Cited by 615Tryptophan and brain disordersNeuroinflammation and Neurodegeneration MechanismsTreatment of Major Depression

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Markers of central inflammation in major depressive disorder: A systematic review and meta-analysis of studies examining cerebrospinal fluid, positron emission tomography and post-mortem brain tissue

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Enache, Daniela, Pariante, Carmine M., Mondelli, Valeria·2019·Brain, Behavior, and Immunity

DOI 10.1016/j.bbi.2019.06.015

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Abstract

BACKGROUND Increased peripheral inflammation has been consistently reported in patients with major depressive disorder (MDD). However, only few studies have explored markers of central (brain) inflammation in patients with MDD. The aim of this study is to systematically review in vivo and post-mortem markers of central inflammation, including studies examining cerebrospinal fluid (CSF), positron emission tomography, and post-mortem brain tissues in subjects suffering with MDD compared with controls. METHODS PubMed and Medline databases were searched up to December 2018. We included studies measuring cerebrospinal fluid (CSF) cytokines and chemokines, positron emission tomography (PET) studies; and post-mortem studies measuring cytokines, chemokines and cell-specific markers of microglia and astrocytes, all in MDD. A meta-analysis was performed only for CSF and PET studies, as studies on post-mortem markers of inflammation had different cell-specific markers and analysed different brain regions. RESULTS A total of 69 studies met the inclusion criteria. CSF levels of IL-6 and TNF-α were higher in patients with MDD compared with controls (standardised mean difference SMD 0.37, 95%CI: 0.17-0.57 and SMD 0.58, 95%CI 0.26-0.90, respectively). CSF levels of IL-6 were increased in suicide attempters regardless of their psychiatric diagnosis. Translocator protein, a PET marker of central inflammation, was elevated in the anterior cingulate cortex and temporal cortex of patients with MDD compared with controls (SMD 0.78, 95%CI: 0.41-1.16 and SMD 0.52, 95%CI: 0.19-0.85 respectively). Abnormalities in CSF and PET inflammatory markers were not correlated with those in peripheral blood. In post-mortem studies, two studies found increased markers of microglia in MDD brains, while four studies found no MDD related changes. Of the studies investigating expression of cell-specific marker for astrocytes, thirteen studies reported a decreased expression of astrocytes specific markers, two studies reported increased expression of astrocytes specific markers, and eleven studies did not detect any difference. Four out of six studies reported decreased markers of oligodendrocytes in the prefrontal cortex. Post-mortem brain levels of tumor necrosis alpha (TNF-α) were also found increased in MDD. CONCLUSIONS Our review suggests the presence of an increase in IL-6 and TNF-alpha levels in CSF and brain parenchyma, in the context of a possible increased microglia activity and reduction of astrocytes and oligodendrocytes markers in MDD. The reduced number of astrocytes may lead to compromised integrity of blood brain barrier with increased monocyte recruitment and infiltration, which is partly supported by post-mortem studies and by PET studies showing an increased TSPO expression in MDD.

