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Open Access 01-02-2017 | Psychiatry and Preclinical Psychiatric Studies − Review Article

Sleep and inflammatory markers in different psychiatric disorders

Authors: Krzysztof Krysta, Marek Krzystanek, Agnieszka Bratek, Irena Krupka-Matuszczyk

Published in: Journal of Neural Transmission | Special Issue 1/2017

Abstract

Many psychiatric disorders, like schizophrenia, affective disorders, addictions and different forms of dementia are associated with sleep disturbances. In the etiology and course of those diseases inflammatory processes are regarded to be an increasingly important factor. They are also a frequently discussed element of the pathology of sleep. In this literature review reports on correlations between poor sleep and inflammatory responses in various psychiatric conditions are discussed. The link between schizophrenia, affective disorders and inflammatory cytokines is a complex phenomenon, which has been already confirmed in a number of studies. However, the presence of sleep deficits in those conditions, being a common symptom of depression and psychoses, can be an additional factor having a considerable impact on the immunological processes in mental illnesses. In the analyzed data, a number of studies are presented describing the role of inflammatory markers in sleep disturbances and psychopathological symptoms of affective, psychotic, neurogenerative and other disorders. Also attention is drawn to possible implications for their treatment. Efforts to use, e.g., anti-inflammatory agents in psychiatry in the context of their impact on sleep are reported. The aspect of inflammatory markers in the role of sleep deprivation as the treatment method in major depressive disorder is also discussed. A general conclusion is drawn that the improvement of sleep quality plays a crucial role in the care for psychiatric patients.

Afonso P, Brissos S, Figueira ML, Paiva T (2010) Discrepant nocturnal melatonin levels in monozygotic twins discordant for schizophrenia and its impact on sleep. Schizophr Res 120:227–228CrossRefPubMed

Ali T, Orr WC (2014) Sleep disturbances and inflammatory bowel disease. Inflamm Bowel Dis 20:1986–1995CrossRefPubMed

Anderson G, Maes M (2012) Melatonin: an overlooked factor in schizophrenia and in the inhibition of anti-psychotic side effects. Metab Brain Dis 27:113–119CrossRefPubMed

Appelberg B, Katila H, Rimon R (1997) Plasma interleukin-1 beta and sleep architecture in schizophrenia and other nonaffective psychoses. Psychosom Med 59:529–532CrossRefPubMed

Berk M, Dean O, Drexhage H, McNeil JJ, Moylan S, O’Neil A, Davey CG, Sanna L, Maes M (2013) Aspirin: a review of its neurobiological properties and therapeutic potential for mental illness. BMC Med 11:74CrossRefPubMedPubMedCentral

Bersani G, Mameli M, Garavini A, Pancheri P, Nordio M (2003) Reduction of night/day difference in melatonin blood levels as a possible disease-related index in schizophrenia. Neuro Endocrinol Lett 24:181–184PubMed

Besedovsky HO, del Rey A, Sorkin E, DaPrada M, Burri R, Honegger C (1983) The immune response evokes changes in brain noradrenergic neurons. Science 221:564–566CrossRefPubMed

Boakye PA, Olechowski C, Rashiq S, Verrier MJ, Kerr B, Witmans M, Baker G, Joyce A, Dick BD (2015) A critical review of neurobiological factors involved in the interactions between chronic pain, depression, and sleep disruption. Clin J Pain. doi:10.1097/ajp.0000000000000260

Brown AS, Derkits EJ (2010) Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 167:261–280CrossRefPubMedPubMedCentral

Buysse DJ, Angst J, Gamma A, Ajdacic V, Eich D, Rossler W (2008) Prevalence, course, and comorbidity of insomnia and depression in young adults. Sleep 31:473–480PubMedPubMedCentral

Cazzullo CL, Scarone S, Grassi B, Vismara C, Trabattoni D, Clerici M (1998) Cytokines production in chronic schizophrenia patients with or without paranoid behaviour. Prog Neuropsychopharmacol Biol Psychiatry 22:947–957CrossRefPubMed

