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Plasma phosphatidylcholine and sphingomyelin concentrations are associated with depression and anxiety symptoms in a Dutch family-based lipidomics study

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Demirkan, Ayşe, Isaacs, Aaron, Ugocsai, Peter, Liebisch, Gerhard, Struchalin, Maksim, Rudan, Igor, Wilson, James F., Pramstaller, Peter P., Gyllensten, Ulf, Campbell, Harry, Schmitz, Gerd, Oostra, Ben A., van Duijn, Cornelia M.·2013·Journal of Psychiatric Research

DOI 10.1016/j.jpsychires.2012.11.001

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Abstract

The central nervous system has the second highest concentration of lipids after adipose tissue. Alterations in neural membrane phospho- and sphingolipid composition can influence crucial intra- and intercellular signalling and alter the membrane's properties. Recently, the polyunsaturated fatty acids (PUFA) hypothesis for depression suggests that phospho- and sphingolipid metabolism includes potential pathways for the disease. In 742 people from a Dutch family-based study, we assessed the relationships between 148 different plasma phospho- and sphingolipid species and depression/anxiety symptoms as measured by the Hospital Anxiety and Depression Scales (HADS-A and HADS-D) and the Centre for Epidemiological Studies Depression Scale (CES-D). We observed significant differences in plasma sphingomyelins (SPM), particularly the SPM 23:1/SPM 16:0 ratio, which was inversely correlated with depressive symptom scores. We observed a similar trend for plasma phosphatidylcholines (PC), particularly the molar proportion of PC O 36:4 and its ratio to ceramide CER 20:0. Absolute levels of PC O 36:4 were also associated with depression symptoms in an independent replication. To our knowledge this is the first study on depressive symptoms that focuses on specific phospho- and sphingolipid molecules in plasma rather than total PUFA concentrations. The findings of this lipidomic study suggests that plasma sphingomyelins and ether phospholipids should be further studied for their potential as biomarkers and for a better understanding of the underlying mechanisms of this systemic disease.

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The Forebrain-Specific Overexpression of Acid Sphingomyelinase Induces Depressive-Like Symptoms in Mice
Zoicas, I., Schumacher, F., Kleuser, B., Reichel, M., Gulbins, E., Fejtová, A., Kornhuber, J., & Rhein, C. (2020) · Cells · doi:10.3390/cells9051244 · Cited by 25
“In contrast, plasma sphingomyelin SM26:1 [12], SM21:0 and SM21:1 [13] levels were decreased in MDD patients, and the SM23:1/SM16:0 ratio was negatively correlated with the severity of depressive symptoms in a Dutch family [14].”
Result
A diet-induced gut microbiota component and related plasma metabolites are associated with depressive-like behaviour in rats
Abildgaard, A. M., Kern, T., Pedersen, O. B., Hansen, T. F., Lund, S. A., & Wegener, G. (2020) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2020.09.001 · Cited by 24
Alterations in the Plasma Lipidome of Adult Women With Bipolar Disorder: A Mass Spectrometry-Based Lipidomics Research
Guo, L., Zhang, T., Li, R., Cui, Z.-Q., Du, J., Yang, J.-B., Xue, F., Chen, Y., Tan, Q.-R., & Peng, Z. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.802710 · Cited by 26
“Previous studies also found that plasma SM was negatively correlated with depressive symptoms (42), and lower concentrations of AcCa and PE were also observed in the plasma of BD patients than that of HCs (43–45).”
Result
mRNA Expression of SMPD1 Encoding Acid Sphingomyelinase Decreases upon Antidepressant Treatment
Rhein, C., Zoicas, I., Marx, L. M., Zeitler, S., Hepp, T., von Zimmermann, C., Mühle, C., Richter‐Schmidinger, T., Lenz, B., Erim, Y., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115700 · Cited by 22
“Conversely, plasma sphingomyelin SM26:1 [31], SM21:0, and SM21:1 [32] levels are decreased in MDD patients, and the SM23:1/SM16:0 ratio is negatively correlated with the severity of depression symptoms [33].”
