Plasma Lipid Profiling Shows Similar Associations with Prediabetes and Type 2 Diabetes

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Abstract

The relationship between lipid metabolism with prediabetes (impaired fasting glucose and impaired glucose tolerance) and type 2 diabetes mellitus is poorly defined. We hypothesized that a lipidomic analysis of plasma lipids might improve the understanding of this relationship. We performed lipidomic analysis measuring 259 individual lipid species, including sphingolipids, phospholipids, glycerolipids and cholesterol esters, on fasting plasma from 117 type 2 diabetes, 64 prediabetes and 170 normal glucose tolerant participants in the Australian Diabetes, Obesity and Lifestyle Study (AusDiab) then validated our findings on 1076 individuals from the San Antonio Family Heart Study (SAFHS). Logistic regression analysis of identified associations with type 2 diabetes (135 lipids) and prediabetes (134 lipids), after adjusting for multiple covariates. In addition to the expected associations with diacylglycerol, triacylglycerol and cholesterol esters, type 2 diabetes and prediabetes were positively associated with ceramide, and its precursor dihydroceramide, along with phosphatidylethanolamine, phosphatidylglycerol and phosphatidylinositol. Significant negative associations were observed with the ether-linked phospholipids alkylphosphatidylcholine and alkenylphosphatidylcholine. Most of the significant associations in the AusDiab cohort (90%) were subsequently validated in the SAFHS cohort. The aberration of the plasma lipidome associated with type 2 diabetes is clearly present in prediabetes, prior to the onset of type 2 diabetes. Lipid classes and species associated with type 2 diabetes provide support for a number of existing paradigms of dyslipidemia and suggest new avenues of investigation.

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Most cited references 29

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Plasmalogens the neglected regulatory and scavenging lipid species.

Stefan Wallner, Stefan Wallner (2011)

Plasmalogens are a class of phospholipids carrying a vinyl ether bond in sn-1 and an ester bond in sn-2 position of the glycerol backbone. Although they are widespread in all tissues and represent up to 18% of the total phospholipid mass in humans, their physiological function is still poorly understood. The aim of this review is to give an overview over the current knowledge in plasmalogen biology and pathology with an emphasis on neglected aspects of their involvement in neurological and metabolic diseases. Furthermore a better understanding of plasmalogen biology in health and disease could also lead to the development of better diagnostic and prognostic biomarkers for vascular and metabolic diseases such as obesity and diabetes mellitus, inflammation, neuro-degeneration and cancer. Copyright © 2011 Elsevier Ireland Ltd. All rights reserved.

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Trans-palmitoleic acid, metabolic risk factors, and new-onset diabetes in U.S. adults: a cohort study.

S. King, Xiaoling Song, D Siscovick … (2010)

Palmitoleic acid (cis-16:1n-7), which is produced by endogenous fat synthesis, has been linked to both beneficial and deleterious metabolic effects, potentially confounded by diverse determinants and tissue sources of endogenous production. Trans-palmitoleate (trans-16:1n-7) represents a distinctly exogenous source of 16:1n-7, unconfounded by endogenous synthesis or its determinants, that may be uniquely informative. To investigate whether circulating trans-palmitoleate is independently related to lower metabolic risk and incident type 2 diabetes. Prospective cohort study from 1992 to 2006. Four U.S. communities. 3736 adults in the Cardiovascular Health Study. Anthropometric characteristics and levels of plasma phospholipid fatty acids, blood lipids, inflammatory markers, and glucose-insulin measured at baseline in 1992 and dietary habits measured 3 years earlier. Multivariate-adjusted models were used to investigate how demographic, clinical, and lifestyle factors independently related to plasma phospholipid trans-palmitoleate; how trans-palmitoleate related to major metabolic risk factors; and how trans-palmitoleate related to new-onset diabetes (304 incident cases). Findings were validated for metabolic risk factors in an independent cohort of 327 women. In multivariate analyses, whole-fat dairy consumption was most strongly associated with higher trans-palmitoleate levels. Higher trans-palmitoleate levels were associated with slightly lower adiposity and, independently, with higher high-density lipoprotein cholesterol levels (1.9% across quintiles; P = 0.040), lower triglyceride levels (-19.0%; P < 0.001), a lower total cholesterol-HDL cholesterol ratio (-4.7%; P < 0.001), lower C-reactive protein levels (-13.8%; P = 0.05), and lower insulin resistance (-16.7%, P < 0.001). Trans-palmitoleate was also associated with a substantially lower incidence of diabetes, with multivariate hazard ratios of 0.41 (95% CI, 0.27 to 0.64) and 0.38 (CI, 0.24 to 0.62) in quintiles 4 and 5 versus quintile 1 (P for trend < 0.001). Findings were independent of estimated dairy consumption or other fatty acid dairy biomarkers. Protective associations with metabolic risk factors were confirmed in the validation cohort. Results could be affected by measurement error or residual confounding. Circulating trans-palmitoleate is associated with lower insulin resistance, presence of atherogenic dyslipidemia, and incident diabetes. Our findings may explain previously observed metabolic benefits of dairy consumption and support the need for detailed further experimental and clinical investigation. National Heart, Lung, and Blood Institute and National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health.

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Erythrocyte membrane phospholipid fatty acids, desaturase activity, and dietary fatty acids in relation to risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study.