Chaudhry IB, Hallak J, Husain N, Minhas F, Stirling J, Richardson P, Dursun S, Dunn G, Deakin B (2012) Minocycline benefits negative symptoms in early schizophrenia: a randomised double-blind placebo-controlled clinical trial in patients on standard treatment. J Psychopharmacol 26:1185–1193CrossRefPubMed

Chen R, Yin Y, Zhao Z, Huang L, Huang S, Zhuang J, Wu H, Peng H, Li P (2012) Elevation of serum TNF-alpha levels in mild and moderate Alzheimer patients with daytime sleepiness. J Neuroimmunol 244:97–102CrossRefPubMed

Cohen S, Doyle WJ, Alper CM, Janicki-Deverts D, Turner RB (2009) Sleep habits and susceptibility to the common cold. Arch Intern Med 169:62–67CrossRefPubMedPubMedCentral

Cohrs S (2008) Sleep disturbances in patients with schizophrenia: impact and effect of antipsychotics. CNS Drugs 22:939–962CrossRefPubMed

Dameshek W (1930) White blood cells in dementia praecox and dementia paralytietwa. Arch Neurol Psychiatry 24:855

Dean OM, Data-Franco J, Giorlando F, Berk M (2012) Minocycline: therapeutic potential in psychiatry. CNS Drugs 26:391–401CrossRefPubMed

Drexhage RC, Knijff EM, Padmos RC, Heul-Nieuwenhuijzen L, Beumer W, Versnel MA, Drexhage HA (2010) The mononuclear phagocyte system and its cytokine inflammatory networks in schizophrenia and bipolar disorder. Expert Rev Neurother 10:59–76CrossRefPubMed

Ehlers CL, Reed TK, Henriksen SJ (1986) Effects of corticotropin-releasing factor and growth hormone-releasing factor on sleep and activity in rats. Neuroendocrinology 42:467–474CrossRefPubMed

Esposito E, Cuzzocrea S (2010) Antiinflammatory activity of melatonin in central nervous system. Curr Neuropharmacol 8:228–242CrossRefPubMedPubMedCentral

Fernstrom JD, Faller DV (1978) Neutral amino acids in the brain: changes in response to food ingestion. J Neurochem 30:1531–1538CrossRefPubMed

Fillman SG, Weickert TW, Lenroot RK, Catts SV, Bruggemann JM, Catts VS, Weickert CS (2015) Elevated peripheral cytokines characterize a subgroup of people with schizophrenia displaying poor verbal fluency and reduced Broca’s area volume. Mol Psychiatry. doi:10.1038/mp.2015.90 PubMedPubMedCentral

Fond G, Girerd N, Clavel F, Tamouza R, Leboyer M (2014) Recently discovered properties of aspirin may be doubly helpful in bipolar disorders. Med Hypotheses 82:640–641CrossRefPubMed

Hayaishi O (1991) Molecular mechanisms of sleep-wake regulation; roles of prostaglandins D2 and E2. FASEB J 5:2575–2581PubMed

Heffner KL, France CR, Trost Z, Ng HM, Pigeon WR (2011) Chronic low back pain, sleep disturbance, and interleukin-6. Clin J Pain 27:35–41CrossRefPubMedPubMedCentral

Heffner KL, Ng HM, Suhr JA, France CR, Marshall GD, Pigeon WR, Moynihan JA (2012) Sleep disturbance and older adults’ inflammatory responses to acute stress. Am J Geriatr Psychiatry 20:744–752CrossRefPubMedPubMedCentral

Howren MB, Lamkin DM, Suls J (2009) Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med 71:171–186CrossRefPubMed

Illi J, Miaskowski C, Cooper B, Levine JD, Dunn L, West C, Dodd M, Dhruva A, Paul SM, Baggott C, Cataldo J, Langford D, Schmidt B, Aouizerat BE (2012) Association between pro- and anti-inflammatory cytokine genes and a symptom cluster of pain, fatigue, sleep disturbance, and depression. Cytokine 58:437–447CrossRefPubMedPubMedCentral

