Distinct fatty acid signatures in infrapatellar fat pad and synovial fluid of patients with osteoarthritis versus rheumatoid arthritis

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Abstract

Background

Infrapatellar fat pad (IFP) has recently emerged as a potential source of inflammation in knee arthropathies. It has been proposed to be one source of adipocytokines, fatty acids (FA), and FA-derived lipid mediators that could contribute to the pathophysiological processes in the knee joint. Alterations in synovial fluid (SF) lipid composition have been linked to both osteoarthritis (OA) and rheumatoid arthritis (RA). The aim of the present study was to compare the FA signatures in the IFP and SF of RA and OA patients.

Methods

Pairs of IFP and SF samples were collected from the same knees of RA ( n = 10) and OA patients ( n = 10) undergoing total joint replacement surgery. Control SF samples ( n = 6) were harvested during diagnostic or therapeutic arthroscopic knee surgery unrelated to RA or OA. The FA composition in the total lipids of IFP and SF was determined by gas chromatography with flame ionization and mass spectrometric detection.

Results

Arthropathies resulted in a significant reduction in the SF proportions of n-6 polyunsaturated FA (PUFA), more pronouncedly in OA than in RA. OA was also characterized with reduced percentages of 22:6n-3 and lower product/precursor ratios of n-3 PUFA. The proportions of total monounsaturated FA increased in both RA and OA SF. Regarding IFP, RA patients had lower proportions of 20:4n-6, total n-6 PUFA, and 22:6n-3, as well as lower product/precursor ratios of n-3 PUFA compared to OA patients. The average chain length of SF FA decreased in both diagnoses and the double bond index in OA.

Conclusions

The observed complex alterations in the FA signatures could have both contributed to but also limited the inflammatory processes and cartilage destruction in the RA and OA knees.

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Most cited references 47

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Synovial inflammation, immune cells and their cytokines in osteoarthritis: a review.

B.J.E. de Lange-Brokaar, A Ioan-Facsinay, G.J.V.M. van Osch … (2012)

Although osteoarthritis (OA) is considered a non-inflammatory condition, it is widely accepted that synovial inflammation is a feature of OA. However, the role of immune cells and their cytokines in OA is largely unknown. This narrative systematic review summarizes the knowledge of inflammatory properties, immune cells and their cytokines in synovial tissues (STs) of OA patients. Broad literature search in different databases was performed which resulted in 100 articles. Of 100 articles 33 solely investigated inflammation in OA ST with or without comparison with normal samples; the remaining primarily focussed on rheumatoid arthritis (RA) ST. Studies investigating different severity stages or cellular source of cytokines were sparse. OA ST displayed mild/moderate grade inflammation when investigated by means of haematoxylin and eosin (H&E) staining. Most frequently found cells types were macrophages, T cells and mast cells (MCs). Overall the number of cells was lower than in RA, although the number of MCs was as high as or sometimes even higher than in RA ST. Cytokines related to T cell or macrophage function were found in OA ST. Their expression was overall higher than in normal ST, but lower than in RA ST. Their cellular source remains largely unknown in OA ST. Inflammation is common in OA ST and characterized by immune cell infiltration and cytokine secretion. This inflammation seems quantitatively and qualitatively different from inflammation in RA. Further research is needed to clarify the role of inflammation, immune cells and their cytokines in the pathogenesis of OA. Copyright © 2012 Osteoarthritis Research Society International. Published by Elsevier Ltd. All rights reserved.

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Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids.

Jing X. Kang, Jingdong Wang, Lin feng Wu … (2004)

Mammals cannot naturally produce omega-3 (n-3) fatty acids--beneficial nutrients found mainly in fish oil--from the more abundant omega-6 (n-6) fatty acids and so they must rely on a dietary supply. Here we show that mice engineered to carry a fat-1 gene from the roundworm Caenorhabditis elegans can add a double bond into an unsaturated fatty-acid hydrocarbon chain and convert n-6 to n-3 fatty acids. This results in an abundance of n-3 and a reduction in n-6 fatty acids in the organs and tissues of these mice, in the absence of dietary n-3. As well as presenting an opportunity to investigate the roles played by n-3 fatty acids in the body, our discovery indicates that this technology might be adapted to enrich n-3 fatty acids in animal products such as meat, milk and eggs.

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The infrapatellar fat pad of patients with osteoarthritis has an inflammatory phenotype.

I Klein-Wieringa, M. Kloppenburg, Y. Bastiaansen-Jenniskens … (2011)

Obesity is a risk factor for the development of osteoarthritis (OA) in hands and knees. Adipose tissue can secrete different adipokines with powerful immunomodulatory effects. The infrapatellar fat pad (IFP) is an intra-articular organ in the vicinity of the synovium and cartilage. It is hypothesised that IFP-derived soluble factors could contribute to pathological processes in the knee joint. A study was therefore undertaken to compare the release of inflammatory mediators in the IFP and subcutaneous adipose tissue (ScAT) and to characterise the adipocytes and immune cell infiltrate in these tissues. Paired IFP and ScAT samples were obtained from 27 patients with primary OA. The stromal vascular cell fraction (SVF) was isolated and characterised by fluorescence activated cell sorting. Cytokine and adipokine release in fat- and adipocyte-conditioned media was measured by luminex. IFP secreted higher levels of inflammatory mediators such as interleukin 6 (IL-6), adipsin, adiponectin and visfatin than ScAT. This could be due to differences in the phenotype of adipocytes and/or in the composition and phenotype of the SVF cells. IFP adipocyte-conditioned media showed a trend towards more IL-6 and adipsin than ScAT. Moreover, the SVF fraction of IFP contained more cells/g tissue, a lower percentage of T cells and a higher percentage of mast cells than ScAT. In addition, T cells had a predominantly pro-inflammatory phenotype while macrophages had a mixed pro- and anti-inflammatory phenotype in the IFP. There are profound differences in secreted inflammatory factors and immune cell composition between the IFP and ScAT. These data indicate that IFP-derived soluble mediators could contribute to pathophysiological processes in the OA knee joint.

