Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-06-06T13:25:18.494Z Has data issue: false hasContentIssue false

Plasma redox and inflammatory patterns during major depressive episodes: a cross-sectional investigation in elderly patients with mood disorders

Published online by Cambridge University Press:  19 May 2020

Barbara Carpita*
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Laura Betti
Affiliation:
Department of Pharmacy, University of Pisa, Pisa, Italy
Lionella Palego
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Natalia Bartolommei
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Lucia Chico
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Livia Pasquali
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Gabriele Siciliano
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Fabio Monzani
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Riccardo Franchi
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Sara Rogani
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Federico Mucci
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Camilla Elefante
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Lorenzo Lattanzi
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Donatella Marazziti
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
Gino Giannaccini
Affiliation:
Department of Pharmacy, University of Pisa, Pisa, Italy
Liliana Dell’Osso
Affiliation:
Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
*
Barbara Carpita, MD Email: barbara.carpita1986@gmail.com

Abstract

Background

While both depression and aging have been associated with oxidative stress and impaired immune response, little is known about redox patterns in elderly depressed subjects. This study investigates the relationship between redox/inflammatory patterns and depression in a sample of elderly adults.

Methods

The plasma levels of the advanced products of protein oxidation (AOPP), catalase (CAT), ferric reducing antioxidant power (FRAP), glutathione transferase (GST), interleukin 6 (IL-6), superoxide dismutase (SOD), total thiols (TT), and uric acid (UA) were evaluated in 30 patients with mood disorders with a current depressive episode (depressed patients, DP) as well as in 30 healthy controls (HC) aged 65 years and over. Subjects were assessed with the Hamilton Depression Rating Scale (HAM-D), the Hamilton Rating Scale for Anxiety (HAM-A), the Geriatric Depression Rating Scale (GDS), the Scale for Suicide Ideation (SSI), the Reason for Living Inventory (RFL), the Activities of Daily Living (ADL), and the Instrumental Activity of Daily Living (IADL).

Results

DP showed higher levels than HC of AOPP and IL-6, while displaying lower levels of FRAP, TT, and CAT. In the DP group, specific correlations were found among biochemical parameters. SOD, FRAP, UA, and TT levels were also significantly related to psychometric scale scores.

Conclusion

Specific alterations of redox systems are detectable among elderly DP.

Type
Original Research
Copyright
© The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Barbara Carpita and Laura Betti contributed equally to the work. Gino Giannaccini and Liliana Dell’Osso contributed equally to the work.

