Sick for science: experimental endotoxemia as a translational tool to develop and test new therapies for inflammation-associated depression.


Journal

Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835

Informations de publication

Date de publication:
08 2021
Historique:
received: 03 04 2019
accepted: 06 08 2020
revised: 25 07 2020
pubmed: 3 9 2020
medline: 28 1 2022
entrez: 3 9 2020
Statut: ppublish

Résumé

Depression is one of the global leading causes of disability, but treatments remain limited and classical antidepressants were found to be ineffective in a substantial proportion of patients. Thus, novel effective therapies for the treatment of depression are urgently needed. Given the emerging role of inflammation in the etiology and pathophysiology of affective disorders, we herein illustrate how experimental endotoxemia, a translational model of systemic inflammation, could be used as a tool to develop and test new therapeutic options against depression. Our concept is based on the striking overlap of inflammatory, neural, and affective characteristics in patients with inflammation-associated depression and in endotoxin-challenged healthy subjects. Experimental administration of endotoxin in healthy volunteers is safe, well-tolerated, and without known long-term health risks. It offers a highly standardized translational approach to characterize potential targets of therapies against inflammation-associated depression, as well as to identify characteristics of patients that would benefit from these interventions, and, therefore, could contribute to improve personalization of treatment and to increase the overall rate of responders.

Identifiants

pubmed: 32873895
doi: 10.1038/s41380-020-00869-2
pii: 10.1038/s41380-020-00869-2
pmc: PMC8550942
doi:

Substances chimiques

Endotoxins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

3672-3683

Informations de copyright

© 2020. The Author(s).