Background
Alterations of Plasma Lipids in Adult Women With Major Depressive Disorder and Bipolar Depression
Zhang, T., Guo, L., Li, R., Wang, F., Yang, W., Yang, J.-B., Cui, Z.-Q., Zhou, C., Chen, Y., Yu, H., et al. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.927817 · Cited by 23
Circadian Time Structure of Circulating Plasma Lipid Components in Healthy Indians of Different Age Groups
Singh, R., Sharma, S., Singh, R. K., & Cornélissen, G. (2015) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-015-0519-8 · Cited by 23
Role of dietary and nutritional interventions in ceramide-associated diseases
Wang, S., Jin, Z., Wu, B., Morris, A. J., & Deng, P. (2024) · Journal of Lipid Research · doi:10.1016/j.jlr.2024.100726 · Cited by 22
Amitriptyline at an Environmentally Relevant Concentration Alters the Profile of Metabolites Beyond Monoamines in Gilt-Head Bream
Ziarrusta, H., Ribbenstedt, A., Mijangos, L., Picart‐Armada, S., Perera-Lluna, A., Prieto, A., Izagirre, U., Benskin, J. P., Olivares, M., Zuloaga, O., et al. (2019) · Environmental Toxicology and Chemistry · doi:10.1002/etc.4381 · Cited by 21
“An inverse correlation between phosphatidylcholines and sphingolipids and neurological disorders (anxiety and depression) has also been found in the literature (Demirkan et al. 2013).”
Background
A multi-omics study of circulating phospholipid markers of blood pressure
Liu, J., de Vries, P. S., Fabiola Del Greco, M., Johansson, Å., Schraut, K. E., Hayward, C., van Dijk, K. W., Franco, O. H., Hicks, A. A., Vitart, V., et al. (2022) · Scientific Reports · doi:10.1038/s41598-021-04446-7 · Cited by 21
Investigation of the Hepatoprotective Effect of Prunus mume Sieb. et Zucc Extract in a Mouse Model of Alcoholic Liver Injury Through High-Resolution Metabolomics
Khan, A., Pan, J. H., Cho, S., Lee, S., Kim, Y. J., & Park, Y. H. (2017) · Journal of Medicinal Food · doi:10.1089/jmf.2016.3874 · Cited by 20
“Previous studies performed on the importance of PC have demonstrated several important roles of PC, such as PC makes acetylcholine in human brain,(39) and has been shown to be interrelated with several brain-centered conditions such as dementia,(40) Alzheimer’s disease,(41) anxiety, and depressive disorders.(42) Heavy…”
Biomarker screening for antenatal depression in women who underwent caesarean section: a matched observational study with plasma Lipidomics
Wu, Z., Zhao, P., Long, Z., Li, J., Yang, G., Zhang, Q., Duan, G., & Li, H. (2019) · BMC Psychiatry · doi:10.1186/s12888-019-2241-1 · Cited by 20
Untargeted Plasma Metabolomic Profiling in Patients with Major Depressive Disorder Using Ultra-High Performance Liquid Chromatography Coupled with Mass Spectrometry
Homorogan, C., Nitusca, D., Enatescu, V., Schubart, P., Moraru, C., Socaciu, C., & Marian, C. (2021) · Metabolites · doi:10.3390/metabo11070466 · Cited by 19
“It is known that AA alone can modulate membrane polarization and fluidity, thus being directly involved in neural cell function and MDD symptomatology [22,33].”
Background
A Diet Supplemented with Polyphenols, Prebiotics and Omega-3 Fatty Acids Modulates the Intestinal Microbiota and Improves the Profile of Metabolites Linked with Anxiety in Dogs
Ephraim, E., Brockman, J. A., & Jewell, D. E. (2022) · Biology · doi:10.3390/biology11070976 · Cited by 22
“A Dutch family-based lipidomics study of 742 people found inverse correlations between the ratio of sphingomyelin 23:1/sphingomyelin 16:0 and depression/anxiety symptoms, indicating a role for sphingomyelins in these disorders [53].”
Background
Platelet activating factors are associated with depressive symptoms in coronary artery disease patients: a hypothesis-generating study
Lanctôt, K. L., Mazereeuw, G., Herrmann, N., Xu, H., Blanchard, A. P., Figeys, D., OH, P. I., & Bennett, S. A. L. (2015) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s87111 · Cited by 19
“17 These findings are also in line with previously reported associations between PC-derived lipid mediators and depressive symptoms 29 or depressive symptom-like behavior.”
Alterations in Plasma Lipidomic Profiles in Adult Patients with Schizophrenia and Major Depressive Disorder
Wang, F., Guo, L., Zhang, T., Cui, Z., Wang, J., Zhang, C., Xue, F., Zhou, C., Li, B., Tan, Q., et al. (2022) · Medicina · doi:10.3390/medicina58111509 · Cited by 18
“Supporting these findings, previous studies found that levels of PE were decreased in the serum and postmortem prefrontal white matter in SCZ patients [31,32], and serum PE was also negatively correlated with depressive symptoms [33].”