References

Kessler, RC, Bromet, EJ. The epidemiology of depression across cultures. Annu Rev Public Health. 2013;34:119138.CrossRefGoogle ScholarPubMed
Lim, GY, Tam, WW, Lu, Y, et al. Prevalence of Depression in the Community from 30 Countries between 1994 and 2014. Sci Rep. 2008;8(1):2861CrossRefGoogle Scholar
Kessler, RC, Berglund, P, Demler, O, et al. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005;62(6):593602.CrossRefGoogle ScholarPubMed
Wittchen, HU, Jacobi, F, Rehm, J, et al. The size and burden of mental disorders and other disorders of the brain in Europe 2010. Eur Neuropsychopharmacol. 2011;21(9):655679.CrossRefGoogle ScholarPubMed
Martin, J, Streit, F, Treutlein, J, et al. Expert and self-assessment of lifetime symptoms and diagnosis of major depressive disorder in large-scale genetic studies in the general population: comparison of a clinical interview and a self-administered checklist. Psychiatr Genet. 2017;27(5):187196.CrossRefGoogle Scholar
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (5th ed). Washington, DC: American Psychiatric Association; 2013.Google Scholar
Cheng, ST, Fung, HH, Chan, AC. Self-perception and psychological well-being: the benefits of foreseeing a worse future. Psychol Aging. 2009;24(2):623633.CrossRefGoogle ScholarPubMed
Aziz, R, Steffens, DC. What are the causes of late-life depression? Psychiatr Clin North Am. 2013;36(4):497516.CrossRefGoogle ScholarPubMed
Valiengo Lda, C, Stella, F, Forlenza, OV. Mood disorders in the elderly: prevalence, functional impact, and management challenges. Neuropsychiatr Dis Treat. 2016;12:21052114.Google ScholarPubMed
Pandya, CD, Howell, KR, Pillai, A. Antioxidants as potential therapeutics for neuropsychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry. 2013;46:214223.CrossRefGoogle ScholarPubMed
Lemogne, C, Gorwood, P, Boni, C, et al. Cognitive appraisal and life stress moderate the effects of the 5-HTTLPR polymorphism on amygdala reactivity. Hum Brain Mapp. 2011;32(11):18561867.CrossRefGoogle ScholarPubMed
Roy, A, Campbell, MK. A unifying framework for depression: bridging the major biological and psychosocial theories through stress. Clin Invest Med. 2013;36(4):E170E190.CrossRefGoogle ScholarPubMed
Carpita, B, Marazziti, D, Palego, L, et al. Microbiota, immune system and autism spectrum disorders. An integrative model towards novel treatment options. Curr Med Chem. 2019; doi:10.2174/0929867326666190328151539. [epub ahead of print].Google Scholar
Leonard, BE. The HPA and immune axes in stress: the involvement of the serotonergic system. Eur Psychiatry. 2005;20(Suppl 3):S302S306.CrossRefGoogle ScholarPubMed
Maletic, V, Robinson, M, Oakes, T, et al. Neurobiology of depression: an integrated view of key findings. Int J Clin Pract. 2007;61(12):20302040.CrossRefGoogle ScholarPubMed
Maes, M. Inflammatory and oxidative and nitrosative stress pathways underpinning chronic fatigue, somatization and psychosomatic symptoms. Curr Opin Psychiatry. 2009;22(1):7583.CrossRefGoogle ScholarPubMed
Orzechowska, A, Zajączkowska, M, Talarowska, M, et al. Depression and ways of coping with stress: a preliminary study. Med Sci Monit. 2013;19:10501056.CrossRefGoogle ScholarPubMed
Jeon, SW, Kim, YK. Molecular neurobiology and promising new treatment in depression. Int J Mol Sci. 2016;17(3):381CrossRefGoogle ScholarPubMed
Dantzer, R, O’Connor, JC, Freund, GG, et al. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):4656.CrossRefGoogle ScholarPubMed
Schiepers, OJS, Wichers, MC, Maes, M. Cytokines and major depression. Progr Neuro-Psychopharmacol Biol Psychiatry. 2005;29(2):201217.CrossRefGoogle ScholarPubMed
Halliwell, B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol. 2006;141(2):312322.CrossRefGoogle ScholarPubMed
Maes, M, Yirmyia, R, Noraberg, J, et al. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab Brain Dis. 2009;24(1):2753.CrossRefGoogle ScholarPubMed
Michel, TM, Pülschen, D, Thome, J. The role of oxidative stress in depressive disorders. Curr Pharm Des. 2012;18(36):58905899.CrossRefGoogle ScholarPubMed