Références

WHO. Depression and other common mental disorders: global health estimates. WHO; 2017.
Rush AJ, Trivedi MH, Wisniewski SR, Nierenberg AA, Stewart JW, Warden D, et al. Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: a STAR*D report. Am J Psychiatry. 2006;163:1905–17.
pubmed: 17074942
Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9:46–56.
pubmed: 18073775 pmcid: 2919277
Miller AH, Raison CL. The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat Rev Immunol. 2016;16:22–34.
pubmed: 26711676 pmcid: 5542678
Yirmiya R, Rimmerman N, Reshef R. Depression as a microglial disease. Trends Neurosci. 2015;38:637–58.
pubmed: 26442697
Bell JA, Kivimaki M, Bullmore ET, Steptoe A, Carvalho LA, MRC ImmunoPsychiatry Consortium. Repeated exposure to systemic inflammation and risk of new depressive symptoms among older adults. Transl Psychiatry. 2017;7:e1208.
pubmed: 28809860 pmcid: 5611724
Khandaker GM, Pearson RM, Zammit S, Lewis G, Jones PB. 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. 2014;71:1121–8.
pubmed: 25133871 pmcid: 4561502
Dantzer R, O’Connor JC, Lawson MA, Kelley KW. Inflammation-associated depression: from serotonin to kynurenine. Psychoneuroendocrinology. 2011;36:426–36.
pubmed: 21041030
Lotrich FE. Inflammatory cytokine-associated depression. Brain Res. 2015;1617:113–25.
pubmed: 25003554
Wium-Andersen MK, Orsted DD, Nielsen SF, Nordestgaard BG. Elevated C-reactive protein levels, psychological distress, and depression in 73, 131 individuals. JAMA Psychiatry. 2013;70:176–84.
pubmed: 23266538
Osimo EF, Cardinal RN, Jones PB, Khandaker GM. Prevalence and correlates of low-grade systemic inflammation in adult psychiatric inpatients: an electronic health record-based study. Psychoneuroendocrinology. 2018;91:226–34.
pubmed: 29544672 pmcid: 5910056
Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, et al. A meta-analysis of cytokines in major depression. Biol Psychiatry. 2010;67:446–57.
pubmed: 20015486
Chamberlain SR, Cavanagh J, de Boer P, Mondelli V, Jones DNC, Drevets WC, et al. Treatment-resistant depression and peripheral C-reactive protein. Br J Psychiatry. 2019;214:11–19.
pubmed: 29764522 pmcid: 6124647
Haroon E, Daguanno AW, Woolwine BJ, Goldsmith DR, Baer WM, Wommack EC, et al. Antidepressant treatment resistance is associated with increased inflammatory markers in patients with major depressive disorder. Psychoneuroendocrinology. 2018;95:43–9.
pubmed: 29800779 pmcid: 6427066
Beutler B. TLR4 as the mammalian endotoxin sensor. Curr Top Microbiol. 2002;270:109–20.
Engler H, Brendt P, Wischermann J, Wegner A, Rohling R, Schoemberg T, et al. Selective increase of cerebrospinal fluid IL-6 during experimental systemic inflammation in humans: association with depressive symptoms. Mol Psychiatry. 2017;22:1448–54.
pubmed: 28138158
Leighton SP, Nerurkar L, Krishnadas R, Johnman C, Graham GJ, Cavanagh J. Chemokines in depression in health and in inflammatory illness: a systematic review and meta-analysis. Mol Psychiatry. 2018;23:48–58.
pubmed: 29133955
Felger JC, Haroon E, Patel TA, Goldsmith DR, Wommack EC, Woolwine BJ, et al. What does plasma CRP tell us about peripheral and central inflammation in depression? Mol Psychiatry. 2020;25:1301–11.
D’Mello C, Swain MG. Immune-to-brain communication pathways in inflammation-associated sickness and depression. Curr Top Behav Neurosci. 2017;31:73–94.
pubmed: 27677781
Felger JC. The role of dopamine in inflammation-associated depression: mechanisms and therapeutic implications. Curr Top Behav Neurosci. 2017;31:199–219.
pubmed: 27225499
Dantzer R. Role of the kynurenine metabolism pathway in inflammation-induced depression: preclinical approaches. Curr Top Behav Neurosci. 2017;31:117–38.
pubmed: 27225497 pmcid: 6585430
Harrison NA. Brain structures implicated in inflammation-associated depression. Curr Top Behav Neurosci. 2017;31:221–48.
pubmed: 27272069
Dooley LN, Kuhlman KR, Robles TF, Eisenberger NI, Craske MG, Bower JE. The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. Neurosci Biobehav Rev. 2018;94:219–37.
pubmed: 30201219 pmcid: 6192535
Hart BL. Biological basis of the behavior of sick animals. Neurosci Biobehav Rev. 1988;12:123–37.
pubmed: 3050629
Frenois F, Moreau M, O’Connor J, Lawson M, Micon C, Lestage J, et al. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology. 2007;32:516–31.
pubmed: 17482371 pmcid: 1978247
Vichaya EG, Hunt SC, Dantzer R. Lipopolysaccharide reduces incentive motivation while boosting preference for high reward in mice. Neuropsychopharmacology. 2014;39:2884–90.
pubmed: 24917202 pmcid: 4200499
Reichenberg A, Yirmiya R, Schuld A, Kraus T, Haack M, Morag A, et al. Cytokine-associated emotional and cognitive disturbances in humans. Arch Gen Psychiatry. 2001;58:445–52.
pubmed: 11343523
Grigoleit JS, Kullmann JS, Wolf OT, Hammes F, Wegner A, Jablonowski S, et al. Dose-dependent effects of endotoxin on neurobehavioral functions in humans. PLoS ONE. 2011;6:e28330.
pubmed: 22164271 pmcid: 3229570
