Associations of depression status with plasma levels of candidate lipid and amino acid metabolites: a meta-analysis of individual data from three independent samples of US postmenopausal women.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
04
09
2019
accepted:
14
08
2020
revised:
04
08
2020
pubmed:
30
8
2020
medline:
27
1
2022
entrez:
30
8
2020
Statut:
ppublish
Résumé
Recent animal and small clinical studies have suggested depression is related to altered lipid and amino acid profiles. However, this has not been examined in a population-based sample, particularly in women. We identified multiple metabolites associated with depression as potential candidates from prior studies. Cross-sectional data from three independent samples of postmenopausal women were analyzed, including women from the Women's Health Initiative-Observational Study (WHI-OS, n = 926), the WHI-Hormone Trials (WHI-HT; n = 1,325), and the Nurses' Health Study II Mind-Body Study (NHSII-MBS; n = 218). Positive depression status was defined as having any of the following: elevated depressive symptoms, antidepressant use, or depression history. Plasma metabolites were measured using liquid chromatography-tandem mass spectrometry (21 phosphatidylcholines (PCs), 7 lysophosphatidylethanolamines, 5 ceramides, 3 branched chain amino acids, and 9 neurotransmitters). Associations between depression status and metabolites were evaluated using multivariable linear regression; results were pooled by random-effects meta-analysis with multiple testing adjustment using the false discovery rate (FDR). Prevalence rates of positive depression status were 24.4% (WHI-OS), 25.7% (WHI-HT), and 44.7% (NHSII-MBS). After multivariable adjustment, positive depression status was associated with higher levels of glutamate and PC 36 : 1/38 : 3, and lower levels of tryptophan and GABA-to-glutamate and GABA-to-glutamine ratio (FDR-p < 0.05). Positive associations with LPE 18 : 0/18 : 1 and inverse associations with valine and serotonin were also observed, although these associations did not survive FDR adjustment. Associations of positive depression status with several candidate metabolites including PC 36 : 1/38 : 3 and amino acids involved in neurotransmission suggest potential depression-related metabolic alterations in postmenopausal women, with possible implications for later chronic disease.
Identifiants
pubmed: 32859999
doi: 10.1038/s41380-020-00870-9
pii: 10.1038/s41380-020-00870-9
pmc: PMC7914294
mid: NIHMS1620612
doi:
Substances chimiques
Amino Acids
0
Lipids
0
Types de publication
Journal Article
Meta-Analysis
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
3315-3327Subventions
Organisme : NIDDK NIH HHS
ID : P30 DK040561
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201600002C
Pays : United States
Organisme : NCI NIH HHS
ID : UM1 CA176726
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201600004C
Pays : United States
Organisme : NHLBI NIH HHS
ID : K01 HL143034
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201600001C
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA067262
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA163451
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201600018C
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201300008C
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA176726
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201600003C
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG051600
Pays : United States
Informations de copyright
© 2020. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Smoller JW, Allison M, Cochrane BB, Curb JD, Perlis RH, Robinson JG, et al. Antidepressant use and risk of incident cardiovascular morbidity and mortality among postmenopausal women in the Women’s Health Initiative study. Arch Intern Med. 2009;169:2128–39.
pubmed: 20008698
doi: 10.1001/archinternmed.2009.436
Wassertheil-Smoller S, Shumaker S, Ockene J, Talavera GA, Greenland P, Cochrane B, et al. Depression and cardiovascular sequelae in postmenopausal women. The Women’s Health Initiative (WHI). Arch Intern Med. 2004;164:289–98.
pubmed: 14769624
doi: 10.1001/archinte.164.3.289
Yu M, Zhang X, Lu F, Fang L. Depression and risk for diabetes: a meta-analysis. Can J Diabetes. 2015;39:266–72.
pubmed: 25773933
doi: 10.1016/j.jcjd.2014.11.006
Pan A, Keum N, Okereke OI, Sun Q, Kivimaki M, Rubin RR, et al. Bidirectional association between depression and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies. Diabetes Care. 2012;35:1171–80.
pubmed: 22517938
pmcid: 3329841
doi: 10.2337/dc11-2055
Pan A, Sun Q, Okereke OI, Rexrode KM, Hu FB. Depression and risk of stroke morbidity and mortality: a meta-analysis and systematic review. JAMA. 2011;306:1241–9.