Zunszain, PA, Anacker, C, Cattaneo, A, et al. Glucocorticoids, cytokines and brain abnormalities in depression. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35(3):722729.CrossRefGoogle ScholarPubMed
Maes, M, Landucci Bonifacio, K, Morelli, NR, et al. Major differences in neurooxidative and neuronitrosative stress pathways between major depressive disorder and types I and II bipolar disorder. Mol Neurobiol. 2019;56(1):141156.CrossRefGoogle ScholarPubMed
Yang, C, Wardenaar, KJ, Bosker, FJ, et al. Inflammatory markers and treatment outcome in treatment resistant depression: a systematic review. J Affect Disord. 2019;257:640649.CrossRefGoogle ScholarPubMed
Leonard, BE. The concept of depression as a dysfunction of the immune system. Curr Immunol Rev. 2010;6(3):205212.CrossRefGoogle ScholarPubMed
Leonard, BE, Maes, M. Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci Biobehav Rev. 2012;36(2):764785.CrossRefGoogle ScholarPubMed
Miller, AH, Maletic, V, Raison, CL. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry. 2009;65(9):732741.CrossRefGoogle ScholarPubMed
Sanacora, G, Treccani, G, Popoli, M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology. 2012;62(1):6377.CrossRefGoogle ScholarPubMed
Duman, RS, Monteggia, LM. A neurotrophic model for stress-related mood disorders. Biol Psychiatry. 2006;59:11161127.CrossRefGoogle ScholarPubMed
Catena Dell’Osso, M, Bellantuono, C, Consoli, G, et al. Inflammatory and neurodegenerative pathways in depression: a new avenue for antidepressant development? Curr Med Chem. 2011;18(2):245255.CrossRefGoogle ScholarPubMed
Choi, S, Lee, S, Matejkowski, J, et al. The relationships among depression, physical health conditions and healthcare expenditures for younger and older Americans. J Mental Health. 2014;23(3):140145.CrossRefGoogle ScholarPubMed
Park, SJ, Hong, S, Jang, H, et al. The prevalence of chronic physical diseases comorbid with depression among different sex and age groups in South Korea: a population-based study, 2007-2014. Psychiatry Investig. 2018;15(4):370375.CrossRefGoogle ScholarPubMed
Zhang, Y, Chen, Y, Ma, L. Depression and cardiovascular disease in elderly: current understanding. J Clin Neurosci. 2018;47:15.CrossRefGoogle ScholarPubMed
Sergiev, PV, Dontsova, OA, Berezkin, GV. Theories of aging: an ever-evolving field. Acta Naturae. 2015;7(1):918.CrossRefGoogle Scholar
Diniz, BS, Mendes-Silva, AP, Silva, LB, et al. Oxidative stress markers imbalance in late-life depression. J Psychiatry Res. 2018;102:2933.CrossRefGoogle ScholarPubMed
Wolkowitz, OM, Mellon, SH, Epel, ES, et al. Leukocyte telomere length in major depression: correlations with chronicity, inflammation and oxidative stress-preliminary findings. PLoS One. 2011;6(3):e17837CrossRefGoogle ScholarPubMed
Ishihara, L, Brayne, C. A systematic review of depression and mental illness preceding Parkinson’s disease. Acta Neurol Scand. 2006;113(4):211220.CrossRefGoogle ScholarPubMed
Fiske, A, Wetherell, JL, Gatz, M. Depression in older adults. Annu Rev Clin Psychol. 2009;5:363389.CrossRefGoogle ScholarPubMed
Aarsland, D, Påhlhagen, S, Ballard, CG, et al. Depression in Parkinson disease-epidemiology, mechanisms and management. Nat Rev Neurol. 2012;8(1):3547.CrossRefGoogle Scholar
Milaneschi, Y, Cesari, M, Simonsick, EM, et al. Lipid peroxidation and depressed mood in community-dwelling older men and women. PLoS One. 2013;8(6):e65406CrossRefGoogle ScholarPubMed
Palta, P, Samuel, LJ, Miller, ER srd, et al. Depression and oxidative stress: results from a meta-analysis of observational studies. Psychosom Med . 2014;76(1):1219.CrossRefGoogle ScholarPubMed
Witko-Sarsat, V, Friedlander, M, Nguyen Khoa, T, et al. Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. J Immunol. 1998;161(5):25242532.Google ScholarPubMed
Lushchak, V. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact. 2014;224:164175.CrossRefGoogle ScholarPubMed
Maes, M, Bonifacio, KL, Morelli, NR, et al. Generalized anxiety disorder (GAD) and comorbid major depression with GAD are characterized by enhanced nitro-oxidative stress, increased lipid peroxidation, and lowered lipid-associated antioxidant defenses. Neurotox Res. 2018;34(3):489510.CrossRefGoogle ScholarPubMed