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BackgroundInfluential
White Matter Abnormalities in First-Episode, Treatment-Naive Young Adults With Major Depressive Disorder
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Glial fibrillary acidic protein is differentially expressed across cortical and subcortical regions in healthy brains and downregulated in the thalamus and caudate nucleus of depressed suicides
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BackgroundResultInfluential
Astrogliopathology
Verkhratsky, A., Rodriguez, J. J., & Steardo, L. (2013) · The Neuroscientist · doi:10.1177/1073858413510208 · Cited by 147 · cited 1×
“Additionally, the GAP junction between astrocytes and astrocytes and between astrocytes and neurons may be affected and this would lead to an impairment in the ion homeostasis and synaptic circuit (Rajkowska and Stockmeier, 2013; Verkhratsky et al., 2014).”
Background
Glial fibrillary acidic protein is reduced in cerebellum of subjects with major depression, but not schizophrenia
Fatemi, S. H., Laurence, J. A., Araghi‐Niknam, M., Stary, J. M., Schulz, S. C., Lee, S. S., & Gottesman, I. I. (2003) · Schizophrenia Research · doi:10.1016/j.schres.2003.08.014 · Cited by 141 · cited 2×
“, 2017), lateral cerebellum (Fatemi et al., 2004), and white matter in ventral prefrontal cortex (Rajkowska et al.”
Background
Translocator protein (18 kDa TSPO) binding, a marker of microglia, is reduced in major depression during cognitive-behavioral therapy
Li, H., Sagar, A. P., & Kéri, S. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.12.011 · Cited by 134 · cited 6×
“First (Holmes et al., 2018; Su et al., 2016) and second (Hannestad et al., 2013; Li et al., 2018; Richards et al., 2018; Setiawan et al., 2018) generation TSPO PET tracers were used.”
BackgroundMethodInfluential
PROINFLAMMATORY AND “RESILIENCY” PROTEINS IN THE CSF OF PATIENTS WITH MAJOR DEPRESSION: Cytokines, Resiliency Proteins and Major Depression
Martinez, J. M., Garakani, A., Yehuda, R., & Gorman, J. M. (2012) · Depression and Anxiety · doi:10.1002/da.20876 · Cited by 131 · cited 6×
“Some studies, which found a decreased in neurotrophic factors in patients with MDD, argue that in patients with MDD there is primarily an impairment in synaptic plasticity and neuroplasticity (Martinez et al., 2012)(Rajkowska and Stockmeier, 2013).”
BackgroundResultInfluential
CSF and plasma cytokines at delivery and postpartum mood disturbances
Boufidou, F., Lambrinoudaki, I., Argeitis, J., Zervas, I. M., Pliatsika, P., Leonardou, A. A., Petropoulos, G., Hassiakos, D., Papadias, K., & Nikolaou, C. (2008) · Journal of Affective Disorders · doi:10.1016/j.jad.2008.07.008 · Cited by 118 · cited 2×
“9 We included 12 studies which investigated cytokines, chemokines and complement C5 in CSF of MDD patients (Blasko et al., 2006; Boufidou et al., 2009; Carpenter et al., 2004; Hestad et al., 2016; Ishii et al., 2018; Kern et al., 2014; Levine et al., 1999; Lindqvist et al., 2009; Martinez et al., 2012; Palhagen et al.…”
Background
Regionally-specific changes in levels of tumour necrosis factor in the dorsolateral prefrontal cortex obtained postmortem from subjects with major depressive disorder
Dean, B., Tawadros, N., Scarr, E., & Gibbons, A. S. (2009) · Journal of Affective Disorders · doi:10.1016/j.jad.2009.04.027 · Cited by 111
Innate immunity in the postmortem brain of depressed and suicide subjects: Role of Toll-like receptors
Pandey, G. N., Rizavi, H. S., Bhaumik, R., & Ren, X. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.09.024 · Cited by 110 · cited 1×
“, 2019, 2014) found similar levels of toll like receptor 1, 2, 3, 4 mRNA in MDD suicide victims and MDD no suicide victims, but increased levels of protein toll like receptor 3, 4 and 6 in MDD suicide victims compared with MDD non-suicide victims (Pandey et al., 2019).”
Result
Reduced connexin 43 immunolabeling in the orbitofrontal cortex in alcohol dependence and depression
Miguel-Hidalgo, J. J., Wilson, B. A., Hussain, S., Meshram, A., Rajkowska, G., & Stockmeier, C. A. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2014.04.007 · Cited by 110
