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Modification of subcutaneous white adipose tissue inflammation by omega-3 fatty acids is limited in human obesity-a double blind, randomised clinical trial

Modification of subcutaneous white adipose tissue inflammation by omega-3 fatty acids is limited in human obesity-a double blind, randomised clinical trial
Modification of subcutaneous white adipose tissue inflammation by omega-3 fatty acids is limited in human obesity-a double blind, randomised clinical trial

Background: Obesity is associated with enhanced inflammation. However, investigation in human subcutaneous white adipose tissue (scWAT) is limited and the mechanisms by which inflammation occurs have not been well elucidated. Marine long chain omega-3 polyunsaturated fatty acids (LC n-3 PUFAs) have anti-inflammatory actions and may reduce scWAT inflammation.

Methods: Subcutaneous white adipose tissue (scWAT) biopsies were collected from individuals living with obesity (n=45) and normal weight individuals (n=39) prior to and following a 12-week intervention with either 3 g/day of a fish oil concentrate (providing 1.1 g eicosapentaenoic acid (EPA) + 0.8 g docosahexaenoic acid (DHA)) or 3 g/day of corn oil. ScWAT fatty acid, oxylipin, and transcriptome profiles were assessed by gas chromatography, ultra-pure liquid chromatography tandem mass spectrometry, RNA sequencing and qRT-PCR, respectively.

Findings: Obesity was associated with greater scWAT inflammation demonstrated by lower concentrations of specialised pro-resolving mediators (SPMs) and hydroxy-DHA metabolites and an altered transcriptome with differential expression of genes involved in LC n-3 PUFA activation, oxylipin synthesis, inflammation, and immune response. Intervention with LC n-3 PUFAs increased their respective metabolites including the SPM precursor 14-hydroxy-DHA in normal weight individuals and decreased arachidonic acid derived metabolites and expression of genes involved in immune and inflammatory response with a greater effect in normal weight individuals.

Interpretation: Downregulated expression of genes responsible for fatty acid activation and metabolism may contribute to an inflammatory oxylipin profile and limit the effects of LC n-3 PUFAs in obesity. There may be a need for personalised LC n-3 PUFA supplementation based on obesity status.

Funding: European Commission Seventh Framework Programme (Grant Number 244995) and Czech Academy of Sciences (Lumina quaeruntur LQ200111901).

Adipose tissue, Immune system, Inflammation, LC n-3 PUFA, Lipids, Obesity
2352-3964
Fisk, Helena L.
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Childs, Caroline E.
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Miles, Elizabeth A.
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Ayres, Robert
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Noakes, Paul S.
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Paras-Chavez, Carolina
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Kuda, Ondrej
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Kopecký, Jan
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Antoun, Elie
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Lillycrop, Karen A.
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Calder, Philip C.
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Fisk, Helena L.
38c7f1f0-5dfc-4f71-aa0f-ec4f0e5839f3
Childs, Caroline E.
9a03fa65-53fe-428f-bf8c-1efe134f3d12
Miles, Elizabeth A.
20332899-ecdb-4214-95bc-922dde36d416
Ayres, Robert
da3a1f2b-432f-46f8-857f-ceae18ce7b40
Noakes, Paul S.
0ed50cd9-de73-4851-8039-ee72860d8ae5
Paras-Chavez, Carolina
f0170853-485a-4ef7-bc03-727884b13dbd
Kuda, Ondrej
cbc45f70-44cf-421a-be89-2d5213be9591
Kopecký, Jan
fc750f70-c5d6-499b-8da7-0bb307b44526
Antoun, Elie
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Lillycrop, Karen A.
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Calder, Philip C.
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Fisk, Helena L., Childs, Caroline E., Miles, Elizabeth A., Ayres, Robert, Noakes, Paul S., Paras-Chavez, Carolina, Kuda, Ondrej, Kopecký, Jan, Antoun, Elie, Lillycrop, Karen A. and Calder, Philip C. (2022) Modification of subcutaneous white adipose tissue inflammation by omega-3 fatty acids is limited in human obesity-a double blind, randomised clinical trial. EBioMedicine, 77, [103909]. (doi:10.1016/j.ebiom.2022.103909).