DellaGioia N, Devine L, Pittman B, Hannestad J. Bupropion pre-treatment of endotoxin-induced depressive symptoms. Brain Behav Immun. 2013;31:197–204.
pubmed: 23064079
Eisenberger NI, Berkman ET, Inagaki TK, Rameson LT, Mashal NM, Irwin MR. Inflammation-induced anhedonia: endotoxin reduces ventral striatum responses to reward. Biol Psychiatry. 2010;68:748–54.
pubmed: 20719303 pmcid: 3025604
Lasselin J, Elsenbruch S, Lekander M, Axelsson J, Karshikoff B, Grigoleit JS, et al. Mood disturbance during experimental endotoxemia: predictors of state anxiety as a psychological component of sickness behavior. Brain Behav Immun. 2016;57:30–7.
pubmed: 26790758
Sandiego CM, Gallezot JD, Pittman B, Nabulsi N, Lim K, Lin SF, et al. Imaging robust microglial activation after lipopolysaccharide administration in humans with PET. Proc Natl Acad Sci USA. 2015;112:12468–73.
pubmed: 26385967 pmcid: 4603509
Hannestad J, Subramanyam K, Dellagioia N, Planeta-Wilson B, Weinzimmer D, Pittman B, et al. Glucose metabolism in the insula and cingulate is affected by systemic inflammation in humans. J Nucl Med. 2012;53:601–7.
pubmed: 22414635
Eisenberger NI, Inagaki TK, Mashal NM, Irwin MR. Inflammation and social experience: an inflammatory challenge induces feelings of social disconnection in addition to depressed mood. Brain Behav Immun. 2010;24:558–63.
pubmed: 20043983 pmcid: 2856755
Hermann DM, Mullington J, Hinze-Selch D, Schreiber W, Galanos C, Pollmacher T. Endotoxin-induced changes in sleep and sleepiness during the day. Psychoneuroendocrinology. 1998;23:427–37.
pubmed: 9802118
Marraffa A, Lekander M, Solsjo P, Olsson MJ, Lasselin J, Axelsson J. Yawning, a thermoregulatory mechanism during fever? A study of yawning frequency and its predictors during experimentally induced sickness. Physiol Behav. 2017;182:27–33.
pubmed: 28939427
Reichenberg A, Kraus T, Haack M, Schuld A, Pollmacher T, Yirmiya R. Endotoxin-induced changes in food consumption in healthy volunteers are associated with TNF-alpha and IL-6 secretion. Psychoneuroendocrinology. 2002;27:945–56.
pubmed: 12383455
Lasselin J, Treadway MT, Lacourt TE, Soop A, Olsson MJ, Karshikoff B, et al. Lipopolysaccharide alters motivated behavior in a monetary reward task: a randomized trial. Neuropsychopharmacology. 2017;42:801–10.
pubmed: 27620550
Draper A, Koch RM, van der Meer JW, Aj Apps M, Pickkers P, Husain M, et al. Effort but not reward sensitivity is altered by acute sickness induced by experimental endotoxemia in humans. Neuropsychopharmacology. 2018;43:1107–18.
Benson S, Brinkhoff A, Lueg L, Roderigo T, Kribben A, Wilde B, et al. Effects of acute systemic inflammation on the interplay between sad mood and affective cognition. Transl Psychiatry. 2017;7:1281.
pubmed: 29225332 pmcid: 5802562
DellaGioia N, Hannestad J. A critical review of human endotoxin administration as an experimental paradigm of depression. Neurosci Biobehav Rev. 2010;34:130–43.
pubmed: 19666048
Schedlowski M, Engler H, Grigoleit JS. Endotoxin-induced experimental systemic inflammation in humans: a model to disentangle immune-to-brain communication. Brain Behav Immun. 2014;35:1–8.
pubmed: 24491305
Altemus M, Sarvaiya N, Neill Epperson C. Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol. 2014;35:320–30.
pubmed: 24887405 pmcid: 4890708
Lasselin J, Lekander M, Axelsson J, Karshikoff B. Sex differences in how inflammation affects behavior: What we can learn from experimental inflammatory models in humans. Front Neuroendocrinol. 2018;50:91–106.
pubmed: 29935190
Engler H, Benson S, Wegner A, Spreitzer I, Schedlowski M, Elsenbruch S. Men and women differ in inflammatory and neuroendocrine responses to endotoxin but not in the severity of sickness symptoms. Brain Behav Immun. 2016;52:18–26.
pubmed: 26291403
Cho HJ, Eisenberger NI, Olmstead R, Breen EC, Irwin MR. Preexisting mild sleep disturbance as a vulnerability factor for inflammation-induced depressed mood: a human experimental study. Transl Psychiatry. 2016;6:e750.
pubmed: 26954978 pmcid: 4872448
Karshikoff B, Lekander M, Soop A, Lindstedt F, Ingvar M, Kosek E, et al. Modality and sex differences in pain sensitivity during human endotoxemia. Brain Behav Immun. 2015;46:35–43.
pubmed: 25486090
Moieni M, Irwin MR, Jevtic I, Olmstead R, Breen EC, Eisenberger NI. Sex differences in depressive and socioemotional responses to an inflammatory challenge: implications for sex differences in depression. Neuropsychopharmacology. 2015;40:1709–16.
pubmed: 25598426 pmcid: 4915253
Wegner A, Benson S, Rebernik L, Spreitzer I, Jager M, Schedlowski M, et al. Sex differences in the pro-inflammatory cytokine response to endotoxin unfold in vivo but not ex vivo in healthy humans. Innate Immun. 2017;23:432–9.
pubmed: 28443392
Moieni M, Tan KM, Inagaki TK, Muscatell KA, Dutcher JM, Jevtic I, et al. Sex differences in the relationship between inflammation and reward sensitivity: a randomized controlled trial of endotoxin. Biol Psychiatry Cogn Neurosci Neuroimaging. 2019;4:619–26.
pubmed: 31103547 pmcid: 6612452