pubmed: 21934057
pmcid: 3242806
doi: 10.1001/jama.2011.1282
Haapakoski R, Mathieu J, Ebmeier KP, Alenius H, Kivimaki M. Cumulative meta-analysis of interleukins 6 and 1beta, tumour necrosis factor alpha and C-reactive protein in patients with major depressive disorder. Brain Behav Immun. 2015;49:206–15.
pubmed: 26065825
pmcid: 4566946
doi: 10.1016/j.bbi.2015.06.001
Wesolowska K, Elovainio M, Hintsa T, Jokela M, Pulkki-Raback L, Lipsanen J, et al. Is the association between depressive symptoms and glucose bidirectional? A population-based study. Health Psychol. 2018;37:603–12.
pubmed: 29672099
doi: 10.1037/hea0000612
Whooley MA, de Jonge P, Vittinghoff E, Otte C, Moos R, Carney RM, et al. Depressive symptoms, health behaviors, and risk of cardiovascular events in patients with coronary heart disease. JAMA. 2008;300:2379–88.
pubmed: 19033588
pmcid: 2677371
doi: 10.1001/jama.2008.711
Whooley MA, Wong JM. Depression and cardiovascular disorders. Annu Rev Clin Psychol. 2013;9:327–54.
pubmed: 23537487
doi: 10.1146/annurev-clinpsy-050212-185526
Liu X, Zheng P, Zhao X, Zhang Y, Hu C, Li J, et al. Discovery and validation of plasma biomarkers for major depressive disorder classification based on liquid chromatography-mass spectrometry. J Proteome Res. 2015;14:2322–30.
pubmed: 25784130
doi: 10.1021/acs.jproteome.5b00144
Shi B, Tian J, Xiang H, Guo X, Zhang L, Du G, et al. A (1)H-NMR plasma metabonomic study of acute and chronic stress models of depression in rats. Behav Brain Res. 2013;241:86–91.
pubmed: 23219962
doi: 10.1016/j.bbr.2012.11.036
Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005;62:593–602.
pubmed: 15939837
doi: 10.1001/archpsyc.62.6.593
Demmer RT, Gelb S, Suglia SF, Keyes KM, Aiello AE, Colombo PC, et al. Sex differences in the association between depression, anxiety, and type 2 diabetes mellitus. Psychosom Med. 2015;77:467–77.
pubmed: 25867970
pmcid: 4431947
doi: 10.1097/PSY.0000000000000169
Möller-Leimkühler AM. Gender differences in cardiovascular disease and comorbid depression. Dialogues Clin Neurosci. 2007;9:71–83.
pubmed: 17506227
pmcid: 3181845
doi: 10.31887/DCNS.2007.9.1/ammoeller
Karel MJ. Aging and depression: vulnerability and stress across adulthood. Clin Psychol Rev. 1997;17:847–79.
pubmed: 9439871
doi: 10.1016/S0272-7358(97)00053-6
Gordon T, Kannel WB, Hjortland MC, McNamara PM. Menopause and coronary heart disease. The Framingham Study. Ann Intern Med. 1978;89:157–61.
pubmed: 677576
doi: 10.7326/0003-4819-89-2-157
Anderson GL, Manson J, Wallace R, Lund B, Hall D, Davis S, et al. Implementation of the Women’s Health Initiative study design. Ann Epidemiol. 2003;13:S5–17.
pubmed: 14575938
doi: 10.1016/S1047-2797(03)00043-7
Paynter NP, Balasubramanian R, Giulianini F, Wang DD, Tinker LF, Gopal S, et al. Metabolic Predictors of Incident Coronary Heart Disease in Women. Circulation. 2018;137:841–53.
pubmed: 29459470
pmcid: 5854187
doi: 10.1161/CIRCULATIONAHA.117.029468
Huang T, Trudel-Fitzgerald C, Poole EM, Sawyer S, Kubzansky LD, Hankinson SE, et al. The Mind-Body Study: study design and reproducibility and interrelationships of psychosocial factors in the Nurses’ Health Study II. Cancer Causes Control. 2019;30:779–90.
pubmed: 31049751
pmcid: 6631300
doi: 10.1007/s10552-019-01176-0
Robins LN, Helzer JE, Croughan J, Ratcliff KS. National Institute of Mental Health Diagnostic Interview Schedule. Its history, characteristics, and validity. Arch Gen Psychiatry. 1981;38:381–9.
