The Specific Interaction of Lithium and Suicide History on Temporal Cortical Thickness in Bipolar Disorder
Journal: Journal of Clinical Medicine Research DOI: 10.32629/jcmr.v6i2.4058
Abstract
Background: Lithium, which exerts an antisuicidal effect in bipolar disorder (BD), was frequently reported to increase the grey matter in the temporal lobe. Suicide was also associated with brain structural abnormalities, including abnormalities in the temporal cortex. However, whether there exists an interactive effect of lithium treatment and suicide on the temporal cortex is still unknown. Methods: Our study recruited 165 BD patients (39 patients with suicide attempt history (SAH), 126 patients without SAH) and 147 healthy controls (HC), Structural imaging data were obtained by the Magnetic resonance imaging (MRI) of 3.0 Tesla, and were processed under the Freesurfer v6.0 software. We extracted eight thickness measurements from temporal cortex, including bilateral superior temporal gyrus, middle temporal gyrus, inferior temporal gyrus and transverse temporal cortex. General linear model was performed with eight thickness measurements with as dependent variables. Bonferroni correction for multiple comparisons of these measurements was applied to the results. Results: Compared to HC, BD without lithium treatment showed significantly decreased thickness in all measurements (all P < 0.05), while BD with lithium treatment only showed significant thinner left superior temporal and right superior temporal thickness (all P < 0.05). We found a significant SAH by lithium treatment interaction on left middle temporal thickness (F = 9.172, P = 0.024, Partial Eta Squared = 0.055), Post hoc tests with the Bonferroni correction revealed that in lithium-treated BD patients, left middle temporal thickness in patients with SAH were higher than patients without SAH. Interestingly, in the BD patients without lithium treatment, the patients with SAH had thinner middle temporal thickness compared to patients without SAH. Conclusions: This is the first study of the association between lithium therapy and suicidality on the temporal thickness in BD. We observed an increased effect of lithium on middle temporal thickness in BD patients with suicide history. Our result suggested that left middle temporal cortex might be a potential target for suicide therapy, as well as for monitoring the antisuicidal effect of lithium.
Keywords
Lithium, bipolar disorder, temporal cortex, cortical thickness
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[29]Maller JJ, Thaveenthiran P, Thomson RH, McQueen S, Fitzgerald PB: Volumetric, cortical thickness and white matter integrity alterations in bipolar disorder type I and II. J Affect Disord 2014, 169:118-127.
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[31]Abé C, Liberg B, Song J, Bergen SE, Petrovic P, Ekman CJ, Sellgren CM, Ingvar M, Landén M: Longitudinal Cortical Thickness Changes in Bipolar Disorder and the Relationship to Genetic Risk, Mania, and Lithium Use. Biological Psychiatry 2020, 87(3):271-281.
[32]Dickerson BC, Wolk DA, Alzheimer's Disease Neuroimaging I: MRI cortical thickness biomarker predicts AD-like CSF and cognitive decline in normal adults. Neurology 2012, 78(2):84-90.
[33]Wagner G, Schultz CC, Koch K, Schachtzabel C, Sauer H, Schlosser RG: Prefrontal cortical thickness in depressed patients with high-risk for suicidal behavior. J Psychiatr Res 2012, 46(11):1449-1455.
[34]Mahon K, Burdick KE, Wu J, Ardekani BA, Szeszko PR: Relationship between suicidality and impulsivity in bipolar I disorder: a diffusion tensor imaging study. Bipolar Disord 2012, 14(1):80-89.
[35]Winkler AM, Kochunov P, Blangero J, Almasy L, Zilles K, Fox PT, Duggirala R, Glahn DC: Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 2010, 53(3):1135-1146.
[36]van Heeringen K, Mann JJ: The neurobiology of suicide. Lancet Psychiatry 2014, 1(1):63-72.
[37]Padoa-Schioppa C, Assad JA: Neurons in the orbitofrontal cortex encode economic value. Nature 2006, 441(7090):223-226.
[38]Saleem KS, Kondo H, Price JL: Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J Comp Neurol 2008, 506(4):659-693.
[39]Hou L, Heilbronner U, Degenhardt F, Adli M, Akiyama K, Akula N, Ardau R, Arias B, Backlund L, Banzato CEM et al: Genetic variants associated with response to lithium treatment in bipolar disorder: a genome-wide association study. Lancet 2016, 387(10023):1085-1093.
[40]Lee YJ, Kim YK: The impact of glycogen synthase kinase 3beta gene on psychotic mania in bipolar disorder patients. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(5):1303-1308.
[41]Gigante AD, Young LT, Yatham LN, Andreazza AC, Nery FG, Grinberg LT, Heinsen H, Lafer B: Morphometric post-mortem studies in bipolar disorder: possible association with oxidative stress and apoptosis. Int J Neuropsychopharmacol 2011, 14(8):1075-1089.
[42]Chitty KM, Lagopoulos J, Lee RS, Hickie IB, Hermens DF: A systematic review and meta-analysis of proton magnetic resonance spectroscopy and mismatch negativity in bipolar disorder. Eur Neuropsychopharmacol 2013, 23(11):1348-1363.
[43]Yuksel C, Ongur D: Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol Psychiatry 2010, 68(9):785-794.
[44]Nortje G, Stein DJ, Radua J, Mataix-Cols D, Horn N: Systematic review and voxel-based meta-analysis of diffusion tensor imaging studies in bipolar disorder. J Affect Disord 2013, 150(2):192-200.