Toll-Like Receptors 2, -3 and -4 Prime Microglia but not Astrocytes Across Central Nervous System Regions for ATP-Dependent Interleukin-1β Release
Facci, L., Barbierato, M., Marinelli, C., Argentini, C., Skaper, S. D., & Giusti, P. (2014) · Scientific Reports · doi:10.1038/srep06824 · Cited by 109
S100B-immunopositive astrocytes and oligodendrocytes in the hippocampus are differentially afflicted in unipolar and bipolar depression: A postmortem study
Gos, T., Schroeter, M. L., Lessel, W., Bernstein, H.-G., Dobrowolny, H., Schiltz, K., Bogerts, B., & Steiner, J. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.07.005 · Cited by 106 · cited 4×
“We included 12 studies which measured oligodendrocytes in post-mortem MDD brains (Aston et al., 2005; Barley et al., 2009; Gos et al., 2013; Hayashi et al., 2011; Honer et al., 1999; Lutz et al., 2017; Miguel-Hidalgo et al., 2017; Rajkowska et al., 2015; Tanti et al., 2018; Uranova et al., 2004; Vostrikov et al., 2007…”
BackgroundInfluential
Oligodendrocyte morphometry and expression of myelin – Related mRNA in ventral prefrontal white matter in major depressive disorder
Rajkowska, G., Mahajan, G., Maciąg, D., Sathyanesan, M., Iyo, A. H., Moulana, M., Kyle, P. B., Woolverton, W. L., Miguel-Hidalgo, J. J., Stockmeier, C. A., et al. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.04.010 · Cited by 105 · cited 3×
“We included 12 studies which measured oligodendrocytes in post-mortem MDD brains (Aston et al., 2005; Barley et al., 2009; Gos et al., 2013; Hayashi et al., 2011; Honer et al., 1999; Lutz et al., 2017; Miguel-Hidalgo et al., 2017; Rajkowska et al., 2015; Tanti et al., 2018; Uranova et al., 2004; Vostrikov et al., 2007…”
Background
Role of Complex Epigenetic Switching in Tumor Necrosis Factor-α Upregulation in the Prefrontal Cortex of Suicide Subjects
Wang, Q., Roy, B., Turecki, G., Shelton, R. C., & Dwivedi, Y. (2018) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2017.16070759 · Cited by 103 · cited 16×
“CSF levels of IL-6 and TNF-α were higher in patients with MDD compared with controls (standardised mean difference SMD 0.37, 95%CI: 0.17-0.57 and SMD 0.58, 95%CI 0.26-0.90, respectively).”
BackgroundInfluential
Gene expression deficits in pontine locus coeruleus astrocytes in men with major depressive disorder
Chandley, M., Szebeni, K., Szebeni, A., Crawford, J. D., Stockmeier, C. A., Turecki, G., Miguel-Hidalgo, J. J., & Ordway, G. A. (2013) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.120110 · Cited by 101 · cited 5×
“We included 24 studies which assessed astrocytes in postmortem brains of patients with MDD (Altshuler et al., 2010; Barley et al., 2009; Bernard et al., 2011; Chandley et al., 2013; Cobb et al., 2016; Damadzic et al., 2001; Davis et al., 2002; Fatemi et al., 2004; Gos et al., 2013; Miguel-Hidalgo et al., 2014, 2011, 2…”
BackgroundInfluential
Different changes in cortical tumor necrosis factor-α-related pathways in schizophrenia and mood disorders
Dean, B., Gibbons, A. S., Tawadros, N., Brooks, L., Everall, I., & Scarr, E. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.95 · Cited by 99 · cited 2×
“Ten studies measured cytokines (Clark et al., 2016; Dean et al., 2013, 2010; Hoyo-Becerra et al., 2013; Pandey et al., 2019, 2012; Pantazatos et al., 2017; Tonelli et al., 2008; Wang et al., 2018) and chemokines (Clark et al., 2016; Torres-Platas et al., 2014) expression in postmortem brains of MDD…”
BackgroundResult
Glial fibrillary acidic protein and glutamine synthetase in subregions of prefrontal cortex in schizophrenia and mood disorder
Toro, C. T., Hallak, J. E. C., Dunham, J. S., & Deakin, J. F. W. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.05.067 · Cited by 95
Higher CSF Interleukin-6 and CSF Interleukin-8 in Current Depression in Older Women. Results from a Population-Based Sample
Kern, S., Skoog, I., Börjesson-Hanson, A., Blennow, K., Zetterberg, H., Östling, S., Kern, J., Gudmundsson, P., Marlow, T., Rosengren, L., et al. (2014) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.05.006 · Cited by 94
Low plasma vascular endothelial growth factor (VEGF) associated with completed suicide