pubmed: 6260053
doi: 10.1001/archpsyc.1981.01780290015001
Andresen EM, Malmgren JA, Carter WB, Patrick DL. Screening for depression in well older adults: evaluation of a short form of the CES-D (Center for Epidemiologic Studies Depression Scale). Am J Prev Med. 1994;10:77–84.
pubmed: 8037935
doi: 10.1016/S0749-3797(18)30622-6
Townsend MK, Clish CB, Kraft P, Wu C, Souza AL, Deik AA, et al. Reproducibility of metabolomic profiles among men and women in 2 large cohort studies. Clin Chem. 2013;59:1657–67.
pubmed: 23897902
doi: 10.1373/clinchem.2012.199133
George SM, Ballard-Barbash R, Manson JE, Reedy J, Shikany JM, Subar AF, et al. Comparing indices of diet quality with chronic disease mortality risk in postmenopausal women in the Women’s Health Initiative Observational Study: evidence to inform national dietary guidance. Am J Epidemiol. 2014;180:616–25.
pubmed: 25035143
pmcid: 4157698
doi: 10.1093/aje/kwu173
Langer RD, White E, Lewis CE, Kotchen JM, Hendrix SL, Trevisan M. The Women’s Health Initiative Observational Study: baseline characteristics of participants and reliability of baseline measures. Ann Epidemiol. 2003;13:S107–21.
pubmed: 14575943
doi: 10.1016/S1047-2797(03)00047-4
Huang T, Zeleznik OA, Poole EM, Clish CB, Deik AA, Scott JM, et al. Habitual sleep quality, plasma metabolites and risk of coronary heart disease in post-menopausal women. Int J Epidemiol. 2019;48:1262–74.
pubmed: 30371783
doi: 10.1093/ije/dyy234
Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C, Witschi J, et al. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol. 1985;122:51–65.
pubmed: 4014201
doi: 10.1093/oxfordjournals.aje.a114086
Wolf AM, Hunter DJ, Colditz GA, Manson JE, Stampfer MJ, Corsano KA, et al. Reproducibility and validity of a self-administered physical activity questionnaire. Int J Epidemiol. 1994;23:991–9.
pubmed: 7860180
doi: 10.1093/ije/23.5.991
Huang T, Poole EM, Vetter C, Rexrode KM, Kubzansky LD, Schernhammer E, et al. Habitual sleep quality and diurnal rhythms of salivary cortisol and dehydroepiandrosterone in postmenopausal women. Psychoneuroendocrinology. 2017;84:172–80.
pubmed: 28738312
pmcid: 5561416
doi: 10.1016/j.psyneuen.2017.07.484
Hertzmark E, Spiegelman D. The SAS METAANAL Macro. 2012. https://www.hsph.harvard.edu/donna-spiegelman/software/metaanal/ .
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.
doi: 10.1016/0197-2456(86)90046-2
pubmed: 3802833
Storey JD. A direct approach false discovery rates. R Stat Soc. 2002;64:479–98.
doi: 10.1111/1467-9868.00346
Dunlop DD, Song J, Lyons JS, Manheim LM, Chang RW. Racial/ethnic differences in rates of depression among preretirement adults. Am J Public Health. 2003;93:1945–52.
pubmed: 14600071
pmcid: 1199525
doi: 10.2105/AJPH.93.11.1945
Patel MJ, Batch BC, Svetkey LP, Bain JR, Turer CB, Haynes C, et al. Race and sex differences in small-molecule metabolites and metabolic hormones in overweight and obese adults. Omics. 2013;17:627–35.
pubmed: 24117402
pmcid: 3837434
doi: 10.1089/omi.2013.0031
Krystal JH, Sanacora G, Blumberg H, Anand A, Charney DS, Marek G, et al. Glutamate and GABA systems as targets for novel antidepressant and mood-stabilizing treatments. Mol Psychiatry. 2002;7:S71–80.
pubmed: 11986998
doi: 10.1038/sj.mp.4001021
Musazzi L, Treccani G, Mallei A, Popoli M. The action of antidepressants on the glutamate system: regulation of glutamate release and glutamate receptors. Biol Psychiatry. 2013;73:1180–8.
pubmed: 23273725
doi: 10.1016/j.biopsych.2012.11.009
Czysz AH, South C, Gadad BS, Arning E, Soyombo A, Bottiglieri T, et al. Can targeted metabolomics predict depression recovery? Results from the CO-MED trial. Transl Psychiatry. 2019;9:11.