Result
Serum ceramide concentrations are associated with depression in patients after ischemic stroke-A two-center case-controlled study
Hong, L., Wang, H., Leijie, X., Dandan, Z., Liu, P., Hu, Z., Ma, R., Yijun, S., Guanghui, Z., & Guojun, Z. (2021) · Clinica Chimica Acta · doi:10.1016/j.cca.2021.03.014 · Cited by 19
Mass spectrometry analysis of blood plasma lipidome as method of disease diagnostics, evuation of effectiveness and optimization of drug therapy
Lokhov, P. G., Maslov, D. L., Balashova, E. E., Trifonova, O. P., Medvedeva, N. V., Torkhovskaya, T. I., Ipatova, O. M., Archakov, A. I., Прокопьевич, М. П., Kukharchuk, V. V., et al. (2015) · Biomeditsinskaya Khimiya · doi:10.18097/pbmc20156101007 · Cited by 17
Saikosaponin antidepressant mechanism: Improving the sphingolipid metabolism in the cortex via Apolipoprotein E and triggering neurovascular coupling
Song, Y., Lai, M., Liao, Z., Zhang, Z., Zhu, G., Yang, M., Ai, Z., Zheng, Q., & Su, D. (2024) · Phytomedicine · doi:10.1016/j.phymed.2024.155829 · Cited by 17
Urinary Lipidomics: evidence for multiple sources and sexual dimorphism in healthy individuals
Graessler, J., Mehnert, C. S., Schulte, K., Bergmann, S., Strauss, S., Bornstein, T. D., Licinio, J., Wong, M., Birkenfeld, A. L., & Bornstein, S. R. (2017) · The Pharmacogenomics Journal · doi:10.1038/tpj.2017.24 · Cited by 16
Screening for depression in the general population through lipid biomarkers
Tkachev, A., Stekolshchikova, E., Golubova, A., Serkina, A., Morozova, A. Y., Zorkina, Y., Riabinina, D., Golubeva, E., Ochneva, A., Savenkova, V., et al. (2024) · EBioMedicine · doi:10.1016/j.ebiom.2024.105455 · Cited by 15
Application of fatty acid and lipid measurements in neuropsychiatry
Grela, A., Rachel, W., Cole, M., Zyss, T., Zięba, A., & Piekoszewski, W. (2015) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2015-0394 · Cited by 14
“A lipidomic study on a Dutch population was performed [89] and two lipids were found to be highly correlated with depressive symptoms (assessed by the Hospital Anxiety and Depression Scales): 1) PC O 36:4 (1-O-hexadecyl-2-arachidonoyl-sn-glycero-3-phosphocholine; an ether phospholipid that contains a bound AA (C20:4,…”
Method
Tryptophan-5-HT pathway disorder was uncovered in the olfactory bulb of a depression mice model by metabolomic analysis
Chen, G., Zhou, S., Chen, Q., Liu, M., Dong, M.-X., Hou, J., & Zhou, B. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.965697 · Cited by 14
“Clinical research indicated that plasma PC concentrations of depression patients were associated with the severity of depression (Demirkan et al., 2013).”
Background
Association Between Abnormal Plasma Lipid Metabolism and Psychological Characteristics in Adolescents With Major Depressive Disorder
Wang, Y., Chen, H., Wang, J., Chen, S., Liu, J., Chen, X., Li, S., Tang, H., Zhou, J., Ye, Y., et al. (2025) · Depression and Anxiety · doi:10.1155/da/5564796 · Cited by 15
“Absolute levels of PC O 36:4 were also negatively correlated with depressive symptoms in an independent validation with 753 individuals [42].”
