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

26 Citations (Scopus)

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) or white 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 chromatography-mass 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
JournalThe American journal of clinical nutrition
Volume109
Issue number6
DOIs
Publication statusPublished - 1 Jun 2019
MoE publication typeA1 Journal article-refereed

Funding

The study was supported by the Academy of Finland and Biocenter Finland, International Agency for Research on Cancer, Region Languedoc-Roussillon, Agropolis Fondation, Organisation de Coopération et de Développement Economiques (OCDE), Association Franco-Finlandaise pour la Recherche Scientifique et Technique (AFFRST), and the French National Education Ministry. The intervention study was carried out as a part of the FIBREFECTS (Grain fiber modification for gut mediated health effects) funded mainly by TEKES—the Finnish Funding Agency for Technology and Innovation—and to a smaller extent by Oy Karl Fazer Ab, Vaasan Oy, and Ravintoraisio Oy. The study was also supported by a grant from Raisio plc Research Foundation to JL, and by grants from the Nordic Centre of Excellence to MK (SYSDIET; 070014) and to HM (HELGA; 070015).

Keywords

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

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