Kraynak TE, Marsland AL, Wager TD, Gianaros PJ. Functional neuroanatomy of peripheral inflammatory physiology: a meta-analysis of human neuroimaging studies. Neurosci Biobehav Rev. 2018;94:76–92.
Kullmann JS, Grigoleit JS, Wolf OT, Engler H, Oberbeck R, Elsenbruch S, et al. Experimental human endotoxemia enhances brain activity during social cognition. Soc Cogn Affect Neurosci. 2014;9:786–93.
pubmed: 23547245
Eisenberger NI, Inagaki TK, Rameson LT, Mashal NM, Irwin MR. An fMRI study of cytokine-induced depressed mood and social pain: the role of sex differences. Neuroimage. 2009;47:881–90.
pubmed: 19376240
Inagaki TK, Muscatell KA, Irwin MR, Moieni M, Dutcher JM, Jevtic I, et al. The role of the ventral striatum in inflammatory-induced approach toward support figures. Brain Behav Immun. 2015;44:247–52.
pubmed: 25459101
Kullmann JS, Grigoleit JS, Lichte P, Kobbe P, Rosenberger C, Banner C, et al. Neural response to emotional stimuli during experimental human endotoxemia. Hum Brain Mapp. 2013;34:2217–27.
pubmed: 22461242
Labrenz F, Wrede K, Forsting M, Engler H, Schedlowski M, Elsenbruch S, et al. Alterations in functional connectivity of resting state networks during experimental endotoxemia - An exploratory study in healthy men. Brain Behav Immun. 2016;54:17–26.
pubmed: 26597151
Lekander M, Karshikoff B, Johansson E, Soop A, Fransson P, Lundstrom JN, et al. Intrinsic functional connectivity of insular cortex and symptoms of sickness during acute experimental inflammation. Brain Behav Immun. 2016;56:34–41.
pubmed: 26732827
Muscatell KA, Moieni M, Inagaki TK, Dutcher JM, Jevtic I, Breen EC, et al. Exposure to an inflammatory challenge enhances neural sensitivity to negative and positive social feedback. Brain Behav Immun. 2016;57:21–9.
pubmed: 27032568 pmcid: 5011017
Inagaki TK, Muscatell KA, Irwin MR, Cole SW, Eisenberger NI. Inflammation selectively enhances amygdala activity to socially threatening images. Neuroimage. 2012;59:3222–6.
pubmed: 22079507
Stuhrmann A, Suslow T, Dannlowski U. Facial emotion processing in major depression: a systematic review of neuroimaging findings. Biol mood Anxiety Disord. 2011;1:10.
pubmed: 22738433 pmcid: 3384264
Golkar A, Lonsdorf TB, Olsson A, Lindstrom KM, Berrebi J, Fransson P, et al. Distinct contributions of the dorsolateral prefrontal and orbitofrontal cortex during emotion regulation. PLoS ONE. 2012;7:e48107.
pubmed: 23144849 pmcid: 3492343
Hamilton JP, Etkin A, Furman DJ, Lemus MG, Johnson RF, Gotlib IH. Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. Am J Psychiatry. 2012;169:693–703.
pubmed: 22535198
Felger JC, Li Z, Haroon E, Woolwine BJ, Jung MY, Hu X, et al. Inflammation is associated with decreased functional connectivity within corticostriatal reward circuitry in depression. Mol Psychiatry. 2016;21:1358–65.
pubmed: 26552591
Harrison NA, Voon V, Cercignani M, Cooper EA, Pessiglione M, Critchley HD. A neurocomputational account of how inflammation enhances sensitivity to punishments versus rewards. Biol Psychiatry. 2016;80:73–81.
pubmed: 26359113 pmcid: 4918729
Allen TA, Lam RW, Milev R, Rizvi SJ, Frey BN, MacQueen GM, et al. Early change in reward and punishment sensitivity as a predictor of response to antidepressant treatment for major depressive disorder: a CAN-BIND-1 report. Psychol Med. 2019;49:1629–38.
pubmed: 30220263
Benson S, Rebernik L, Wegner A, Kleine-Borgmann J, Engler H, Schlamann M, et al. Neural circuitry mediating inflammation-induced central pain amplification in human experimental endotoxemia. Brain Behav Immun. 2015;48:222–31.
Karshikoff B, Jensen KB, Kosek E, Kalpouzos G, Soop A, Ingvar M, et al. Why sickness hurts: A central mechanism for pain induced by peripheral inflammation. Brain Behav Immun. 2016;57:38–46.
Mayberg HS, Liotti M, Brannan SK, McGinnis S, Mahurin RK, Jerabek PA, et al. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry. 1999;156:675–82.
pubmed: 10327898
Paulus MP, Stein MB. Interoception in anxiety and depression. Brain Struct Funct. 2010;214:451–63.
pubmed: 20490545 pmcid: 2886901
Quadt L, Critchley HD, Garfinkel SN. The neurobiology of interoception in health and disease. Ann N Y Acad Sci. 2018;1428:112–28.
Enache D, Pariante CM, Mondelli V. 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. Brain Behav Immun. 2019;81:24–40.
pubmed: 31195092
Setiawan E, Wilson AA, Mizrahi R, Rusjan PM, Miler L, Rajkowska G, et al. Role of translocator protein density, a marker of neuroinflammation, in the brain during major depressive episodes. JAMA Psychiatry. 2015;72:268–75.
Holmes SE, Hinz R, Conen S, Gregory CJ, Matthews JC, Anton-Rodriguez JM, et al. Elevated translocator protein in anterior cingulate in major depression and a role for inflammation in suicidal thinking: a positron emission tomography study. Biol Psychiatry. 2018;83:61–9.
pubmed: 28939116
Richards EM, Zanotti-Fregonara P, Fujita M, Newman L, Farmer C, Ballard ED, et al. PET radioligand binding to translocator protein (TSPO) is increased in unmedicated depressed subjects. EJNMMI Res. 2018;8:57.