Ho, RCM, Chua, AC, Tran, BX, et al. Factors associated with the risk of developing coronary artery disease in medicated patients with major depressive disorder. Int J Environ Res Public Health. 2018;15(10):E2073CrossRefGoogle ScholarPubMed
Lopresti, AL, Hood, SD, Drummond, PD. A review of lifestyle factors that contribute to important pathways associated with major depression: diet, sleep and exercise. J Affect Disord. 2013;148(1):1227.CrossRefGoogle ScholarPubMed
Magalhães, LM, Segundo, MA, Reis, S, et al. Methodological aspects about in vitro evaluation of antioxidant properties. Anal Chimica Acta. 2008;613(1):119.CrossRefGoogle ScholarPubMed
Glantzounis, GK, Tsimoyiannis, EC, Kappas, AM, et al. Uric acid and oxidative stress. Curr Pharm Des. 2005;11(32):41454151.CrossRefGoogle ScholarPubMed
Wium-Andersen, MK, Kobylecki, CJ, Afzal, S, et al. Association between the antioxidant uric acid and depression and antidepressant medication use in 96 989 individuals. Acta Psychiatr Scand. 2017;136(4):424433.CrossRefGoogle ScholarPubMed
Wigner, P, Czarny, P, Galecki, P, et al. The molecular aspects of oxidative & nitrosative stress and the tryptophan catabolites pathway (TRYCATs) as potential causes of depression. Psychiatry Res. 2018;262:566574.CrossRefGoogle ScholarPubMed
Aquilano, K, Baldelli, S, Ciriolo, MR. Glutathione: new roles in redox signaling for an old antioxidant. Front Pharmacol. 2014;5:196CrossRefGoogle ScholarPubMed
Palego, L, Betti, L, Giannaccini, G. Sulfur metabolism and sulfur-containing amino acids: I—molecular effectors. Biochem Pharmacol. 2015;4:158Google Scholar
Durmaz, O, İspir, E, Baykan, H, et al. The impact of repetitive transcranial magnetic stimulation on oxidative stress in subjects with medication-resistant depression. J ECT. 2018;34(2):127131.CrossRefGoogle ScholarPubMed
Zhang, H, Davies, KJA, Forman, HJ. Oxidative stress response and Nrf2 signaling in aging. Free Radic Biol Med. 2015;88(Pt B):314336.CrossRefGoogle Scholar
Andreazza, AC, Gildengers, A, Rajji, , et al. Oxidative stress in older patients with bipolar disorder. Am J Geriatr Psychiatry. 2015;23(3):314319.CrossRefGoogle ScholarPubMed
Brink, TL, Yesavage, JA, Lum, O, et al. Screening test for geriatric depression. Clin Gerontol. 1981;1(1):3743.CrossRefGoogle Scholar
Hamilton, M. A rating scale for depression. J Neurol Neurosurg Psychiat. 1960;23:5662.CrossRefGoogle ScholarPubMed
Hamilton, M. The assessment of anxiety states by rating. Brit J Med Psychol. 1958;32:5055.CrossRefGoogle Scholar
Linehan, MM, Goodstein, JL, Nielsen, SL, et al. Reasons for staying alive when you’re thinking of killing yourself: The Reasons for Living Inventory. J Consult Clin Psychol. 1983;51(2):276286.CrossRefGoogle Scholar
Beck, AT, Rensik, HL, Lettieri, DJ, eds. The Prediction of Suicide. Bowie, MD: Charles Press; 1974.Google Scholar
Katz, S, Ford, AB, Moskowitz, RW, et al. Studies of illness in the aged—the index of ADL: a standardize measure of biological and psychosocial function. JAMA. 1963;185:914919.CrossRefGoogle Scholar
Lawton, MP, Brody, EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9(3):179186.CrossRefGoogle ScholarPubMed
Witko-Sarsat, V, Friedlander, M, Capeillère-Blandin, C, et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney International. 1996;49(5):13041313.CrossRefGoogle ScholarPubMed
Benzie, IFF, Strain, JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996;239(1):7076.CrossRefGoogle ScholarPubMed
Helenius, M, Jalkanen, S, Yegutkin, GG. Enzyme-coupled assays for simultaneous detection of nanomolar ATP, ADP, AMP, adenosine, inosine and pyrophosphate concentrations in extracellular fluids. Biochim Biophys Acta: Mol Cell Res. 2012;1823(10):19671975.CrossRefGoogle ScholarPubMed
Hu, ML. Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol. 1994;233:380385.CrossRefGoogle ScholarPubMed
Peskin, AV, Winterbourn, CC. A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1). Clin Chim Acta. 2000;293(1–2):157166.CrossRefGoogle Scholar
Zhou, JY, Prognon, P. Raw material enzymatic activity determination: a specific case for validation and comparison of analytical methods—the example of superoxide dismutase (SOD). J Pharm Biomed Anal. 2006;40(5):11431148.CrossRefGoogle Scholar
