Basic Study
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World J Gastroenterol. May 14, 2022; 28(18): 1965-1980
Published online May 14, 2022. doi: 10.3748/wjg.v28.i18.1965
Effect of ancient Khorasan wheat on gut microbiota, inflammation, and short-chain fatty acid production in patients with fibromyalgia
Simone Baldi, Giuditta Pagliai, Monica Dinu, Leandro Di Gloria, Giulia Nannini, Lavinia Curini, Marco Pallecchi, Edda Russo, Elena Niccolai, Giovanna Danza, Stefano Benedettelli, Giovanna Ballerini, Barbara Colombini, Gianluca Bartolucci, Matteo Ramazzotti, Francesco Sofi, Amedeo Amedei
Simone Baldi, Giuditta Pagliai, Monica Dinu, Leandro Di Gloria, Giulia Nannini, Lavinia Curini, Edda Russo, Elena Niccolai, Barbara Colombini, Francesco Sofi, Amedeo Amedei, Department of Experimental and Clinical Medicine, University of Florence, Florence 50134, Italy
Giuditta Pagliai, Monica Dinu, Francesco Sofi, Unit of Clinical Nutrition, Careggi University Hospital, Florence 50134, Italy
Marco Pallecchi, Gianluca Bartolucci, Department of Neurosciences, Psychology, Drug Research and Child Health, Section of Pharmaceutical and Nutraceutical Sciences, University of Florence, Sesto Fiorentino 50019, Italy
Giovanna Danza, Matteo Ramazzotti, Department of Biomedical, Experimental and Clinical Sciences “Mario Serio”, University of Florence, Florence 50134, Italy
Stefano Benedettelli, Department of Agriculture, Food, Environment and Forestry, University of Florence, Florence 50144, Italy
Giovanna Ballerini, Multidisciplinary Center for Pain Therapy, Reference Center for Fibromyalgia, Piero Palagi Hospital, USL Toscana Centro, Florence 50122, Italy
Amedeo Amedei, SOD of Interdisciplinary Internal Medicine, Careggi University Hospital, Florence 50134, Italy
Author contributions: Baldi S and Pagliai G contributed equally to writing the manuscript; Baldi S, Pagliai G, Dinu M, and Russo E contributed to paper conceptualization and design; Baldi S, Pagliai G, Dinu M, Ramazzotti M, Bartolucci G, Pallecchi M, Di Gloria L, Curini L, Nannini G, Niccolai E, and Russo E performed the research analysis; Amedei A, Sofi F, Ramazzotti M, Bartolucci G, Danza G, Ballerini G, Colombini B, and Benedettelli S critically revised the paper; Amedei A and Sofi F equally coordinated and supervised the research. All authors read and approved the final version of the manuscript.
Supported by a grant from Kamut Enterprises of Europe, Oudenaarde, Belgium.
Institutional review board statement: The study was approved by the local ethics committee “Comitato Etico Regionale per la Sperimentazione Clinica della Regione Toscana, Sezione AREA VASTA CENTRO” (SPE 12.630), and adhered to the principles of the Declaration of Helsinki and the Data Protection Act.
Informed consent statement: Informed written consent was obtained from the patients for publication of this report and any accompanying images.
Conflict-of-interest statement: The authors declare no competing interests for this article.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Amedeo Amedei, BSc, Reader (Associate Professor), Department of Experimental and Clinical Medicine, University of Florence, Largo Brambilla 3, Florence 50134, Italy. aamedei@unifi.it
Received: November 26, 2021
Peer-review started: November 26, 2021
First decision: January 8, 2022
Revised: January 19, 2022
Accepted: March 27, 2022
Article in press: March 27, 2022
Published online: May 14, 2022
Processing time: 166 Days and 17.1 Hours
Abstract
BACKGROUND

Fibromyalgia (FM) syndrome is mainly characterized by widespread pain, sleeping disorders, fatigue, and cognitive dysfunction. In many cases, gastrointestinal distress is also reported, suggesting the potential pathogenic role of the gut microbiota (GM). The GM is deeply influenced by several environmental factors, especially the diet, and recent findings highlighted significant symptom improvement in FM patients following various nutritional interventions such as vegetarian diet, low-fermentable oligosaccharides, disaccharides, monosaccharides, and polyols based diets, gluten-free diet, and especially an ancient grain supplementation. In particular, a recent study reported that a replacement diet with ancient Khorasan wheat led to an overall improvement in symptom severity of FM patients.

AIM

To examine the effects of ancient Khorasan wheat on the GM, inflammation, and short-chain fatty acid production in FM patients.

METHODS

After a 2-wk run-in period, 20 FM patients were enrolled in this randomized, double-blind crossover trial. In detail, they were assigned to consume either Khorasan or control wheat products for 8 wk and then, following an 8-wk washout period, crossed. Before and after treatments, GM characterization was performed by 16S rRNA sequencing while the fecal molecular inflammatory response and the short-chain fatty acids (SCFAs) were respectively determined with the Luminex MAGPIX detection system and a mass chromatography-mass spectrometry method.

RESULTS

The Khorasan wheat replacement diet, in comparison with the control wheat diet, had more positive effects on intestinal microbiota composition and on both the fecal immune and SCFAs profiles such as the significant increase of butyric acid levels (P = 0.054), candidatus Saccharibacteria (P = 9.95e-06) and Actinobacteria, and the reduction of Enterococcaceae (P = 4.97e-04). Moreover, the improvement of various FM symptoms along with the variation of some gut bacteria after the Khorasan wheat diet have been documented; in fact we reported positive correlations between Actinobacteria and both Tiredness Symptoms Scale (P < 0.001) and Functional Outcome of Sleep Questionnaire (P < 0.05) scores, between Verrucomicrobiae and both Widespread Pain Index (WPI) + Symptom Severity scale (SS) (P < 0.05) and WPI (P < 0.05) scores, between candidatus Saccharibacteria and SS score (P < 0.05), and between Bacteroidales and Sleep-Related and Safety Behaviour Questionnaire score (P < 0.05).

CONCLUSION

The replacement diet based on ancient Khorasan wheat results in beneficial GM compositional and functional modifications that positively correlate with an improvement of FM symptomatology.

Keywords: Fibromialgya; Gut microbiota; Khorasan wheat; Fibromialgya symptoms; Ancient wheat

Core Tip: Fibromyalgia (FM) syndrome is mainly characterized by widespread pain but in many cases, gastrointestinal distress is also reported, suggesting the potential pathogenic role of the intestinal microbiota. Since gut microbiota is deeply influenced by diet, significant symptom improvement has been reported in FM patients following various nutritional interventions such as vegetarian diet, low-fermentable oligosaccharides, disaccharides, monosaccharides, and polyols based diets, gluten-free diet, and especially an ancient grain based diet. We reported that a replacement diet based on ancient Khorasan wheat, compared to a control wheat diet, resulted in beneficial gut microbiota compositional and functional modifications that positively correlated with an improvement of FM symptomatology.