pubmed: 30664617
pmcid: 6341111
doi: 10.1038/s41398-018-0349-6
Dinoff A, Herrmann N, Lanctot KL. Ceramides and depression: a systematic review. J Affect Disord. 2017;213:35–43.
pubmed: 28189963
doi: 10.1016/j.jad.2017.02.008
Demirkan A, Isaacs A, Ugocsai P, Liebisch G, Struchalin M, Rudan I, et al. Plasma phosphatidylcholine and sphingomyelin concentrations are associated with depression and anxiety symptoms in a Dutch family-based lipidomics study. J Psychiatr Res. 2013;47:357–62.
pubmed: 23207112
doi: 10.1016/j.jpsychires.2012.11.001
Zheng P, Gao HC, Li Q, Shao WH, Zhang ML, Cheng K, et al. Plasma metabonomics as a novel diagnostic approach for major depressive disorder. J Proteome Res. 2012;11:1741–8.
pubmed: 22239730
doi: 10.1021/pr2010082
Paige LA, Mitchell MW, Krishnan KR, Kaddurah-Daouk R, Steffens DC. A preliminary metabolomic analysis of older adults with and without depression. Int J Geriatr Psychiatry. 2007;22:418–23.
pubmed: 17048218
doi: 10.1002/gps.1690
Assies J, Pouwer F, Lok A, Mocking RJ, Bockting CL, Visser I, et al. Plasma and erythrocyte fatty acid patterns in patients with recurrent depression: a matched case-control study. PLoS ONE. 2010;5:e10635.
pubmed: 20498721
pmcid: 2871041
doi: 10.1371/journal.pone.0010635
Pan JX, Xia JJ, Deng FL, Liang WW, Wu J, Yin BM, et al. Diagnosis of major depressive disorder based on changes in multiple plasma neurotransmitters: a targeted metabolomics study. Transl Psychiatry. 2018;8:130.
pubmed: 29991685
pmcid: 6039504
doi: 10.1038/s41398-018-0183-x
Boland EM, Rao H, Dinges DF, Smith RV, Goel N, Detre JA, et al. Meta-analysis of the antidepressant effects of acute sleep deprivation. J Clin Psychiatry. 2017;78:e1020–34.
pubmed: 28937707
doi: 10.4088/JCP.16r11332
Dallaspezia S, Benedetti F. Sleep deprivation therapy for depression. Curr Top Behav Neurosci. 2015;25:483–502.
pubmed: 25549913
doi: 10.1007/7854_2014_363
Davies SK, Ang JE, Revell VL, Holmes B, Mann A, Robertson FP, et al. Effect of sleep deprivation on the human metabolome. Proc Natl Acad Sci USA. 2014;111:10761–6.
pubmed: 25002497
pmcid: 4115565
doi: 10.1073/pnas.1402663111
Quak J, Doornbos B, Roest AM, Duivis HE, Vogelzangs N, Nolen WA, et al. Does tryptophan degradation along the kynurenine pathway mediate the association between pro-inflammatory immune activity and depressive symptoms? Psychoneuroendocrinology. 2014;45:202–10.
pubmed: 24845191
doi: 10.1016/j.psyneuen.2014.03.013
Shabel SJ, Proulx CD, Piriz J, Malinow R. Mood regulation. GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment. Science. 2014;345:1494–8.
pubmed: 25237099
pmcid: 4305433
doi: 10.1126/science.1250469
Ussher JR, Elmariah S, Gerszten RE, Dyck JR. The emerging role of metabolomics in the diagnosis and prognosis of cardiovascular disease. J Am Coll Cardiol. 2016;68:2850–70.
pubmed: 28007146
doi: 10.1016/j.jacc.2016.09.972
Guasch-Ferre M, Hruby A, Toledo E, Clish CB, Martinez-Gonzalez MA, Salas-Salvado J, et al. Metabolomics in prediabetes and diabetes: a systematic review and meta-analysis. Diabetes Care. 2016;39:833–46.
pubmed: 27208380
pmcid: 4839172
doi: 10.2337/dc15-2251
Rhee EP, Cheng S, Larson MG, Walford GA, Lewis GD, McCabe E, et al. Lipid profiling identifies a triacylglycerol signature of insulin resistance and improves diabetes prediction in humans. J Clin Invest. 2011;121:1402–11.
pubmed: 21403394
pmcid: 3069773
doi: 10.1172/JCI44442
Cheng S, Rhee EP, Larson MG, Lewis GD, McCabe EL, Shen D, et al. Metabolite profiling identifies pathways associated with metabolic risk in humans. Circulation. 2012;125:2222–31.