Frank Döring, Hans-Georg Joost, Cornelia Weikert … (2010)

The long-term role of fatty acids (FAs) in the cause of diabetes remains largely unclear. We aimed to investigate erythrocyte membrane FAs, desaturase activity, and dietary FAs in relation to the incidence of type 2 diabetes. We applied a nested case-cohort design (n = 2724, including 673 incident diabetes cases) within the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study, which involves 27,548 middle-aged subjects. Thirty erythrocyte membrane FAs (percentage of total FAs) and FA intake (percentage of total fat) were measured at baseline, and physician-confirmed incident diabetes was assessed during a mean follow-up of 7.0 y. We evaluated Δ⁵ desaturase (D5D) and Δ⁶ desaturase (D6D) activity by using FA product-to-precursor ratios (traditional approach) and by investigating variants in FADS1 and FADS2 genes that encode these desaturases (Mendelian randomization approach). As a main finding, erythrocyte 16:1n-7 and 18:3n-6 and FA ratios, which reflect stearoyl coenzyme A desaturase (SCD) and D6D activity, were directly related to diabetes risk in multivariable-adjusted models [relative risks (95% CIs) comparing extreme quintiles: 16:1n-7, 2.11 (1.46, 3.05); 18:3n-6, 2.00 (1.38, 2.88); SCD, 2.61 (1.75, 3.89); and D6D, 2.46 (1.67, 3.63)], whereas the FA ratio that reflects D5D activity was inversely associated with risk [0.46 (0.31, 0.70)]. The Mendelian randomization approach corroborated the direct relation for D6D activity and tended to support the inverse relation for D5D activity. Proportions of dietary FAs showed only modest to low correlations with erythrocyte FAs and were not significantly associated with risk. The FA profile of erythrocyte membrane phospholipids and activity of desaturase enzymes are strongly linked to the incidence of type 2 diabetes.

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Author and article information

Contributors

Clarissa Menezes Maya-Monteiro: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 27 September 2013

Volume: 8

Issue: 9

Electronic Location Identifier: e74341

Affiliations

[1 ]Baker IDI Heart and Diabetes Institute, Melbourne, Victoria, Australia

[2 ]Department of Genetics, Texas Biomedical Research Institute, San Antonio, Texas, United States of America

[3 ]National ICT Australia (NICTA), University of Melbourne, Melbourne, Victoria, Australia

Fundação Oswaldo Cruz, Brazil

Author notes

* E-mail: peter.meikle@ 123456bakeridi.edu.au

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: PJM GW CKB JMW NG LA AGC MCM DJM JBMJ PZ JEC JB JS. Performed the experiments: PJM CKB JMW MAG GLM. Analyzed the data: PJM GW AK IH NG DJM JBMJ JS. Contributed reagents/materials/analysis tools: PJM GW AK IH NG DJM JBMJ JS. Wrote the paper: PJM.

Article

Publisher ID: PONE-D-13-15260

DOI: 10.1371/journal.pone.0074341

PMC ID: 3785490

PubMed ID: 24086336

SO-VID: 6517d2c9-dff8-4dc4-bb96-c8a6f34d4730

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This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 11 April 2013

Date accepted : 1 August 2013

Page count

Pages: 11

Funding

This work was supported by funding from the Dairy Health and Nutrition Consortium, Australia, The National Health and Medical Research Council of Australia, the OIS Program of the Victorian Government, Australia and by Award Number 1R01DK088972-01 from the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, USA. The content is solely the responsibility of the authors and does not necessarily represent the official views of the aforementioned funding bodies. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The AusDiab study co-coordinated by the Baker IDI Heart and Diabetes Institute, gratefully acknowledges the generous support given by: The National Health and Medical Research Council (NHMRC grant 233200), Australian Government Department of Health and Ageing, the Dairy Health and Nutrition Consortium, Abbott Australasia Pty Ltd, Alphapharm Pty Ltd, AstraZeneca, Bristol-Myers Squibb, City Health Centre-Diabetes Service-Canberra, Department of Health and Community Services – Northern Territory, Department of Health and Human Services – Tasmania, Department of Health – New South Wales, Department of Health – Western Australia, Department of Health – South Australia, Department of Human Services – Victoria, Diabetes Australia, Diabetes Australia Northern Territory, Eli Lilly Australia, Estate of the Late Edward Wilson, GlaxoSmithKline, Jack Brockhoff Foundation, Janssen-Cilag,, Kidney Health Australia, Marian & FH Flack Trust, Menzies Research Institute, Merck Sharp & Dohme, Novartis Pharmaceuticals, Novo Nordisk Pharmaceuticals, Pfizer Pty Ltd, Pratt Foundation, Queensland Health, Roche Diagnostics Australia, Royal Prince Alfred Hospital, Sydney, Sanofi Aventis and sanofi-synthelabo. Also, for their invaluable contribution to the set-up and field activities of AusDiab, we are enormously grateful to A Allman, B Atkins, S Bennett, S Chadban, M de Courten, M Dalton, D Dunstan, T Dwyer, D Jolley, D McCarty, A Meehan, S Murray, P Phillips, C Reid, A Stewart, R Tapp, H Taylor, and F Wilson (Baker IDI Heart and Diabetes Institute). Data collection for the SAFHS was supported by grant P01 HL045522 from the National Institutes of Health (to JB). Additional work was supported by National Institutes of Health awards R01 DK082610 and R01 DK079169 (to JC), and R01 HL091035 (to JB). Parts of this investigation were conducted in facilities constructed with support from Research Facilities Improvement Program grants C06 RR013556 and C06 RR017515 from the National Center for Research Resources of the National Institutes of Health.

Plasma Lipid Profiling Shows Similar Associations with Prediabetes and Type 2 Diabetes

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Most cited references 29

Plasmalogens the neglected regulatory and scavenging lipid species.

Trans-palmitoleic acid, metabolic risk factors, and new-onset diabetes in U.S. adults: a cohort study.

Erythrocyte membrane phospholipid fatty acids, desaturase activity, and dietary fatty acids in relation to risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study.

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