Hannestad J, Gallezot JD, Schafbauer T, Lim K, Kloczynski T, Morris ED, et al. Endotoxin-induced systemic inflammation activates microglia: [(1)(1)C]PBR28 positron emission tomography in nonhuman primates. Neuroimage. 2012;63:232–9.
pubmed: 22776451
Attwells S, Setiawan E, Rusjan PM, Xu C, Hutton C, Rafiei D, et al. Translocator protein distribution volume predicts reduction of symptoms during open-label trial of celecoxib in major depressive disorder. Biol Psychiatry. 2020;S0006-3223(20)31326-3.
Meyer JH, Cervenka S, Kim MJ, Kresi WC, Henter ID, Innis RB. Neuroinflammation in psychiatric disorders: pet imaging and promising new targets. Lancet Psychiatry. (in press).
Notter T, Coughlin JM, Sawa A, Meyer U. Reconceptualization of translocator protein as a biomarker of neuroinflammation in psychiatry. Mol Psychiatry. 2018;23:36–47.
pubmed: 29203847
Notter T, Schalbetter SM, Clifton NE, Mattei D, Richetto J, Thomas K, et al. Neuronal activity increases translocator protein (TSPO) levels. Mol Psychiatry. 2020. https://doi.org/10.1038/s41380-020-0745-1 .
Nettis MA, Veronese M, Nikkheslat N, Mariani N, Lombardo G, Sforzini L, et al. PET imaging shows no changes in TSPO brain density after IFN-alpha immune challenge in healthy human volunteers. Transl Psychiatry. 2020;10:89.
pubmed: 32152285 pmcid: 7063038
Forsberg A, Lampa J, Estelius J, Cervenka S, Farde L, Halldin C, et al. Disease activity in rheumatoid arthritis is inversely related to cerebral TSPO binding assessed by [(11)C]PBR28 positron emission tomography. J Neuroimmunol. 2019;334:577000.
pubmed: 31260948
Tamm S, Cervenka S, Forsberg A, Estelius J, Grunewald J, Gyllfors P, et al. Evidence of fatigue, disordered sleep and peripheral inflammation, but not increased brain TSPO expression, in seasonal allergy: a [(11)C]PBR28 PET study. Brain Behav Immun. 2018;68:146–57.
pubmed: 29054675
Byrne ML, Whittle S, Allen NB. The role of brain structure and function in the association between inflammation and depressive symptoms: a systematic review. Psychosom Med. 2016;78:389–400.
pubmed: 26910795
Suffredini AF, Noveck RJ. Human endotoxin administration as an experimental model in drug development. Clin Pharm Ther. 2014;96:418–22.
Adzic M, Brkic Z, Mitic M, Francija E, Jovicic MJ, Radulovic J, et al. Therapeutic strategies for treatment of inflammation-related depression. Curr Neuropharmacol. 2018;16:176–209.
pubmed: 28847294 pmcid: 5883379
Haroon E, Raison CL, Miller AH. Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology. 2012;37:137–62.
pubmed: 21918508
Kohler O, Krogh J, Mors O, Eriksen Benros M. Inflammation in depression and the potential for anti-inflammatory treatment. Curr Neuropharmacol. 2016;14:732–42.
pubmed: 27640518 pmcid: 5050394
Mendlewicz J, Kriwin P, Oswald P, Souery D, Alboni S, Brunello N. Shortened onset of action of antidepressants in major depression using acetylsalicylic acid augmentation: a pilot open-label study. Int Clin Psychopharmacol. 2006;21:227–31.
pubmed: 16687994
Muller N, Schwarz MJ, Dehning S, Douhe A, Cerovecki A, Goldstein-Muller B, et al. The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine. Mol Psychiatry. 2006;11:680–4.
pubmed: 16491133
Tyring S, Gottlieb A, Papp K, Gordon K, Leonardi C, Wang A, et al. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet. 2006;367:29–35.
pubmed: 16399150
Raison CL, Rutherford RE, Woolwine BJ, Shuo C, Schettler P, Drake DF, et al. A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: the role of baseline inflammatory biomarkers. JAMA Psychiatry. 2013;70:31–41.
pubmed: 22945416 pmcid: 4015348
Kohler O, Benros ME, Nordentoft M, Farkouh ME, Iyengar RL, Mors O, et al. Effect of anti-inflammatory treatment on depression, depressive symptoms, and adverse effects: a systematic review and meta-analysis of randomized clinical trials. JAMA Psychiatry. 2014;71:1381–91.
pubmed: 25322082
Kappelmann N, Lewis G, Dantzer R, Jones PB, Khandaker GM. Antidepressant activity of anti-cytokine treatment: a systematic review and meta-analysis of clinical trials of chronic inflammatory conditions. Mol Psychiatry. 2018;23:335–43.
pubmed: 27752078
Husain MI, Chaudhry IB, Husain N, Khoso AB, Rahman RR, Hamirani MM, et al. Minocycline as an adjunct for treatment-resistant depressive symptoms: a pilot randomised placebo-controlled trial. J Psychopharmacol. 2017;31:1166–75.
pubmed: 28857658
Rosenblat JD, McIntyre RS. Efficacy and tolerability of minocycline for depression: a systematic review and meta-analysis of clinical trials. J Affect Disord. 2018;227:219–25.
pubmed: 29102836
Capuron L, Miller AH. Immune system to brain signaling: neuropsychopharmacological implications. Pharm Ther. 2011;130:226–38.
Haroon E, Miller AH. Inflammation effects on brain glutamate in depression: mechanistic considerations and treatment implications. Curr Top Behav Neurosci. 2017;31:173–98.
pubmed: 27830574