Modulatory effect of n-3 polyunsaturated fatty acids on depressive-like behaviors in rats with chronic sleep deprivation: potential involvement of melatonin receptor pathway and brain lipidome
Chang, C., Wu, H.-C., Hsieh, Y.-R., Lai, W.-D., Tung, T.-H., Huang, J.-J., Kao, W., & Huang, S. (2023) · Food & Function · doi:10.1039/d3fo01452e · Cited by 13
Alterations in Metabolome and Microbiome Associated with an Early Stress Stage in Male Wistar Rats: A Multi-Omics Approach
Hernández-Baixauli, J., Puigbò, P., Abasolo-Zabalo, N., Palacios, H. H., Foguet‐Romero, E., Suñol, D., Galofré, M., Caimari, A., Baselga‐Escudero, L., Bas-Prior, J. M. D., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312931 · Cited by 12
Shorter Chain Triglycerides Are Negatively Associated with Symptom Improvement in Schizophrenia
Tkachev, A., Stekolshchikova, E., Anikanov, N., Zozulya, S., Barkhatova, A., Klyushnik, T., & Petrova, D. (2021) · Biomolecules · doi:10.3390/biom11050720 · Cited by 11
Lipidomic analyses reveal the dysregulation of oxidized fatty acids (OxFAs) and acyl-carnitines (CARs) in major depressive disorder: a case-control study
He, L., Duan, N., Wang, C., Shan, R., Li, J., Wang, L., Liu, Q., Tao, J., Liu, L., Ma, X., et al. (2025) · BMC Psychiatry · doi:10.1186/s12888-025-07191-7 · Cited by 11
“Thus, phospho-and sphingolipid molecules can be considered as potential biomarkers of MDD, possibly related to the linoleic/arachidonic acid inflammation pathway [12, 13].”
SGMS2 in primary osteoporosis with facial nerve palsy
Pihlström, S., Richardt, S., Määttä, K. M., Pekkinen, M., Olkkonen, V. M., Mäkitie, O., & Mäkitie, R. E. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1224318 · Cited by 11
Labelfree mapping and profiling of altered lipid homeostasis in the rat hippocampus after traumatic stress: Role of oxidative homeostasis
Kelley, D. P., Chaichi, A., Duplooy, A., Singh, D. P., Gartia, M. R., & Francis, J. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100476 · Cited by 11
“ROS and OXS is have a substantial impact on cellular viability of all neural cell types, but oligodendrocytes, cells that form myelin-sheaths and contribute up to 80% of the brain ’ s total cholesterol are particularly sensitive (Chao et al., 2015; Dietschy, 2009; Schiavone et al., 2013).”
Background
Metabolomic profiles in night shift workers: A cross-sectional study on hospital female nurses
Borroni, E., Frigerio, G., Polledri, E., Mercadante, R., Maggioni, C., Fedrizzi, L., Pesatori, A. C., Fustinoni, S., & Carugno, M. (2023) · Frontiers in Public Health · doi:10.3389/fpubh.2023.1082074 · Cited by 11
“Lower levels of sphingolipids were found in patients with a diagnosis of major depressive disorder: Demirkan and colleagues identified significant negative associations between the sphingomyelin (SM) ratio 23:1 to SM 16:0 and a psychometric depression measure (Center for Epidemiological Studies-Depression Scale: CES-D…”
Background
Integration of non-targeted metabolomics with network pharmacology deciphers the anxiolytic mechanisms of Platycladi Semen extracts in CUMS mice
Xie, J., Li, Y., Liang, Y., Kui, H., Wang, C., & Huang, J. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.116571 · Cited by 11
Omega-3/omega-6 fatty acid ratios in different phospholipid classes and depressive symptoms in coronary artery disease patients
Mazereeuw, G., Herrmann, N., David, W. L., Hillyer, L. M., OH, P. I., & Lanctôt, K. L. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.12.009 · Cited by 11
“A recent study implicated sphingomyelin species, such as SM 23:1 and SM 16:0, as correlates of depressive symptoms (Demirkan et al., 2013); however, that study was unable to characterize the fatty acid chains involved, which is a limitation that may have been overcome by the present study.”
A high coverage pseudotargeted lipidomics method based on three-phase liquid extraction and segment data-dependent acquisition using UHPLC-MS/MS with application to a study of depression rats
Danyang, L., Yang, J., Jin, W., Zhong, Q., & Zhou, T. (2021) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-021-03349-w · Cited by 12
Lipids from ocular meibum and tears may serve as biomarkers for depression and post‐traumatic stress disorder
Gary, A. A., Prislovsky, A., Tovar, A., Locatelli, E. V. T., Felix, E. R., Stephenson, D., Chalfant, C. E., Lai, J. M., Kim, C. K., Mandal, N. A., et al. (2023) · Clinical and Experimental Ophthalmology · doi:10.1111/ceo.14343 · Cited by 10
Altered lipidomics biosignatures in schizophrenia: A systematic review
Messinis, A., Panteli, E., Paraskevopoulou, A., Zymarikopoulou, A.-K., & Filiou, M. D. (2024) · Schizophrenia Research · doi:10.1016/j.schres.2024.06.043 · Cited by 11
Effects of Sex, Age, and Fasting Conditions on Plasma Lipidomic Profiles of Fasted Sprague-Dawley Rats
Saito, K., Ishikawa, M., Murayama, M., Urata, M., Senoo, Y., Toyoshima, K., Kumagai, Y., Maekawa, K., & Saito, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112266 · Cited by 10
The Impact of Electroacupuncture Early Intervention on the Brain Lipidome in a Mouse Model of Post-traumatic Stress Disorder
Zhou, C., Xue, F., Shi, Q., Xue, S., Zhang, T., Ma, X., Yu, L., Liu, C., Wang, H., & Peng, Z. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.812479 · Cited by 9
Neurolipidomic insights into anxiety disorders: Uncovering lipid dynamics for potential therapeutic advances
Maehashi, S., Arora, K., Fisher, A. L., Schweitzer, D. R., & Akefe, I. O. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105741 · Cited by 11
“Rodent model studies have demonstrated that prolonged exposure to stress may lead to an altered composition and function of these neuro-lipids within the central nervous system (Demirkan et al., 2013; Hursi-to ˘ glu and Kurutas, 2023; Bulut et al., 2013).”
