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Plasma lipidomic profile of depressive symptoms: a longitudinal study in a large sample of community-dwelling American Indians in the strong heart study

Molecular Psychiatry volume 28, pages 2480–2489 (2023)Cite this article

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Abstract

Dyslipidemia has been associated with depression, but individual lipid species associated with depression remain largely unknown. The temporal relationship between lipid metabolism and the development of depression also remains to be determined. We studied 3721 fasting plasma samples from 1978 American Indians attending two exams (2001–2003, 2006–2009, mean ~5.5 years apart) in the Strong Heart Family Study. Plasma lipids were repeatedly measured by untargeted liquid chromatography-mass spectrometry (LC-MS). Depressive symptoms were assessed using the 20-item Center for Epidemiologic Studies for Depression (CES-D). Participants at risk for depression were defined as total CES-D score ≥16. Generalized estimating equation (GEE) was used to examine the associations of lipid species with incident or prevalent depression, adjusting for covariates. The associations between changes in lipids and changes in depressive symptoms were additionally adjusted for baseline lipids. We found that lower levels of sphingomyelins and glycerophospholipids and higher level of lysophospholipids were significantly associated with incident and/or prevalent depression. Changes in sphingomyelins, glycerophospholipids, acylcarnitines, fatty acids and triacylglycerols were associated with changes in depressive symptoms and other psychosomatic traits. We also identified differential lipid networks associated with risk of depression. The observed alterations in lipid metabolism may affect depression through increasing the activities of acid sphingomyelinase and phospholipase A2, disturbing neurotransmitters and membrane signaling, enhancing inflammation, oxidative stress, and lipid peroxidation, and/or affecting energy storage in lipid droplets or membrane formation. These findings illuminate the mechanisms through which dyslipidemia may contribute to depression and provide initial evidence for targeting lipid metabolism in developing preventive and therapeutic interventions for depression.

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Fig. 1: Baseline plasma lipids associated with incident depression (mean follow-up: 5.5 years).
Fig. 2: Incremental value of the identified plasma lipids in risk prediction for depression.
Fig. 3: Plasma lipids associated with prevalent depression at baseline or follow-up.
Fig. 4: Manhattan plots displaying the longitudinal associations of change in plasma lipids with change in psychosomatic measures between baseline and follow-up.
Fig. 5: Directions of associations between plasma lipid species and depression in the SHFS.

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Data availability

The phenotype data used in this study can be requested through the Strong Heart Study (https://strongheartstudy.org/). The lipidomic data can be obtained from the corresponding author upon a reasonable request.

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Acknowledgements

We thank the Strong Heart Study (SHS) participants, the Indian Health Service (IHS) facilities, and the participating tribes for their extraordinary cooperation and involvement, which has contributed to the success of the SHS. The content expressed in this article is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the IHS.

Funding

This study was supported by the National Institute of Health (NIH) grant R01DK107532. The Strong Heart Study (SHS) has been funded in whole or in part with federal funds from the National Heart, Lung, and Blood Institute, National Institute of Health, Department of Health and Human Services, under contract numbers 75N92019D00027, 75N92019D00028, 75N92019D00029, and 75N92019D00030. The study was previously supported by research grants: R01HL109315, R01HL109301, R01HL109284, R01HL109282, and R01HL109319 and by cooperative agreements: U01HL41642, U01HL41652, U01HL41654, U01HL65520, and U01HL65521.

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Authors and Affiliations

  1. Department of Epidemiology, College of Public Health & Health Professions and College of Medicine, University of Florida, Gainesville, FL, USA

    Guanhong Miao, Joseph B. Struzeski, Mingjing Chen & Jinying Zhao

  2. Center for Genetic Epidemiology and Bioinformatics, University of Florida, Gainesville, FL, USA

    Guanhong Miao, Joseph B. Struzeski, Mingjing Chen & Jinying Zhao

  3. Department of Pediatrics, University of Washington, Seattle, WA, USA

    Jason Deen

  4. Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA

    Ying Zhang & Elisa T. Lee

  5. Texas Biomedical Research Institute, San Antonio, TX, USA

    Shelley A. Cole

  6. Department of Epidemiology, University of Washington, Seattle, WA, USA

    Amanda M. Fretts

  7. MedStar Health Research Institute, Hyattsville, MD, USA

    Barbara V. Howard

  8. West Coast Metabolomics Center, University of California-Davis, California, CA, USA

    Oliver Fiehn

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JZ and OF conceptualized and designed the study, obtained the funding and generated the data. GM conducted the statistical analyses. JZ and GM drafted the manuscript. All coauthors provided critical review of the manuscript and contributed to data interpretation.

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Correspondence to Jinying Zhao.

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Miao, G., Deen, J., Struzeski, J.B. et al. Plasma lipidomic profile of depressive symptoms: a longitudinal study in a large sample of community-dwelling American Indians in the strong heart study. Mol Psychiatry 28, 2480–2489 (2023). https://doi.org/10.1038/s41380-023-01948-w

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