Yang JJ, Wang N, Yang C, Shi JY, Yu HY, Hashimoto K. Serum interleukin-6 is a predictive biomarker for ketamine’s antidepressant effect in treatment-resistant patients with major depression. Biol Psychiatry. 2015;77:e19–20.
pubmed: 25104172
Kiraly DD, Horn SR, Van Dam NT, Costi S, Schwartz J, Kim-Schulze S, et al. Altered peripheral immune profiles in treatment-resistant depression: response to ketamine and prediction of treatment outcome. Transl psychiatry. 2017;7:e1065.
pubmed: 28323284 pmcid: 5416674
O’Connor JC, Lawson MA, Andre C, Moreau M, Lestage J, Castanon N, et al. Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol Psychiatry. 2009;14:511–22.
pubmed: 18195714
Jeon SA, Lee E, Hwang I, Han B, Park S, Son S, et al. NLRP3 inflammasome contributes to lipopolysaccharide-induced depressive-like behaviors via indoleamine 2,3-dioxygenase induction. Int J Neuropsychopharmacol. 2017;20:896–906.
pubmed: 29016824 pmcid: 5737528
Walker AK, Budac DP, Bisulco S, Lee AW, Smith RA, Beenders B, et al. NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6J mice. Neuropsychopharmacology. 2013;38:1609–16.
pubmed: 23511700 pmcid: 3717543
Ferguson JF, Mulvey CK, Patel PN, Shah RY, Doveikis J, Zhang W, et al. Omega-3 PUFA supplementation and the response to evoked endotoxemia in healthy volunteers. Mol Nutr food Res. 2014;58:601–13.
pubmed: 24190860
Bruce-Keller AJ, Salbaum JM, Berthoud HR. Harnessing gut microbes for mental health: getting from here to there. Biol Psychiatry. 2018;83:214–23.
pubmed: 29031410
Larrieu T, Laye S. Food for mood: relevance of nutritional omega-3 fatty acids for depression and anxiety. Front Physiol. 2018;9:1047.
pubmed: 30127751 pmcid: 6087749
Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J, Tito RY, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol. 2019;4:623–32.
Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J. 2003;17:884–6.
pubmed: 12626436
Paolucci EM, Loukov D, Bowdish DME, Heisz JJ. Exercise reduces depression and inflammation but intensity matters. Biol Psychol. 2018;133:79–84.
pubmed: 29408464
Benson S, Engler H, Wegner A, Rebernik L, Spreitzer I, Schedlowski M, et al. What makes you feel sick after inflammation? predictors of acute and persisting physical sickness symptoms induced by experimental endotoxemia. Clin Pharmacol Ther. 2017;102:141–51.
Moieni M, Irwin MR, Jevtic I, Breen EC, Cho HJ, Arevalo JM, et al. Trait sensitivity to social disconnection enhances pro-inflammatory responses to a randomized controlled trial of endotoxin. Psychoneuroendocrinology. 2015;62:336–42.
pubmed: 26360770 pmcid: 4637264
Lacourt TE, Houtveen JH, Veldhuijzen van Zanten JJ, Bosch JA, Drayson MT, Van Doornen LJ. Negative affectivity predicts decreased pain tolerance during low-grade inflammation in healthy women. Brain Behav Immun. 2015;44:32–6.
pubmed: 25451608
O’Toole MS, Bovbjerg DH, Renna ME, Lekander M, Mennin DS, Zachariae R. Effects of psychological interventions on systemic levels of inflammatory biomarkers in humans: a systematic review and meta-analysis. Brain Behav Immun. 2018;74:68–78.
Morgan N, Irwin MR, Chung M, Wang C. The effects of mind-body therapies on the immune system: meta-analysis. PLoS ONE. 2014;9:e100903.
pubmed: 24988414 pmcid: 4079606
Camara MI, Corrigan F, Jaehne EJ, Jawahar MC, Anscomb H, Baune BT. Effects of centrally administered etanercept on behavior, microglia, and astrocytes in mice following a peripheral immune challenge. Neuropsychopharmacology. 2014;40:502–12.
pubmed: 25103178 pmcid: 4443965
Ohgi Y, Futamura T, Kikuchi T, Hashimoto K. Effects of antidepressants on alternations in serum cytokines and depressive-like behavior in mice after lipopolysaccharide administration. Pharm Biochem Behav. 2013;103:853–9.
Demin KA, Sysoev M, Chernysh MV, Savva AK, Koshiba M, Wappler-Guzzetta EA, et al. Animal models of major depressive disorder and the implications for drug discovery and development. Expert Opin Drug Discov. 2019;14:365–78.
pubmed: 30793996
Hannestad J, DellaGioia N, Ortiz N, Pittman B, Bhagwagar Z. Citalopram reduces endotoxin-induced fatigue. Brain Behav Immun. 2011;25:256–9.
pubmed: 20955776
Felger JC, Haroon E, Miller AH. What’s CRP got to do with it? Tackling the complexities of the relationship between CRP and depression. Brain Behav Immun. 2018;73:163–4.
pubmed: 30077590
Horn SR, Long MM, Nelson BW, Allen NB, Fisher PA, Byrne ML. Replication and reproducibility issues in the relationship between C-reactive protein and depression: A systematic review and focused meta-analysis. Brain Behav Immun. 2018;73:85–114.
pubmed: 29928963 pmcid: 6800199
Del Giudice M, Gangestad SW. Rethinking IL-6 and CRP: Why they are more than inflammatory biomarkers, and why it matters. Brain Behav Immun. 2018;70:61–75.
pubmed: 29499302
Irwin MR, Cole S, Olmstead R, Breen EC, Cho JJ, Moieni M, et al. Moderators for depressed mood and systemic and transcriptional inflammatory responses: a randomized controlled trial of endotoxin. Neuropsychopharmacology. 2019;44:635–41.
Cho JH, Irwin MR, Eisenberger NI, Lamkin DM, Cole SW. Transcriptomic predictors of inflammation-induced depressed mood. Neuropsychopharmacology. 2019;44:923–9.