Influential
One-carbon and energy metabolism in major depression compared to chronic depression in adolescent outpatients: A metabolomic pilot study
Kurkinen, K., Kärkkäinen, O. K., Lehto, S. M., Luoma, I., Kraav, S., Nieminen, A. I., Kivimäki, P., Therman, S., & Tolmunen, T. (2021) · Journal of Affective Disorders Reports · doi:10.1016/j.jadr.2021.100261 · Cited by 10
Lipidomics
Donato, P., Cacciola, F., Beccaria, M., Dugo, P., & Mondello, L. (2015) · Comprehensive analytical chemistry · doi:10.1016/b978-0-444-63340-8.00008-x · Cited by 10
Serum metabolomics in women with major depressive disorder: Associations with mitochondrial function, inflammation, and oxidative stress
Bisle, E., Haange, S., Rojas, R., Behnke, A., Karabatsiakis, A., Gumpp, A. M., Mack, M., Mavioğlu, R. N., Lutz‐Bonengel, S., Rolle-Kampczyk, U. E., et al. (2025) · Psychiatry Research · doi:10.1016/j.psychres.2025.116569 · Cited by 10
“However, other studies report reduced vinyl ether glycerophospholipids in the blood of patients and rat brains under chronic stress (Demirkan et al., 2013; X. Liu et al., 2016; Oliveira et al., 2016; Tkachev et al., 2023).”

Authors: Demirkan, A., Isaacs, A., Ugocsai, P., Liebisch, G., Struchalin, M., Rudan, I., Wilson, J. F., Pramstaller, P. P., Gyllensten, U., Campbell, H., Schmitz, G., Oostra, B. A., & van Duijn, C. M.
Affiliations: Erasmus MC (NL)
University Hospital Regensburg (DE)
University of Split (HR)
University of Edinburgh (GB)
Eurac Research (IT)
Uppsala University (SE)
Corresponding author: Isaacs, Aaron
ORCID: Demirkan, Ayşe
Isaacs, Aaron
Liebisch, Gerhard
Struchalin, Maksim
Rudan, Igor
Wilson, James F.
Pramstaller, Peter P.
Schmitz, Gerd
Venue: Journal of Psychiatric Research
Publisher: Elsevier BV
Published: 2013-03
Volume: 47
Issue: 3
Pages: 357-362
ISSN: 0022-3956 (ISSN-L)
DOI: 10.1016/j.jpsychires.2012.11.001
OpenAlex: W2164766370
Cited by: 163
References: 51
Citations by year: 2026: 11 · 2025: 15 · 2024: 22 · 2023: 14 · 2022: 15 · 2021: 14 · 2020: 11 · 2019: 10 · 2018: 9 · 2017: 9 · 2016: 12 · 2015: 11 · 2014: 7 · 2013: 3
FWCI: 6.25
Type: journal article
Language: en
Open access: green
zenodo.org
Licence: other-oa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of Psychiatric Research (publishedVersion)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Open Research (University of Surrey) (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
Research Publications (Maastricht University) (submittedVersion)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek
H2020 European Research Council
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: depression, anxiety, phospholipids, sphingolipids, ether phospholipids, polyunsaturated fatty acids, lipid biomarkers, family studies, ceramide
MeSH terms: Adult, Aged, Anxiety, Depression, Family Health, Female, Humans, Male, Middle Aged, Netherlands, Phosphatidylcholines, Psychiatric Status Rating Scales, Sphingomyelins

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Plasma phosphatidylcholine and sphingomyelin concentrations are associated with depression and anxiety symptoms in a Dutch family-based lipidomics study

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