Overweight and underweight status are linked to specific gut microbiota and intestinal tricarboxylic acid cycle intermediates.


Journal

Clinical nutrition (Edinburgh, Scotland)
ISSN: 1532-1983
Titre abrégé: Clin Nutr
Pays: England
ID NLM: 8309603

Informations de publication

Date de publication:
10 2020
Historique:
received: 09 07 2019
revised: 04 01 2020
accepted: 10 02 2020
pubmed: 14 3 2020
medline: 17 8 2021
entrez: 14 3 2020
Statut: ppublish

Résumé

Intestinal short-chain fatty acids have been demonstrated to modulate host energy metabolism and are elevated in overweight and obese individuals. We hypothesized that other intestinal energy products especially tricarboxylic acid (TCA) cycle intermediates might also related to overweight status. In addition, little information is available regarding to the potential relationship between gut microbiota and underweight status. Therefore, the aim of this study was to investigate whether gut microbiota and intestinal energy metabolites differ in underweight, normal weight, and overweight individuals, and their correlations with host cardiometabolic risk factors. Gut microbiome, intestinal energy metabolites, circulating cardiometabolic risk factors, and proinflammatory markers were determined in 29 underweight, 67 normal weight, and 67 overweight adults. The fecal concentrations of succinic acid, fumaric acid, malic acid, propionic acid, and adipic acid were significantly increased in the overweight individuals in parallel with a higher relative abundance of Veillonellacea after adjusting for multiple comparisons (all p < 0.05). The intestinal concentration of TCA cycle intermediate succinic acid was positively associated with body weight (r = 0.28, p = 0.04), and malic acid were in positive association with circulating total cholesterol, low-density lipoprotein cholesterol, and interleukin-1β (all r > 0.25, p < 0.05). Compared with the normal weight individuals, the gut microbial α-diversity was lower in the overweight (p = 0.007 for Shannon index and p = 0.009 for Ace index) and underweight (p = 0.05 for Shannon index and p = 0.08 for Ace index) groups. However, no significant differences in the overall gut microbiota composition were observed among the three groups. Our findings revealed that low gut microbiota diversity was associated with both overweight and underweight status. Intestinal TCA cycle intermediates were associated with overweight development and might be potential markers for future studies related to gut microbiota and host cardiometabolic health.

Sections du résumé

BACKGROUND & AIMS
Intestinal short-chain fatty acids have been demonstrated to modulate host energy metabolism and are elevated in overweight and obese individuals. We hypothesized that other intestinal energy products especially tricarboxylic acid (TCA) cycle intermediates might also related to overweight status. In addition, little information is available regarding to the potential relationship between gut microbiota and underweight status. Therefore, the aim of this study was to investigate whether gut microbiota and intestinal energy metabolites differ in underweight, normal weight, and overweight individuals, and their correlations with host cardiometabolic risk factors.
SUBJECTS/METHODS
Gut microbiome, intestinal energy metabolites, circulating cardiometabolic risk factors, and proinflammatory markers were determined in 29 underweight, 67 normal weight, and 67 overweight adults.
RESULTS
The fecal concentrations of succinic acid, fumaric acid, malic acid, propionic acid, and adipic acid were significantly increased in the overweight individuals in parallel with a higher relative abundance of Veillonellacea after adjusting for multiple comparisons (all p < 0.05). The intestinal concentration of TCA cycle intermediate succinic acid was positively associated with body weight (r = 0.28, p = 0.04), and malic acid were in positive association with circulating total cholesterol, low-density lipoprotein cholesterol, and interleukin-1β (all r > 0.25, p < 0.05). Compared with the normal weight individuals, the gut microbial α-diversity was lower in the overweight (p = 0.007 for Shannon index and p = 0.009 for Ace index) and underweight (p = 0.05 for Shannon index and p = 0.08 for Ace index) groups. However, no significant differences in the overall gut microbiota composition were observed among the three groups.
CONCLUSIONS
Our findings revealed that low gut microbiota diversity was associated with both overweight and underweight status. Intestinal TCA cycle intermediates were associated with overweight development and might be potential markers for future studies related to gut microbiota and host cardiometabolic health.

Identifiants

pubmed: 32164980
pii: S0261-5614(20)30062-5
doi: 10.1016/j.clnu.2020.02.014
pii:
doi:

Substances chimiques

Biomarkers 0
Fatty Acids 0
Inflammation Mediators 0

Types de publication

Comparative Study Journal Article Observational Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3189-3198

Informations de copyright

Copyright © 2020 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest The authors declare no conflict of interest.

Auteurs

Yi Wan (Y)

Department of Food Science and Nutrition, Zhejiang University, Hangzhou, 310058, China; Department of Nutrition, Harvard T. H. Chan School of Public Health, Boston, 02115, USA.

Jihong Yuan (J)

No. 1 Department of Nutrition, Chinese People's Liberation Army General Hospital, Beijing, 100000, China.

Jie Li (J)

No. 1 Department of Nutrition, Chinese People's Liberation Army General Hospital, Beijing, 100000, China.

Hao Li (H)

Department of Food Science and Nutrition, Zhejiang University, Hangzhou, 310058, China.

Kanhua Yin (K)

Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, 02115, MA, USA.

Fenglei Wang (F)

Department of Nutrition, Harvard T. H. Chan School of Public Health, Boston, 02115, USA.

Duo Li (D)

Institute of Nutrition and Health, Qingdao University, Qingdao, 266071, China. Electronic address: duoli@qdu.edu.cn.

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Classifications MeSH