pubmed: 30643228 pmcid: 6462041
Musselman DL, Lawson DH, Gumnick JF, Manatunga AK, Penna S, Goodkin RS, et al. Paroxetine for the prevention of depression induced by high-dose interferon alfa. N. Engl J Med. 2001;344:961–6.
pubmed: 11274622
Raison CL, Borisov AS, Majer M, Drake DF, Pagnoni G, Woolwine BJ, et al. Activation of central nervous system inflammatory pathways by interferon-alpha: relationship to monoamines and depression. Biol Psychiatry. 2009;65:296–303.
pubmed: 18801471
Capuron L, Pagnoni G, Drake DF, Woolwine BJ, Spivey JR, Crowe RJ, et al. Dopaminergic mechanisms of reduced basal ganglia responses to hedonic reward during interferon alfa administration. Arch Gen Psychiatry. 2012;69:1044–53.
pubmed: 23026954 pmcid: 3640298
Haroon E, Felger JC, Woolwine BJ, Chen X, Parekh S, Spivey JR, et al. Age-related increases in basal ganglia glutamate are associated with TNF, reduced motivation and decreased psychomotor speed during IFN-alpha treatment: Preliminary findings. Brain Behav Immun. 2015;46:17–22.
pubmed: 25500218
Dipasquale O, Cooper EA, Tibble J, Voon V, Baglio F, Baselli G, et al. Interferon-alpha acutely impairs whole-brain functional connectivity network architecture-A preliminary study. Brain Behav Immun. 2016;58:31–9.
pubmed: 26697999 pmcid: 5074446
Dowell NG, Cooper EA, Tibble J, Voon V, Critchley HD, Cercignani M, et al. Acute changes in striatal microstructure predict the development of interferon-alpha induced fatigue. Biol Psychiatry. 2016;79:320–8.
pubmed: 26169252 pmcid: 4725575
Dowell NG, Bouyagoub S, Tibble J, Voon V, Cercignani M, Harrison NA. Interferon-alpha-induced changes in NODDI predispose to the development of fatigue. Neuroscience. 2019;403:111–7.
pubmed: 29292074
Harrison NA, Brydon L, Walker C, Gray MA, Steptoe A, Critchley HD. Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biol Psychiatry. 2009;66:407–14.
pubmed: 19423079 pmcid: 2885494
Balter LJT, Hulsken S, Aldred S, Drayson MT, Higgs S, Veldhuijzen van Zanten JJCS, et al. Low-grade inflammation decreases emotion recognition–evidence from the vaccination model of inflammation. Brain Behav Immun. 2018;73:216–21.
pubmed: 29742460
Harrison NA, Brydon L, Walker C, Gray MA, Steptoe A, Dolan RJ, et al. Neural origins of human sickness in interoceptive responses to inflammation. Biol Psychiatry. 2009;66:415–22.
pubmed: 19409533 pmcid: 2885492
Suffredini AF, Hochstein HD, McMahon FG. Dose-related inflammatory effects of intravenous endotoxin in humans: evaluation of a new clinical lot of Escherichia coli O:113 endotoxin. J Infect Dis. 1999;179:1278–82.
pubmed: 10191237
Lasselin J, Petrovic P, Olsson MJ, Paues Goranson S, Lekander M, Jensen KB, et al. Sickness behavior is not all about the immune response: Possible roles of expectations and prediction errors in the worry of being sick. Brain Behav Immun. 2018;74:213–21.
pubmed: 30217536
Lasselin J, Schedlowski M, Karshikoff B, Engler H, Lekander M, Konsman JP. Comparison of bacterial lipopolysaccharide-induced sickness behavior in rodents and humans: Relevance for symptoms of anxiety and depression. Neurosci Biobehav Rev. 2020;115:15–24.
Kiers D, Koch RM, Hamers L, Gerretsen J, Thijs EJ, van Ede L, et al. Characterization of a model of systemic inflammation in humans in vivo elicited by continuous infusion of endotoxin. Sci Rep. 2017;7:40149.
pubmed: 28054645 pmcid: 5215288
Capuron L, Raison CL, Musselman DL, Lawson DH, Nemeroff CB, Miller AH. Association of exaggerated HPA axis response to the initial injection of interferon-alpha with development of depression during interferon-alpha therapy. Am J Psychiatry. 2003;160:1342–5.
pubmed: 12832253
Lasselin J, Benson S, Hebebrand J, Boy K, Weskamp V, Handke A, et al. Immunological and behavioral responses to in vivo lipopolysaccharide administration in young and healthy obese and normal-weight humans. Brain Behav Immun. 2020;88:283–93.
Evans DL, Charney DS, Lewis L, Golden RN, Gorman JM, Krishnan KR, et al. Mood disorders in the medically ill: scientific review and recommendations. Biol Psychiatry. 2005;58:175–89.
pubmed: 16084838
Lange T, Dimitrov S, Born J. Effects of sleep and circadian rhythm on the human immune system. Ann N. Y Acad Sci. 2010;1193:48–59.
pubmed: 20398008
MacDonald L, Radler M, Paolini AG, Kent S. Calorie restriction attenuates LPS-induced sickness behavior and shifts hypothalamic signaling pathways to an anti-inflammatory bias. Am J Physiol Regul Integr Comp Physiol. 2011;301:R172–84.
pubmed: 21525175
Lasselin J, Karshikoff B, Axelsson J, Akerstedt T, Benson S, Engler H, et al. Fatigue and sleepiness responses to experimental inflammation and exploratory analysis of the effect of baseline inflammation in healthy humans. Brain Behav Immun. 2020;83:309–14.
pubmed: 31682972
Andreasson A, Wicksell RK, Lodin K, Karshikoff B, Axelsson J, Lekander M. A global measure of sickness behaviour: Development of the Sickness Questionnaire. J Health Psychol. 2018;23:1452–63.