Johansson, LH, Borg, LA. A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem. 1988;174(1):331336.CrossRefGoogle ScholarPubMed
Jendral, JA, Monakhova, YB, Lachenmeier, DW. Formaldehyde in alcoholic beverages: large chemical survey using purpald screening followed by chromotropic Acid spectrophotometry with multivariate curve resolution. Int J Anal Chem. 2011;2011:797604CrossRefGoogle ScholarPubMed
Habig, WH, Pabst, MJ, Jakoby, WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):71307139.CrossRefGoogle ScholarPubMed
Salk, RH, Hyde, JS, Abramson, LY. Gender differences in depression in representative national samples: meta-analyses of diagnoses and symptoms. Psychol Bull. 2017;143(8):783822.CrossRefGoogle ScholarPubMed
Connoly, D, Garvey, J, McKee, G. Factors associated with ADL/IADL disability in community dwelling older adults in the Irish longitudinal study on ageing (TILDA). Disabil Rehabil. 2017;39(8):809816.CrossRefGoogle Scholar
Sonka, K, Fialová, L, Volná, J, et al. Advanced oxidation protein products in obstructive sleep apnea. Prague Med Rep. 2008;109(2–3):159165.Google ScholarPubMed
Lo Gerfo, A, Chico, L, Borgia, L, et al. Lack of association between nuclear factor erythroid-derived 2-like 2 promoter gene polymorphisms and oxidative stress biomarkers in amyotrophic lateral sclerosis patients. Oxid Med Cell Longev. 2014;2014:432626Google Scholar
Mancuso, M, Orsucci, D, Logerfo, A, et al. Oxidative stress biomarkers in mitochondrial myopathies, basally and after cysteine donor supplementation. J Neurol. 2010;257(5):774781.CrossRefGoogle ScholarPubMed
Gautam, M, Agrawal, M, Gautam, M, et al. Role of antioxidants in generalised anxiety disorder and depression. Indian J Psychiatry. 2012;54(3):244247.CrossRefGoogle ScholarPubMed
Ozcan, ME, Gulec, M, Ozerol, E, et al. Antioxidant enzyme activities and oxidative stress in affective disorders. Int Clin Psychopharmacol. 2004;19:8995.CrossRefGoogle ScholarPubMed
Vaváková, M, Ďuračková, Z, Trebatická, J. Markers of oxidative stress and neuroprogression in depression disorder. Oxidative Med Cell Longevity. 2015;2015:898393CrossRefGoogle ScholarPubMed
Balcerczyk, A, Bartosz, G. Thiols are main determinants of total antioxidant capacity of cellular homogenates. Free Radic Res. 2003;37(5):37541.CrossRefGoogle ScholarPubMed
Dowlati, Y, Herrmann, N, Swardfager, W, et al. A meta-analysis of cytokines in major depression. Biol Psychiatry. 2010;67(5):446457.CrossRefGoogle ScholarPubMed
Hellwig, S, Domschke, K. Anxiety in late life: an update on pathomechanisms. Gerontology. 2019;65(5):465473.CrossRefGoogle ScholarPubMed
Ballatori, N, Krance, SM, Notenboom, S, et al. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem. 2009;390(3):191214.CrossRefGoogle ScholarPubMed
Aoyama, K, Nakaki, T. Impaired glutathione dynthesis in neurodegeneration. Int J Mol Sci. 2013;14(10):2102121044.CrossRefGoogle Scholar
Song, EA, Lim, JW, Kim, H. Docosahexaenoic acid inhibits IL-6 expression via PPARγ-mediated expression of catalase in cerulein-stimulated pancreatic acinar cells. Int J Biochem Cell Biol. 2017;88:6068.CrossRefGoogle ScholarPubMed
Vargas, HO, Nunes, SO, Pizzo de Castro, M, et al. Oxidative stress and lowered total antioxidant status are associated with a history of suicide attempts. J Affect Disord. 2013;150(3):923930.CrossRefGoogle ScholarPubMed
Andreazza, AC, Kauer-Sant’anna, M, Frey, BN, et al. Oxidative stress markers in bipolar disorder: a meta-analysis. J Affect Disord. 2008;111(2–3):135144.CrossRefGoogle ScholarPubMed
Andreazza, AC, Kapczinski, F, Kauer-Sant’Anna, M, et al. 3-Nitrotyrosine and glutathione antioxidant system in patients in the early and late stages of bipolar disorder. J Psychiatry Neurosci. 2009;34(4):263271.Google ScholarPubMed
Carpita, B, Muti, D, Dell’Osso, L. Oxidative stress, maternal diabetes, and autism spectrum disorders. Oxid Med Cell Longev. 2018;2018:3717215CrossRefGoogle ScholarPubMed
Supplementary material: File

Carpita et al. Supplementary Materials

Carpita et al. Supplementary Materials

Download Carpita et al. Supplementary Materials(File)
File 36.9 KB