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Author and article information

Contributors

Anne-Mari Mustonen:

ORCID: http://orcid.org/0000-0003-2266-2518

+358-294 45 1111 , Anne-Mari.Mustonen@uef.fi

Reijo Käkelä: reijo.kakela@helsinki.fi

Petri Lehenkari: petri.lehenkari@oulu.fi

Johanna Huhtakangas: johanna.huhtakangas@fimnet.fi

Sanna Turunen: sanna.turunen@oulu.fi

Antti Joukainen: Antti.Joukainen@kuh.fi

Tommi Kääriäinen: tommi.kaariainen@pohjolasairaala.fi

Tommi Paakkonen: tommi.paakkonen@uef.fi

Heikki Kröger: Heikki.Kroger@kuh.fi

Petteri Nieminen: petteri.nieminen@uef.fi

Journal

Journal ID (nlm-ta): Arthritis Res Ther

Journal ID (iso-abbrev): Arthritis Res. Ther

Title: Arthritis Research & Therapy

Publisher: BioMed Central (London )

ISSN (Print): 1478-6354

ISSN (Electronic): 1478-6362

Publication date (Electronic): 22 May 2019

Publication date PMC-release: 22 May 2019

Publication date (Print): 2019

Volume: 21

Electronic Location Identifier: 124

Affiliations

[1 ]ISNI 0000 0001 0726 2490, GRID grid.9668.1, Institute of Biomedicine, School of Medicine, Faculty of Health Sciences, , University of Eastern Finland, ; P.O. Box 1627, FI-70211 Kuopio, Finland

[2 ]ISNI 0000 0001 0726 2490, GRID grid.9668.1, Department of Environmental and Biological Sciences, Faculty of Science and Forestry, , University of Eastern Finland, ; P.O. Box 111, FI-80101 Joensuu, Finland

[3 ]ISNI 0000 0004 0410 2071, GRID grid.7737.4, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, , University of Helsinki, ; P.O. Box 65, FI-00014 Helsinki, Finland

[4 ]ISNI 0000 0004 0410 2071, GRID grid.7737.4, Helsinki University Lipidomics Unit (HiLIPID), Helsinki Institute for Life Science (HiLIFE), , University of Helsinki, ; P.O. Box 65, FI-00014 Helsinki, Finland

[5 ]ISNI 0000 0001 0941 4873, GRID grid.10858.34, Cancer and Translational Medicine Research Unit, Faculty of Medicine, , University of Oulu, ; P.O. Box 5000, FI-90014 Oulu, Finland

[6 ]ISNI 0000 0004 4685 4917, GRID grid.412326.0, Department of Surgery and Medical Research Center, , Oulu University Hospital (OYS), ; P.O. Box 21, FI-90029 Oulu, Finland

[7 ]ISNI 0000 0004 4685 4917, GRID grid.412326.0, Rheumatology Unit and Medical Research Center, , Oulu University Hospital (OYS), ; P.O. Box 21, FI-90029 Oulu, Finland

[8 ]ISNI 0000 0004 0628 207X, GRID grid.410705.7, Department of Orthopaedics, Traumatology and Hand Surgery, , Kuopio University Hospital (KYS), ; P.O. Box 100, FI-70029 Kuopio, Finland

Author information

Anne-Mari Mustonen http://orcid.org/0000-0003-2266-2518

Article

Publisher ID: 1914

DOI: 10.1186/s13075-019-1914-y

PMC ID: 6532171

PubMed ID: 31118103

SO-VID: d56567ac-f944-4972-a549-48519d9aa4e6

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 30 November 2018

Date accepted : 9 May 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004012, Jane ja Aatos Erkon Säätiö;

Award ID: n/a

Award Recipient : Anne-Mari Mustonen

Custom metadata

ScienceOpen disciplines: Orthopedics

Keywords: fatty acid,infrapatellar fat pad,n-3 polyunsaturated fatty acids,n-6 polyunsaturated fatty acids,osteoarthritis,rheumatoid arthritis,synovial fluid

Data availability:

ScienceOpen disciplines: Orthopedics

Keywords: fatty acid, infrapatellar fat pad, n-3 polyunsaturated fatty acids, n-6 polyunsaturated fatty acids, osteoarthritis, rheumatoid arthritis, synovial fluid

Distinct fatty acid signatures in infrapatellar fat pad and synovial fluid of patients with osteoarthritis versus rheumatoid arthritis

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Orthopedics

Most cited references 47

Synovial inflammation, immune cells and their cytokines in osteoarthritis: a review.

Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids.

The infrapatellar fat pad of patients with osteoarthritis has an inflammatory phenotype.

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