Auteurs

Julie Lasselin (J)

Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, 45122, Essen, Germany. Julie.lasselin@su.se.
Stress Research Institute, Stockholm University, 10691, Stockholm, Sweden. Julie.lasselin@su.se.
Department of Clinical Neuroscience, Division for Psychology, Karolinska Institutet, Nobels väg 9, 17177, Stockholm, Sweden. Julie.lasselin@su.se.
Osher Center for Integrative Medicine, ME Neuroradiologi, Karolinska Universitetssjukhuset, Stockholm, Sweden. Julie.lasselin@su.se.

Mats Lekander (M)

Stress Research Institute, Stockholm University, 10691, Stockholm, Sweden.
Department of Clinical Neuroscience, Division for Psychology, Karolinska Institutet, Nobels väg 9, 17177, Stockholm, Sweden.
Osher Center for Integrative Medicine, ME Neuroradiologi, Karolinska Universitetssjukhuset, Stockholm, Sweden.

Sven Benson (S)

Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, 45122, Essen, Germany.

Manfred Schedlowski (M)

Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, 45122, Essen, Germany.
Department of Clinical Neuroscience, Division for Psychology, Karolinska Institutet, Nobels väg 9, 17177, Stockholm, Sweden.

Harald Engler (H)

Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, 45122, Essen, Germany.

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