Isung, J., Mobarrez, F., Nordström, P., Åsberg, M., & Jokinen, J. (2012) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.624549 · Cited by 94 · cited 3×
“Seven studies found no correlation between markers of central inflammation (CSF cytokines or PET TSPO) and peripheral inflammation (Bay-Richter et al., 2015; Hannestad et al., 2013; Holmes et al., 2018; Isung et al., 2012; Lindqvist et al., 2009; Sasayama et al., 2013; Setiawan et al., 2015).”
BackgroundResult
Reduced kynurenine pathway metabolism and cytokine expression in the prefrontal cortex of depressed individuals
Clark, S. M., Pocivavsek, A., Nicholson, J. D., Notarangelo, F. M., LANGENBERG, P. W., McMahon, R. P., Kleinman, J. E., Hyde, T. M., Stiller, J. W., Postolache, T. T., et al. (2016) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.150226 · Cited by 94 · cited 5×
“Clark et al reported an increase in the proportion of IBA1-positive amoebian (active) microglia in the ventrolateral prefrontal cortex of patients with MDD compared with controls and similar density of hypertrophic (non-active) microglia (Clark et al., 2016).”
BackgroundInfluential
Myelination
Barnett, S. C., & Linington, C. (2012) · The Neuroscientist · doi:10.1177/1073858412465655 · Cited by 87 · cited 1×
“Furthermore, an increased level of cytokines and impairment in astrocytes function may lead to an impairment of the myelination and reduced oligodendrocytes density (Barnett and Linington, 2013; Rajkowska et al., 2018).”
Background
Decreased quinolinic acid in the hippocampus of depressive patients: evidence for local anti-inflammatory and neuroprotective responses?
Busse, M., Busse, S., Myint, A.-M., Gos, T., Dobrowolny, H., Müller, U., Bogerts, B., Bernstein, H., & Steiner, J. H. (2014) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-014-0562-0 · Cited by 83 · cited 3×
“We included 8 studies which investigated microglial markers in post-mortem brains of patients with MDD (Brisch et al., 2017; Busse et al., 2015; Clark et al., 2016; Foster et al., 2006; Steiner et al., 2011, 2008; Torres-Platas et al., 2014; Wesseling et al., 2014)(Table 4).”
Background
Prefrontal changes in the glutamate-glutamine cycle and neuronal/glial glutamate transporters in depression with and without suicide
Zhao, J., Verwer, R. W. H., van Wamelen, D. J., Qi, X.-R., Gao, S.-F., Lucassen, P. J., & Swaab, D. F. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.06.017 · Cited by 83
Child abuse associates with an imbalance of oligodendrocyte-lineage cells in ventromedial prefrontal white matter
Tanti, A., Kim, J. J., Wakid, M., Davoli, M.-A., Turecki, G., & Mechawar, N. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.231 · Cited by 81
Cerebrospinal fluid interleukin (IL)-6 in unipolar major depression
Carpenter, L. L., Heninger, G. R., Malison, R. T., Tyrka, A. R., & Price, L. H. (2004) · Journal of Affective Disorders · doi:10.1016/s0165-0327(02)00460-3 · Cited by 79 · cited 2×
“9 We included 12 studies which investigated cytokines, chemokines and complement C5 in CSF of MDD patients (Blasko et al., 2006; Boufidou et al., 2009; Carpenter et al., 2004; Hestad et al., 2016; Ishii et al., 2018; Kern et al., 2014; Levine et al., 1999; Lindqvist et al., 2009; Martinez et al., 2012; Palhagen et al.…”
Background
Monoamines, BDNF, IL-6 and corticosterone in CSF in patients with Parkinson’s disease and major depression
Pålhagen, S., Qi, H., Mårtensson, B., Wålinder, J., Granérus, A., & Svenningsson, P. (2009) · Journal of Neurology · doi:10.1007/s00415-009-5353-6 · Cited by 77 · cited 2×
“9 We included 12 studies which investigated cytokines, chemokines and complement C5 in CSF of MDD patients (Blasko et al., 2006; Boufidou et al., 2009; Carpenter et al., 2004; Hestad et al., 2016; Ishii et al., 2018; Kern et al., 2014; Levine et al., 1999; Lindqvist et al., 2009; Martinez et al., 2012; Palhagen et al.…”
BackgroundResult
Neuroinflammatory and morphological changes in late-life depression: the NIMROD study
Su, L., Faluyi, Y. O., Hong, Y. T., Fryer, T. D., Mak, E., Gabel, S., Hayes, L., Soteriades, S., Williams, G. B., Arnold, R. J., et al. (2016) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.116.190165 · Cited by 77