Irwin M (2002) Effects of sleep and sleep loss on immunity and cytokines. Brain Behav Immun 16:503–512CrossRefPubMed

Irwin M, Rinetti G, Redwine L, Motivala S, Dang J, Ehlers C (2004) Nocturnal proinflammatory cytokine-associated sleep disturbances in abstinent African American alcoholics. Brain Behav Immun 18:349–360CrossRefPubMed

Irwin MR, Wang M, Campomayor CO, Collado-Hidalgo A, Cole S (2006) Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch Intern Med 166:1756–1762CrossRefPubMed

Jhamnani K, Shivakumar V, Kalmady S, Rao NP, Venkatasubramanian G (2013) Successful use of add-on minocycline for treatment of persistent negative symptoms in schizophrenia. J Neuropsychiatry Clin Neurosci 25:E06–E07CrossRefPubMed

Kang WS, Park HJ, Chung JH, Kim JW (2013) REM sleep deprivation increases the expression of interleukin genes in mice hypothalamus. Neurosci Lett 556:73–78CrossRefPubMed

Kapsimalis F, Richardson G, Opp MR, Kryger M (2005) Cytokines and normal sleep. Curr Opin Pulm Med 11:481–484CrossRefPubMed

Khandaker GM, Pearson RM, Zammit S, Lewis G, Jones PB (2014) Association of serum interleukin 6 and C-reactive protein in childhood with depression and psychosis in young adult life: a population-based longitudinal study. JAMA Psychiatry 71:1121–1128CrossRefPubMedPubMedCentral

Krueger JM (2008) The role of cytokines in sleep regulation. Curr Pharm Des 14:3408–3416CrossRefPubMedPubMedCentral

Krueger JM, Clinton JM, Winters BD, Zielinski MR, Taishi P, Jewett KA, Davis CJ (2011) Involvement of cytokines in slow wave sleep. Prog Brain Res 193:39–47CrossRefPubMedPubMedCentral

Kunz M, Cereser KM, Goi PD, Fries GR, Teixeira AL, Fernande BS, Belmonte-de-Abreu PS, Kauer-Sant’Anna M, Kapczinski F, Gama CS (2011) Serum levels of IL-6, IL-10 and TNF-alpha in patients with bipolar disorder and schizophrenia: differences in pro- and anti-inflammatory balance. Rev Bras Psiquiatr 33:268–274CrossRefPubMed

Lotrich FE (2015) Inflammatory cytokine-associated depression. Brain Res 1617:113–125CrossRefPubMed

Maes M, Bosmans E, Meltzer HY (1995) Immunoendocrine aspects of major depression. Relationships between plasma interleukin-6 and soluble interleukin-2 receptor, prolactin and cortisol. Eur Arch Psychiatry Clin Neurosci 245:172–178CrossRefPubMed

Maldonado MD, Pérez-San-Gregorio MA, Reiter RJ (2009) The role of melatonin in the immuno-neuro-psychology of mental disorders. Recent Pat CNS Drug Discov 4:61–69CrossRefPubMed

Matsumura H, Nakajiima T, Osaka T, Satoh S, Kawase K, Kubo E, Kantha SS, Kasahara K, Hayaishi O (1994) Prostaglandin D2-sensitive, sleep-promoting zone defined in the ventral surface of the rostral basal forebrain. Proc Natl Acad Sci USA 91:11998–20002CrossRefPubMedPubMedCentral

Meier-Ewert HK, Ridker PM, Rifai N, Regan MM, Price NJ, Dinges DF, Mullington JM (2004) Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. J Am Coll Cardiol 43:678–683CrossRefPubMed

Merill JE (1992) Tumor necrosis factor alpha, Interleukin 1 and related cytokines in brain development: normal and pathological. Dev Neurosci 14:l–10

Meyer U, Feldon J, Dammann O (2011) Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res 69:26–33CrossRef

Miller BJ, Buckley P, Seabolt W, Mellor A, Kirkpatrick B (2011) Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol Psychiatry 70:663–671CrossRefPubMedPubMedCentral