Record type: Article

Abstract

Background: Obesity is associated with enhanced inflammation. However, investigation in human subcutaneous white adipose tissue (scWAT) is limited and the mechanisms by which inflammation occurs have not been well elucidated. Marine long chain omega-3 polyunsaturated fatty acids (LC n-3 PUFAs) have anti-inflammatory actions and may reduce scWAT inflammation.

Methods: Subcutaneous white adipose tissue (scWAT) biopsies were collected from individuals living with obesity (n=45) and normal weight individuals (n=39) prior to and following a 12-week intervention with either 3 g/day of a fish oil concentrate (providing 1.1 g eicosapentaenoic acid (EPA) + 0.8 g docosahexaenoic acid (DHA)) or 3 g/day of corn oil. ScWAT fatty acid, oxylipin, and transcriptome profiles were assessed by gas chromatography, ultra-pure liquid chromatography tandem mass spectrometry, RNA sequencing and qRT-PCR, respectively.

Findings: Obesity was associated with greater scWAT inflammation demonstrated by lower concentrations of specialised pro-resolving mediators (SPMs) and hydroxy-DHA metabolites and an altered transcriptome with differential expression of genes involved in LC n-3 PUFA activation, oxylipin synthesis, inflammation, and immune response. Intervention with LC n-3 PUFAs increased their respective metabolites including the SPM precursor 14-hydroxy-DHA in normal weight individuals and decreased arachidonic acid derived metabolites and expression of genes involved in immune and inflammatory response with a greater effect in normal weight individuals.

Interpretation: Downregulated expression of genes responsible for fatty acid activation and metabolism may contribute to an inflammatory oxylipin profile and limit the effects of LC n-3 PUFAs in obesity. There may be a need for personalised LC n-3 PUFA supplementation based on obesity status.

Funding: European Commission Seventh Framework Programme (Grant Number 244995) and Czech Academy of Sciences (Lumina quaeruntur LQ200111901).

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Accepted/In Press date: 16 February 2022
e-pub ahead of print date: 2 March 2022
Published date: 2 March 2022
Additional Information: Funding Information: We acknowledge the European Commission for providing funding through its Seventh Framework Programme (grant number 244995) and EPAX, Norway, for the supply of the fish oil and corn oil capsules used in the study. Funding Information: P.C. Calder undertakes unpaid voluntary work as the current President of the Federation of European Nutrition Societies (FENS) and as Past President of ILSI Europe. P.C Calder received funding from the European Commission Seventh Framework Programme (Grant Number 244995). O. Kuda received funding from the Czech Academy of Sciences (Lumina quaeruntur LQ200111901). K.A. Lillycrop holds a contract with Benevolent AI Ltd. E.A. Miles received payment from Abbott Nutrition to present at The British Society for Allergy & Clinical Immunology (BSACI) conference in 2019. There are no other declarations of interests. Publisher Copyright: © 2022 The Author(s) Copyright: Copyright 2022 Elsevier B.V., All rights reserved.
Keywords: Adipose tissue, Immune system, Inflammation, LC n-3 PUFA, Lipids, Obesity

Identifiers

Local EPrints ID: 456533
URI: http://eprints.soton.ac.uk/id/eprint/456533
ISSN: 2352-3964
PURE UUID: e18e1acc-a8cd-46ee-ba85-37887256cacd
ORCID for Elizabeth A. Miles: ORCID iD orcid.org/0000-0002-8643-0655
ORCID for Paul S. Noakes: ORCID iD orcid.org/0000-0002-2678-1971
ORCID for Karen A. Lillycrop: ORCID iD orcid.org/0000-0001-7350-5489
ORCID for Philip C. Calder: ORCID iD orcid.org/0000-0002-6038-710X

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Date deposited: 04 May 2022 17:11
Last modified: 06 Jan 2023 02:41

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Contributors

Author: Helena L. Fisk
Author: Caroline E. Childs
Author: Robert Ayres
Author: Paul S. Noakes ORCID iD
Author: Carolina Paras-Chavez
Author: Ondrej Kuda
Author: Jan Kopecký
Author: Elie Antoun

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