Characterization of diet-dependent temporal changes in circulating short-chain fatty acid concentrations: a randomized crossover dietary trial
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Author(s)
Type
Journal Article
Abstract
Background: Production of Short-chain fatty acids (SCFAs) from food is a complex and dynamic saccharolytic fermentation process mediated by both human and gut microbial factors. SCFA production and knowledge of the relationship between SCFA profiles and dietary patterns is lacking.
Objective: Temporal changes in SCFA levels in response to two contrasting diets were investigated using a novel GC-MS method.
Design: Samples were obtained from a randomized, controlled, crossover trial designed to characterize the metabolic response to four diets. Participants (n=19) undertook these diets during an inpatient stay (of 72-h). Serum samples were collected 2-h after breakfast (AB), lunch (AL) and dinner (AD) on day 3 and a fasting sample (FA) was obtained on day 4. 24-h urine samples were collected on day 3. In this sub-study, samples from the two extreme diets representing a diet with high adherence to WHO healthy eating recommendations and a typical Western diet were analyzed using a bespoke GC-MS method developed to detect and quantify 10 SCFAs and precursors in serum and urine samples.
Results: Considerable inter-individual variation in serum SCFA concentrations was observed across all time points and temporal fluctuations were observed for both diets. Although the sample collection timing exerted a greater magnitude of effect on circulating SCFA concentrations, the unhealthy diet was associated with a lower concentration of acetic acid (FA: coefficient=-17.0; standard error (SE)=5.8; p-trend=0.00615), 2-methylbutyric acid (AL: coefficient=-0.1; SE=0.028; p-trend=4.13x10-4 and AD: coefficient =-0.1; SE:=0.028; p-trend=2.28x10-3) and 2-hydroxybutyric acid (FA: coefficient=-15.8; standard error=5.11; p-trend: 4.09x10-3). In contrast lactic acid was significantly higher in the unhealthy diet (AL: coefficient=750.2; standard error=315.2; p-trend=0.024 and AD: coefficient=1219.3; standard error=322.6; p-trend: 8.28x10-4).
Conclusion: The GC-MS method allowed robust mapping of diurnal patterns in SCFA concentrations, which were impacted by diet and highlighted the importance of standardizing the timing of SCFA measurements in dietary studies.
Objective: Temporal changes in SCFA levels in response to two contrasting diets were investigated using a novel GC-MS method.
Design: Samples were obtained from a randomized, controlled, crossover trial designed to characterize the metabolic response to four diets. Participants (n=19) undertook these diets during an inpatient stay (of 72-h). Serum samples were collected 2-h after breakfast (AB), lunch (AL) and dinner (AD) on day 3 and a fasting sample (FA) was obtained on day 4. 24-h urine samples were collected on day 3. In this sub-study, samples from the two extreme diets representing a diet with high adherence to WHO healthy eating recommendations and a typical Western diet were analyzed using a bespoke GC-MS method developed to detect and quantify 10 SCFAs and precursors in serum and urine samples.
Results: Considerable inter-individual variation in serum SCFA concentrations was observed across all time points and temporal fluctuations were observed for both diets. Although the sample collection timing exerted a greater magnitude of effect on circulating SCFA concentrations, the unhealthy diet was associated with a lower concentration of acetic acid (FA: coefficient=-17.0; standard error (SE)=5.8; p-trend=0.00615), 2-methylbutyric acid (AL: coefficient=-0.1; SE=0.028; p-trend=4.13x10-4 and AD: coefficient =-0.1; SE:=0.028; p-trend=2.28x10-3) and 2-hydroxybutyric acid (FA: coefficient=-15.8; standard error=5.11; p-trend: 4.09x10-3). In contrast lactic acid was significantly higher in the unhealthy diet (AL: coefficient=750.2; standard error=315.2; p-trend=0.024 and AD: coefficient=1219.3; standard error=322.6; p-trend: 8.28x10-4).
Conclusion: The GC-MS method allowed robust mapping of diurnal patterns in SCFA concentrations, which were impacted by diet and highlighted the importance of standardizing the timing of SCFA measurements in dietary studies.
Date Issued
2022-11-01
Date Acceptance
2021-06-07
Citation
The American Journal of Clinical Nutrition, 2022, 116 (5), pp.1368-1378
ISSN
0002-9165
Publisher
Oxford University Press (OUP)
Start Page
1368
End Page
1378
Journal / Book Title
The American Journal of Clinical Nutrition
Volume
116
Issue
5
Copyright Statement
© The Author(s) 2022. Published by Oxford University Press on behalf of the American Society for Nutrition.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
License URL
Sponsor
Imperial College Healthcare NHS Trust- BRC Funding
Identifier
https://academic.oup.com/ajcn/advance-article/doi/10.1093/ajcn/nqab211/6711581?login=true
Grant Number
RDA27
Subjects
Science & Technology
Life Sciences & Biomedicine
Nutrition & Dietetics
short-chain fatty acids
branched-chain fatty acid
diet
fiber
metabolite
GC-MS
NITROGEN-METABOLISM ROLE
HUMAN LARGE-INTESTINE
GUT MICROBIOTA
APPETITE REGULATION
LIPID-METABOLISM
HUMAN-COLON
GLUCOSE
INSULIN
FERMENTATION
ACETATE
GC-MS
branched-chain fatty acid
diet
fiber
metabolite
short-chain fatty acids
Nutrition & Dietetics
09 Engineering
11 Medical and Health Sciences
Publication Status
Published
Date Publish Online
2022-09-22