Glial fibrillary acidic protein in late life major depressive disorder: an immunocytochemical study
Davis, S. (2002) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.73.5.556 · Cited by 77 · cited 3×
“, 2002); and only one study showed higher GFAP immunoreactivity in dorsolateral prefrontal cortex in brains of elderly patients with MDD (Davis et al., 2002).”
Background
A quantitative immunohistochemical study of astrocytes in the entorhinal cortex in schizophrenia, bipolar disorder and major depression: absence of significant astrocytosis
Damadzic, R., Bigelow, L. B., Krimer, L. S., Goldenson, D. A., Saunders, R. C., Kleinman, J. E., & Herman, M. M. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00529-9 · Cited by 76 · cited 2×
“, 2006), entorhinal cortex (Damadzic et al., 2001), substantia nigra (Williams et al.”
Background
Astrocyte pathology in the ventral prefrontal white matter in depression
Rajkowska, G., Legutko, B., Moulana, M., Syed, M., Romero, D. G., Stockmeier, C. A., & Miguel-Hidalgo, J. J. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.04.005 · Cited by 70 · cited 5×
“We included 24 studies which assessed astrocytes in postmortem brains of patients with MDD (Altshuler et al., 2010; Barley et al., 2009; Bernard et al., 2011; Chandley et al., 2013; Cobb et al., 2016; Damadzic et al., 2001; Davis et al., 2002; Fatemi et al., 2004; Gos et al., 2013; Miguel-Hidalgo et al., 2014, 2011, 2…”
BackgroundInfluential
Altered Chemokine Levels in the Cerebrospinal Fluid and Plasma of Suicide Attempters
Janelidze, S., Ventorp, F., Erhardt, S., Hansson, O., Minthon, L., Flax, J., Samuelsson, M., Traskman-Bendz, L., & Brundin, L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.09.010 · Cited by 69
Clinical Findings Documenting Cellular and Molecular Abnormalities of Glia in Depressive Disorders
Czéh, B., & Nagy, S. A. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00056 · Cited by 65 · cited 2×
“6 a systematic review and did not present the large amount of inconclusive post-mortem studies on glial markers in patients with MDD and bipolar disorder (Czeh and Nagy, 2018).”
Background
Calprotectin in microglia from frontal cortex is up‐regulated in schizophrenia: evidence for an inflammatory process?
Foster, F., Kandanearatchi, A., Beasley, C. L., Williams, B. P., Khan, N., Fagerhol, M. K., & Everall, I. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05219.x · Cited by 62 · cited 1×
“We included 8 studies which investigated microglial markers in post-mortem brains of patients with MDD (Brisch et al., 2017; Busse et al., 2015; Clark et al., 2016; Foster et al., 2006; Steiner et al., 2011, 2008; Torres-Platas et al., 2014; Wesseling et al., 2014)(Table 4).”
Background
Microglia in the dorsal raphe nucleus plays a potential role in both suicide facilitation and prevention in affective disorders
Brisch, R., Steiner, J., Mawrin, C., Krzyżanowska, M., Jankowski, Z., & Gos, T. (2017) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-017-0774-1 · Cited by 60 · cited 3×
“We included 8 studies which investigated microglial markers in post-mortem brains of patients with MDD (Brisch et al., 2017; Busse et al., 2015; Clark et al., 2016; Foster et al., 2006; Steiner et al., 2011, 2008; Torres-Platas et al., 2014; Wesseling et al., 2014)(Table 4).”
Background
Interleukin-6 and the soluble IL-6 receptor are decreased in cerebrospinal fluid of geriatric patients with major depression: no alteration of soluble gp130
Stübner, S., Schön, T., Padberg, F., Teipel, S. J., Schwarz, M. J., Haslinger, A., Buch, K., Dukoff, R., Lasser, R., Müller, N., et al. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00916-1 · Cited by 59
Targeted Multiplexed Selected Reaction Monitoring Analysis Evaluates Protein Expression Changes of Molecular Risk Factors for Major Psychiatric Disorders
Wesseling, H., Gottschalk, M. G., & Bahn, S. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu015 · Cited by 54 · cited 4×