pubmed: 22496159
pmcid: 3376658
doi: 10.1161/CIRCULATIONAHA.111.067827
Wurtz P, Havulinna AS, Soininen P, Tynkkynen T, Prieto-Merino D, Tillin T, et al. Metabolite profiling and cardiovascular event risk: a prospective study of 3 population-based cohorts. Circulation. 2015;131:774–85.
pubmed: 25573147
pmcid: 4351161
doi: 10.1161/CIRCULATIONAHA.114.013116
Shah SH, Bain JR, Muehlbauer MJ, Stevens RD, Crosslin DR, Haynes C, et al. Association of a peripheral blood metabolic profile with coronary artery disease and risk of subsequent cardiovascular events. Circ Cardiovasc Genet. 2010;3:207–14.
pubmed: 20173117
doi: 10.1161/CIRCGENETICS.109.852814
Yu E, Ruiz-Canela M, Guasch-Ferre M, Zheng Y, Toledo E, Clish CB, et al. Increases in plasma tryptophan are inversely associated with incident cardiovascular disease in the Prevencion con Dieta Mediterranea (PREDIMED) Study. J Nutr. 2017;147:314–22.
pubmed: 28179491
pmcid: 5320398
Wang TJ, Larson MG, Vasan RS, Cheng S, Rhee EP, McCabe E, et al. Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17:448–53.
pubmed: 21423183
pmcid: 3126616
doi: 10.1038/nm.2307
Ruiz-Canela M, Toledo E, Clish CB, Hruby A, Liang L, Salas-Salvado J, et al. Plasma branched-chain amino acids and incident cardiovascular disease in the PREDIMED Trial. Clin Chem. 2016;62:582–92.
pubmed: 26888892
pmcid: 4896732
doi: 10.1373/clinchem.2015.251710
Magnusson M, Lewis GD, Ericson U, Orho-Melander M, Hedblad B, Engstrom G, et al. A diabetes-predictive amino acid score and future cardiovascular disease. Eur Heart J. 2013;34:1982–9.
pubmed: 23242195
doi: 10.1093/eurheartj/ehs424
Puyat JH, Kazanjian A, Wong H, Goldner E. Comorbid chronic general health conditions and depression care: a population-based analysis. Psychiatr Serv. 2017;68:907–15.
pubmed: 28457213
doi: 10.1176/appi.ps.201600309
Menear M, Dore I, Cloutier AM, Perrier L, Roberge P, Duhoux A, et al. Chronic physical comorbidity burden and the quality of depression treatment in primary care: a systematic review. J Psychosom Res. 2015;78:314–23.
pubmed: 25649274
doi: 10.1016/j.jpsychores.2015.01.001
Pan A, Lucas M, Sun Q, van Dam RM, Franco OH, Manson JE, et al. Bidirectional association between depression and type 2 diabetes mellitus in women. Arch Intern Med. 2010;170:1884–91.
pubmed: 21098346
pmcid: 3065781
doi: 10.1001/archinternmed.2010.356
Whang W, Kubzansky LD, Kawachi I, Rexrode KM, Kroenke CH, Glynn RJ, et al. Depression and risk of sudden cardiac death and coronary heart disease in women: results from the Nurses’ Health Study. J Am Coll Cardiol. 2009;53:950–8.
pubmed: 19281925
pmcid: 2664253
doi: 10.1016/j.jacc.2008.10.060
Huang T, Poole EM, Okereke OI, Kubzansky LD, Eliassen AH, Sood AK, et al. Depression and risk of epithelial ovarian cancer: results from two large prospective cohort studies. Gynecol Oncol. 2015;139:481–6.
pubmed: 26449316
pmcid: 4679423
doi: 10.1016/j.ygyno.2015.10.004
Yin P, Lehmann R, Xu G. Effects of pre-analytical processes on blood samples used in metabolomics studies. Anal Bioanal Chem. 2015;407:4879–92.
pubmed: 25736245
pmcid: 4471316
doi: 10.1007/s00216-015-8565-x
Townsend MK, Bao Y, Poole EM, Bertrand KA, Kraft P, Wolpin BM, et al. Impact of pre-analytic blood sample collection factors on metabolomics. Cancer Epidemiol Biomark Prev. 2016;25:823–29.
doi: 10.1158/1055-9965.EPI-15-1206