Mills PJ, Ancoli-Israel S, von Kanel R, Mausbach BT, Aschbacher K, Patterson TL, Ziegler MG, Dimsdale JE, Grant I (2009) Effects of gender and dementia severity on Alzheimer’s disease caregivers’ sleep and biomarkers of coagulation and inflammation. Brain Behav Immun 23:605–610CrossRefPubMed

Miyaoka T, Wake R, Furuya M, Liaury K, Ieda M, Kawakami K, Tsuchie K, Taki M, Ishihara K, Araki T, Horiguchi J (2012) Minocycline as adjunctive therapy for patients with unipolar psychotic depression: an open-label study. Prog Neuropsychopharmacol Biol Psychiatry 37:222–226CrossRefPubMed

Moller-Levet CS, Archer SN, Bucca G, Laing EE, Slak A, Kabiljo R, Lo JC, Santhi N, von Schantz M, Smith CP, Dijk DJ (2013) Effects of insufficient sleep on circadian rhythmicity and expression amplitude of the human blood transcriptome. Proc Natl Acad Sci USA 110:E1132–E1141CrossRefPubMedPubMedCentral

Monteleone P, Maj M, Fusco M, Kemali D, Reiter RJ (1992) Depressed nocturnal plasma melatonin levels in drug-free paranoid schizophrenics. Schizophr Res 7:77–84CrossRefPubMed

Monteleone P, Natale M, La Rocca A, Maj M (1997) Decreased nocturnal secretion of melatonin in drug-free schizophrenics: no change after subchronic treatment with antipsychotics. Neuropsychobiology 36:159–163CrossRefPubMed

Monti JM, BaHammam AS, Pandi-Perumal SR, Bromundt V, Spence DW, Cardinali DP, Brown GM (2013) Sleep and circadian rhythm dysregulation in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 43:209–216CrossRefPubMed

Motivala SJ (2011) Sleep and inflammation: psychoneuroimmunology in the context of cardiovascular disease. Ann Behav Med 42:141–152CrossRefPubMed

Motivala SJ, Sarfatti A, Olmos L, Irwin MR (2005) Inflammatory markers and sleep disturbance in major depression. Psychosom Med 67:187–194CrossRefPubMed

Nishino S, Mignot E, Benson KL, Zarcone VP Jr (1998) Cerebrospinal fluid prostaglandins and corticotropin releasing factor in schizophrenics and controls: relationship to sleep architecture. Psychiatry Res 78:141–150CrossRefPubMed

Noto C, Maes M, Ota VK, Teixeira AL, Bressan RA, Gadelha A, Brietzke E (2015) High predictive value of immune-inflammatory biomarkers for schizophrenia diagnosis and association with treatment resistance. World J Biol Psychiatry. doi:10.3109/15622975.2015.1062552

Opp M, Obal F, Krueger JM (1989) Corticotropin-releasing factor attenuates interleukin 1-induced sleep and fever in rabbits. Am J Physiol 257:528–535

Petrikis P, Voulgari PV, Tzallas AT, Archimandriti DT, Skapinakis P, Mavreas V (2015) Cytokine profile in drug-naive, first episode patients with psychosis. J Psychosom Res. doi:10.1016/j.jpsychores.2015.06.011 PubMed

Porkka-Heiskanen T, Zitting KM, Wigren HK (2013) Sleep, its regulation and possible mechanisms of sleep disturbances. Acta Physiol (Oxf) 208:311–328CrossRef

Potvin S, Stip E, Sepehry AA, Gendron A, Bah R, Kouassi E (2008) Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biol Psychiatry 63:801–808CrossRefPubMed

Prather AA, Rabinovitz M, Pollock BG, Lotrich FE (2009) Cytokine-induced depression during IFN-alpha treatment: the role of IL-6 and sleep quality. Brain Behav Immun 23:1109–1116CrossRefPubMedPubMedCentral

Redwine L, Dang J, Hall M, Irwin M (2003) Disordered sleep, nocturnal cytokines, and immunity in alcoholics. Psychosom Med 65:75–85CrossRefPubMed