“We included 8 studies which investigated microglial markers in post-mortem brains of patients with MDD (Brisch et al., 2017; Busse et al., 2015; Clark et al., 2016; Foster et al., 2006; Steiner et al., 2011, 2008; Torres-Platas et al., 2014; Wesseling et al., 2014)(Table 4).”
BackgroundResultInfluential
Increased cerebrospinal fluid complement C5 levels in major depressive disorder and schizophrenia
Ishii, T., Hattori, K., Miyakawa, T., Watanabe, K., Hidese, S., Sasayama, D., Ota, M., Teraishi, T., Hori, H., Yoshida, S., et al. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.02.131 · Cited by 53 · cited 1×
“9 We included 12 studies which investigated cytokines, chemokines and complement C5 in CSF of MDD patients (Blasko et al., 2006; Boufidou et al., 2009; Carpenter et al., 2004; Hestad et al., 2016; Ishii et al., 2018; Kern et al., 2014; Levine et al., 1999; Lindqvist et al., 2009; Martinez et al., 2012; Palhagen et al.…”
Background
A novel, rapid, quantitative cell-counting method reveals oligodendroglial reduction in the frontopolar cortex in major depressive disorder
Hayashi, Y., Nihonmatsu-Kikuchi, N., Yu, X., Ishimoto, K., Hisanaga, S.-I., & Tatebayashi, Y. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.84 · Cited by 52 · cited 3×
“, 2007), and in the frontopolar prefrontal cortex (BA 10) (Hayashi et al., 2011) .”
Background
Neuropathological changes in the substantia nigra in schizophrenia but not depression
Williams, M. R., Galvin, K., OSullivan, B., Macdonald, C., Ching, E. W.-K., Turkheimer, F., Howes, O. D., Pearce, R. K. B., Hirsch, S. R., & Maier, M. (2013) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-013-0479-z · Cited by 52 · cited 4×
“We included 12 studies which measured oligodendrocytes in post-mortem MDD brains (Aston et al., 2005; Barley et al., 2009; Gos et al., 2013; Hayashi et al., 2011; Honer et al., 1999; Lutz et al., 2017; Miguel-Hidalgo et al., 2017; Rajkowska et al., 2015; Tanti et al., 2018; Uranova et al., 2004; Vostrikov et al., 2007…”
BackgroundInfluential
Concomitant interferon alpha stimulation and TLR3 activation induces neuronal expression of depression-related genes that are elevated in the brain of suicidal persons
Hoyo-Becerra, C., Huebener, A., Trippler, M., Lutterbeck, M., Liu, Z. J., Truebner, K., Bajanowski, T., Gerken, G., Hermann, D. M., & Schlaak, J. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083149 · Cited by 49 · cited 2×
“Although IL-6 mRNA was no different between depressed and controls subjects, IL-6 mRNA has been reported to be increased in suicide victims (Hoyo-Becerra et al., 2013; Pandey et al., 2012).”
Background
MicroRNA-21: Expression in oligodendrocytes and correlation with low myelin mRNAs in depression and alcoholism
Miguel-Hidalgo, J. J., Hall, K. O., Bonner, H., Roller, A., Syed, M., Park, C. J., Ball, J. P., Rothenberg, M. E., Stockmeier, C. A., & Romero, D. G. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.08.009 · Cited by 47
Patients with depression display cytokine levels in serum and cerebrospinal fluid similar to patients with diffuse neurological symptoms without a defined diagnosis
Hestad, K. A., Engedal, K., Whist, J. E., Aukrust, P., Farup, P. G., Mollnes, T. E., & Ueland, T. (2016) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s101925 · Cited by 42 · cited 10×
“A recent meta-analysis focused specifically on CSF cytokines in patients with MDD, schizophrenia and bipolar disorder, and found increased CSF levels of IL-6 and IL8 in these patients (Wang and Miller, 2018); however, this systematic review and metaanalysis did not include two previous studies, which focused exclusive…”
BackgroundResultInfluential
Glucocorticoid programming of neuroimmune function
Walker, D. J., & Spencer, K. A. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.07.016 · Cited by 42
Vascular and extravascular immunoreactivity for intercellular adhesion molecule 1 in the orbitofrontal cortex of subjects with major depression: Age-dependent changes
Miguel-Hidalgo, J. J., Overholser, J. C., Jurjus, G., Meltzer, H. Y., Dieter, L., Konick, L. C., Stockmeier, C. A., & Rajkowska, G. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.03.052 · Cited by 34

