased plasma serotonin and other metabolite changes in healthy adults after consumption of wholegrain rye : An untargeted metabolomics study. In: The American journal of clinical nutrition. 2019 ; Vol. 109, No. 6. pp. 1630-1639.
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title = "Decreased plasma serotonin and other metabolite changes in healthy adults after consumption of wholegrain rye: An untargeted metabolomics study",
abstract = "Background: Wholegrain consumption has been associated with beneficial health effects including reduction of diabetes and cancer risk; however, the underlying mechanisms are not fully understood. Objective: The aim of this study was to characterize the effects of wholegrain rye intake on circulating metabolites in a human intervention study using untargeted metabolomics. Methods: The intervention consisted of 2 successive 4-wk periods in a randomized crossover design, where 15 adults consumed wholegrain rye bread (WGR) orwhite wheat bread enriched with fermented rye bran (WW+RB), following a 4-wk rye-free period with white wheat bread (WW). Fasting plasma samples were collected at the end of each period and analyzed using liquid chromatographymass spectrometry. Metabolic profiles were compared to identify compounds discriminating WGR from the WW+RB and WW periods. Because peripheral serotonin is produced mainly in the gut, a hypothesis of its altered biosynthesis as a response to increased cereal fiber intake was tested by measuring intestinal serotonin of mice fed for 9 wk on a high-fat diet supplemented with different sources of fiber (rye bran flour, ground wheat aleurone, or powdered cellulose). Results: Five endogenous metabolites and 15 rye phytochemicals associated with WGR intake were identified. Plasma concentrations of serotonin, taurine, and glycerophosphocholine were significantly lower after the WGR than WW period (Q > 0.05). Concentrations of 2 phosphatidylethanolamine plasmalogens, PE(18:2/P-18:0) and PE(18:2/P-16:0), were lower after the WGR period than the WW+RB period (Q > 0.05). The concentration of serotonin was significantly lower in the colonic tissue of mice that consumed rye bran or wheat aleurone compared with cellulose (P< 0.001). Conclusions: Wholegrain rye intake decreases plasma serotonin in healthy adults when compared with refined wheat. Intake of rye bran and wheat aleurone decreases colonic serotonin in mice. These results suggest that peripheral serotonin could be a potential link between wholegrain consumption and its associated health effects. Data used in the study were derived from a trial registered at www.clinicaltrials.gov as NCT03550365.",
keywords = "5-HT, alkylresorcinol, dietary intervention, glycerophosphocholine, metabolomics, plasmalogen, rye, serotonin, taurine, wholegrain",
author = "Pekka Keski-Rahkonen and Marjukka Kolehmainen and Jenni Lappi and Valerie Micard and Jenna Jokkala and Natalia Rosa-Sibakov and Jussi Pihlajam{\"a}ki and Kirjavainen, {Pirkka V.} and Hannu Mykk{\"a}nen and Kaisa Poutanen and Gunter, {Marc J.} and Augustin Scalbert and Kati Hanhineva",
year = "2019",
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doi = "10.1093/ajcn/nqy394",
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Keski-Rahkonen, P, Kolehmainen, M, Lappi, J, Micard, V, Jokkala, J, Rosa-Sibakov, N, Pihlajamäki, J, Kirjavainen, PV, Mykkänen, H, Poutanen, K, Gunter, MJ, Scalbert, A & Hanhineva, K 2019, 'Decreased plasma serotonin and other metabolite changes in healthy adults after consumption of wholegrain rye: An untargeted metabolomics study', The American journal of clinical nutrition, vol. 109, no. 6, pp. 1630-1639. https://doi.org/10.1093/ajcn/nqy394

Decreased plasma serotonin and other metabolite changes in healthy adults after consumption of wholegrain rye : An untargeted metabolomics study. / Keski-Rahkonen, Pekka (Corresponding Author); Kolehmainen, Marjukka; Lappi, Jenni; Micard, Valerie; Jokkala, Jenna; Rosa-Sibakov, Natalia; Pihlajamäki, Jussi; Kirjavainen, Pirkka V.; Mykkänen, Hannu; Poutanen, Kaisa; Gunter, Marc J.; Scalbert, Augustin; Hanhineva, Kati.

In: The American journal of clinical nutrition, Vol. 109, No. 6, 26.04.2019, p. 1630-1639.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Decreased plasma serotonin and other metabolite changes in healthy adults after consumption of wholegrain rye

T2 - An untargeted metabolomics study

AU - Keski-Rahkonen, Pekka

AU - Kolehmainen, Marjukka

AU - Lappi, Jenni

AU - Micard, Valerie

AU - Jokkala, Jenna

AU - Rosa-Sibakov, Natalia

AU - Pihlajamäki, Jussi

AU - Kirjavainen, Pirkka V.