Ritter PS, Kretschmer K, Pfennig A, Soltmann B (2013) Disturbed sleep in bipolar disorder is related to an elevation of IL-6 in peripheral monocytes. Med Hypotheses 81:1031–1033CrossRefPubMed

Savitz J, Preskorn S, Teague TK, Drevets D, Yates W, Drevets W (2012) Minocycline and aspirin in the treatment of bipolar depression: a protocol for a proof-of-concept, randomised, double-blind, placebo-controlled, 2 × 2 clinical trial. BMJ Open 22(2):e000643CrossRef

Shi J, Levinson DF, Duan J, Sanders AR, Zheng Y, Pe’er I, Dudbridge F, Holmans PA et al (2009) Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460:753–757PubMedPubMedCentral

Vgontzas AN, Zoumakis E, Bixler EO, Lin HM, Follett H, Kales A, Chrousos GP (2004) Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines. J Clin Endocrinol Metab 89:2119–2126CrossRefPubMed

Voderholzer U, Fiebich BL, Dersch R, Feige B, Piosczyk H, Kopasz M, Riemann D, Lieb K (2012) Effects of sleep deprivation on nocturnal cytokine concentrations in depressed patients and healthy control subjects. J Neuropsychiatry Clin Neurosci 24:354–366CrossRefPubMed

von Kanel R, Dimsdale JE, Ancoli-Israel S, Mills PJ, Patterson TL, McKibbin CL, Archuleta C, Grant I (2006) Poor sleep is associated with higher plasma proinflammatory cytokine interleukin-6 and procoagulant marker fibrin D-dimer in older caregivers of people with Alzheimer’s disease. J Am Geriatr Soc 54:431–437CrossRef

Weschenfelder J, Sander C, Kluge M, Kirkby KC, Himmerich H (2012) The influence of cytokines on wakefulness regulation: clinical relevance, mechanisms and methodological problems. Psychiatr Danub 24:112–126PubMed

Wichniak A, Jarema M (2012) Cytokines, sleep and wakefulness regulation, and general health: a commentary to the review “The influence of cytokines on wakefulness regulation”. Psychiatr Danub 24:127–129PubMed

Wisor JP, Schmidt MA, Clegern WC (2011) Evidence for neuroinflammatory and microglial changes in the cerebral response to sleep loss. Sleep 34(3):261–272PubMedPubMedCentral

Wulff K, Dijk DJ, Middleton B, Foster RG, Joyce EM (2012) Sleep and circadian rhythm disruption in schizophrenia. Br J Psychiatry 200:308–316CrossRefPubMedPubMedCentral

Xiu MH, Lin CG, Tian L, Tan YL, Chen J, Chen S, Tan SP, Wang ZR, Yang F, Chen DC, Zhang XY (2015) Increased IL-3 serum levels in chronic patients with schizophrenia: associated with psychopathology. Psychiatry Res. doi:10.1016/j.psychres.2015.07.029 PubMed

Zeitzer JM (2013) Control of sleep and wakefulness in health and disease. Prog Mol Biol Transl Sci 119:137–154CrossRefPubMed

Zhu B, Dong Y, Xu Z, Gompf HS, Ward SA, Xue Z, Miao C, Zhang Y, Chamberlin NL, Xie Z (2012) Sleep disturbance induces neuroinflammation and impairment of learning and memory. Neurobiol Dis 48:348–355CrossRefPubMedPubMedCentral

Zielinski MR, Kim Y, Karpova SA, McCarley RW, Strecker RE, Gerashchenko D (2014) Chronic sleep restriction elevates brain interleukin-1 beta and tumor necrosis factor-alpha and attenuates brain-derived neurotrophic factor expression. Neurosci Lett 580c:27–31CrossRef

Title: Sleep and inflammatory markers in different psychiatric disorders
Authors: Krzysztof Krysta
Marek Krzystanek
Agnieszka Bratek
Irena Krupka-Matuszczyk
Publication date: 01-02-2017
Publisher: Springer Vienna
Published in: Journal of Neural Transmission / Issue Special Issue 1/2017
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-015-1492-3

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Sleep and inflammatory markers in different psychiatric disorders

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