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2 of the 97 references couldn’t be matched to a known paper.

Sorted by citations

COVID-19 pandemic and mental health consequences: Systematic review of the current evidence
Vindegaard, N., & Benros, M. E. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.05.048 · Cited by 3,221
The Bidirectional Relationship of Depression and Inflammation: Double Trouble
Beurel, E., Toups, M., & Nemeroff, C. B. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.002 · Cited by 2,136
“Furthermore, a recent meta-analysis suggests increased microglial activity is associated with increased IL-6, IL-8, and TNF levels in CSF and brain parenchyma of MDD patients (Wang and Miller, 2018) and reduced astrocytes and oligodendrocytes numbers in MDD patients (Enache et al., 2019).”
Background
Major depressive disorder
Marx, W., Penninx, B. W. J. H., Solmi, M., Furukawa, T. A., Firth, J., Carvalho, A. F., & Berk, M. (2023) · Nature Reviews Disease Primers · doi:10.1038/s41572-023-00454-1 · Cited by 910
Comorbid depression in medical diseases
Gold, S. M., Köhler‐Forsberg, O., Moss-Morris, R. E., Mehnert-Theuerkauf, A., Miranda, J. J., Bullinger, M., Steptoe, A., Whooley, M. A., & Otte, C. (2020) · Nature Reviews Disease Primers · doi:10.1038/s41572-020-0200-2 · Cited by 583
Persistent psychopathology and neurocognitive impairment in COVID-19 survivors: effect of inflammatory biomarkers at three-month follow-up
Mazza, M. G., Palladini, M., De Lorenzo, R., Magnaghi, C., Poletti, S., Furlan, R., Ciceri, F., Rovere-Querini, P., & Benedetti, F. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2021.02.021 · Cited by 513
“Depressed patients are characterized by higher levels of cytokines when compared to healthy controls with consistent results in literature when considering IL-1β, IL6, IL-10, CCL2, TNF-α, and transforming growth factor-β (TGF-β) (Enache et al., 2019; Eyre et al., 2016; Howren et al., 2009; Kohler et al., 2017; Poletti…”

See all 615

Authors: Enache, D., Pariante, C. M., & Mondelli, V.
Affiliations: King's College London (GB)
National Health Service (GB)
Corresponding author: Mondelli, Valeria
ORCID: Enache, Daniela
Pariante, Carmine M.
Mondelli, Valeria
Venue: Brain, Behavior, and Immunity
Publisher: Elsevier BV
Published: 2019-10
Volume: 81
Pages: 24-40
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2019.06.015
OpenAlex: W2953025937
Semantic Scholar: 83e5363ffd00c2dba7a412e43a5a292f085d67ed
Cited by: 615
References: 97
Citations by year: 2026: 54 · 2025: 74 · 2024: 160 · 2023: 91 · 2022: 86 · 2021: 87 · 2020: 52 · 2019: 11
FWCI: 3.71
Type: journal article
Language: en
Open access: green
kclpure.kcl.ac.uk
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion, cc-by-nc-nd)
Funders: GlaxoSmithKline foundation
South London and Maudsley NHS Foundation Trust
Kingâs College London
Svenska LÃ¤karesÃ¤llskapet (MQBF1)
National Institute for Health Research
Medical Research Foundation (MRF-160-0005)
H. Lundbeck A/S
Wellcome Trust
Medical Research Council
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Health Sciences › Medicine › Pharmacology (medical) › Treatment of Major Depression
Keywords: major depressive disorder, neuroinflammation, cerebrospinal fluid cytokines, interleukin-6, TNF-α, translocator protein (TSPO), positron emission tomography, microglia, astrocytes, oligodendrocytes, suicide attempters, postmortem brain, peripheral inflammation, prefrontal cortex, anterior cingulate cortex
MeSH terms: Astrocytes, Autopsy, Brain, Major Depressive Disorder, Female, Humans, Inflammation, Male, Oligodendroglia, Tumor Necrosis Factor-alpha, Biomarkers, Interleukin-6, Cytokines, Prefrontal Cortex, Microglia, Receptors, GABA, Chemokines, Positron-Emission Tomography

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Markers of central inflammation in major depressive disorder: A systematic review and meta-analysis of studies examining cerebrospinal fluid, positron emission tomography and post-mortem brain tissue

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