AU - Mykkänen, Hannu

AU - Poutanen, Kaisa

AU - Gunter, Marc J.

AU - Scalbert, Augustin

AU - Hanhineva, Kati

PY - 2019/4/26

Y1 - 2019/4/26

N2 - Background: Wholegrain consumption has been associated with beneficial health effects including reduction of diabetes and cancer risk; however, the underlying mechanisms are not fully understood. Objective: The aim of this study was to characterize the effects of wholegrain rye intake on circulating metabolites in a human intervention study using untargeted metabolomics. Methods: The intervention consisted of 2 successive 4-wk periods in a randomized crossover design, where 15 adults consumed wholegrain rye bread (WGR) orwhite wheat bread enriched with fermented rye bran (WW+RB), following a 4-wk rye-free period with white wheat bread (WW). Fasting plasma samples were collected at the end of each period and analyzed using liquid chromatographymass spectrometry. Metabolic profiles were compared to identify compounds discriminating WGR from the WW+RB and WW periods. Because peripheral serotonin is produced mainly in the gut, a hypothesis of its altered biosynthesis as a response to increased cereal fiber intake was tested by measuring intestinal serotonin of mice fed for 9 wk on a high-fat diet supplemented with different sources of fiber (rye bran flour, ground wheat aleurone, or powdered cellulose). Results: Five endogenous metabolites and 15 rye phytochemicals associated with WGR intake were identified. Plasma concentrations of serotonin, taurine, and glycerophosphocholine were significantly lower after the WGR than WW period (Q > 0.05). Concentrations of 2 phosphatidylethanolamine plasmalogens, PE(18:2/P-18:0) and PE(18:2/P-16:0), were lower after the WGR period than the WW+RB period (Q > 0.05). The concentration of serotonin was significantly lower in the colonic tissue of mice that consumed rye bran or wheat aleurone compared with cellulose (P< 0.001). Conclusions: Wholegrain rye intake decreases plasma serotonin in healthy adults when compared with refined wheat. Intake of rye bran and wheat aleurone decreases colonic serotonin in mice. These results suggest that peripheral serotonin could be a potential link between wholegrain consumption and its associated health effects. Data used in the study were derived from a trial registered at www.clinicaltrials.gov as NCT03550365.

AB - Background: Wholegrain consumption has been associated with beneficial health effects including reduction of diabetes and cancer risk; however, the underlying mechanisms are not fully understood. Objective: The aim of this study was to characterize the effects of wholegrain rye intake on circulating metabolites in a human intervention study using untargeted metabolomics. Methods: The intervention consisted of 2 successive 4-wk periods in a randomized crossover design, where 15 adults consumed wholegrain rye bread (WGR) orwhite wheat bread enriched with fermented rye bran (WW+RB), following a 4-wk rye-free period with white wheat bread (WW). Fasting plasma samples were collected at the end of each period and analyzed using liquid chromatographymass spectrometry. Metabolic profiles were compared to identify compounds discriminating WGR from the WW+RB and WW periods. Because peripheral serotonin is produced mainly in the gut, a hypothesis of its altered biosynthesis as a response to increased cereal fiber intake was tested by measuring intestinal serotonin of mice fed for 9 wk on a high-fat diet supplemented with different sources of fiber (rye bran flour, ground wheat aleurone, or powdered cellulose). Results: Five endogenous metabolites and 15 rye phytochemicals associated with WGR intake were identified. Plasma concentrations of serotonin, taurine, and glycerophosphocholine were significantly lower after the WGR than WW period (Q > 0.05). Concentrations of 2 phosphatidylethanolamine plasmalogens, PE(18:2/P-18:0) and PE(18:2/P-16:0), were lower after the WGR period than the WW+RB period (Q > 0.05). The concentration of serotonin was significantly lower in the colonic tissue of mice that consumed rye bran or wheat aleurone compared with cellulose (P< 0.001). Conclusions: Wholegrain rye intake decreases plasma serotonin in healthy adults when compared with refined wheat. Intake of rye bran and wheat aleurone decreases colonic serotonin in mice. These results suggest that peripheral serotonin could be a potential link between wholegrain consumption and its associated health effects. Data used in the study were derived from a trial registered at www.clinicaltrials.gov as NCT03550365.

KW - 5-HT

KW - alkylresorcinol

KW - dietary intervention

KW - glycerophosphocholine

KW - metabolomics

KW - plasmalogen

KW - rye

KW - serotonin

KW - taurine

KW - wholegrain

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U2 - 10.1093/ajcn/nqy394

DO - 10.1093/ajcn/nqy394

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JO - The American journal of clinical nutrition

JF - The American journal of clinical nutrition

SN - 0002-9165

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