[45]Vederine FE, Wessa M, Leboyer M, Houenou J: A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(8):1820-1826.
[46]Muneer A: Bipolar Disorder: Role of Inflammation and the Development of Disease Biomarkers. Psychiatry Investig 2016, 13(1):18-33.
[47]de Sousa RT, Zanetti MV, Talib LL, Serpa MH, Chaim TM, Carvalho AF, Brunoni AR, Busatto GF, Gattaz WF, Machado-Vieira R: Lithium increases platelet serine-9 phosphorylated GSK-3beta levels in drug-free bipolar disorder during depressive episodes. J Psychiatr Res 2015, 62:78-83.
[48]Ngok-Ngam P, Watcharasit P, Thiantanawat A, Satayavivad J: Pharmacological inhibition of GSK3 attenuates DNA damage-induced apoptosis via reduction of p53 mitochondrial translocation and Bax oligomerization in neuroblastoma SH-SY5Y cells. Cell Mol Biol Lett 2013, 18(1):58-74.
[49]Emamghoreishi M, Keshavarz M, Nekooeian AA: Acute and chronic effects of lithium on BDNF and GDNF mRNA and protein levels in rat primary neuronal, astroglial and neuroastroglia cultures. Iran J Basic Med Sci 2015, 18(3):240-246.
[50]Myint AM, Kim YK: Network beyond IDO in psychiatric disorders: revisiting neurodegeneration hypothesis. Prog Neuropsychopharmacol Biol Psychiatry 2014, 48:304-313.
[51]Wang HM, Zhang T, Li Q, Huang JK, Chen RF, Sun XJ: Inhibition of glycogen synthase kinase-3beta by lithium chloride suppresses 6-hydroxydopamine-induced inflammatory response in primary cultured astrocytes. Neurochem Int 2013, 63(5):345-353.
[2]Gitlin MJ, Swendsen J, Heller TL, Hammen C: Relapse and impairment in bipolar disorder. Am J Psychiatry 1995, 152(11):1635-1640.
[3]Chen YW, Dilsaver SC: Lifetime rates of suicide attempts among subjects with bipolar and unipolar disorders relative to subjects with other Axis I disorders. Biol Psychiatry 1996, 39(10):896-899.
[4]Tiihonen J, Lonnqvist J, Wahlbeck K, Klaukka T, Tanskanen A, Haukka J: Antidepressants and the risk of suicide, attempted suicide, and overall mortality in a nationwide cohort. Arch Gen Psychiatry 2006, 63(12):1358-1367.
[5]Sani G, Perugi G, Tondo L: Treatment of Bipolar Disorder in a Lifetime Perspective: Is Lithium Still the Best Choice? Clin Drug Investig 2017, 37(8):713-727.
[6]Practice guideline for the assessment and treatment of patients with suicidal behaviors. Am J Psychiatry 2003, 160(11 Suppl):1-60.
[7]Yildiz A, Vieta E, Leucht S, Baldessarini RJ: Efficacy of antimanic treatments: meta-analysis of randomized, controlled trials. Neuropsychopharmacology 2011, 36(2):375-389.
[8]Bani-Fatemi A, Tasmim S, Graff-Guerrero A, Gerretsen P, Strauss J, Kolla N, Spalletta G, De Luca V: Structural and functional alterations of the suicidal brain: An updated review of neuroimaging studies. Psychiatry Res Neuroimaging 2018, 278:77-91.
[9]Hozer F, Houenou J: Can neuroimaging disentangle bipolar disorder? J Affect Disord 2016, 195:199-214.
[10]Cox Lippard ET, Johnston JA, Blumberg HP: Neurobiological risk factors for suicide: insights from brain imaging. Am J Prev Med 2014, 47(3 Suppl 2):S152-162.
[11]Desmyter S, van Heeringen C, Audenaert K: Structural and functional neuroimaging studies of the suicidal brain. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(4):796-808.
[12]Zhang H, Chen Z, Jia Z, Gong Q: Dysfunction of neural circuitry in depressive patients with suicidal behaviors: a review of structural and functional neuroimaging studies. Prog Neuropsychopharmacol Biol Psychiatry 2014, 53:61-66.
[13]Jollant F, Near J, Turecki G, Richard-Devantoy S: Spectroscopy markers of suicidal risk and mental pain in depressed patients. Prog Neuropsychopharmacol Biol Psychiatry 2016.
[14]van Heeringen C, Bijttebier S, Godfrin K: Suicidal brains: a review of functional and structural brain studies in association with suicidal behaviour. Neurosci Biobehav Rev 2011, 35(3):688-698.
[15]Hirose T, Tsujii N, Mikawa W, Shirakawa O: Delayed hemodynamic responses associated with a history of suicide attempts in bipolar disorder: a multichannel near-infrared spectroscopy study. Psychiatry Res Neuroimaging 2018, 280:15-21.
[16]Benedetti F, Radaelli D, Poletti S, Locatelli C, Falini A, Colombo C, Smeraldi E: Opposite effects of suicidality and lithium on gray matter volumes in bipolar depression. J Affect Disord 2011, 135(1-3):139-147.
[17]Duarte DGG, Neves MCL, Albuquerque MR, Turecki G, Ding Y, de Souza-Duran FL, Busatto G, Correa H: Structural brain abnormalities in patients with type I bipolar disorder and suicidal behavior. Psychiatry Res Neuroimaging 2017, 265:9-17.
[18]Dominguez-Baleon C, Gutierrez-Mondragon LF, Campos-Gonzalez AI, Renteria ME: Neuroimaging Studies of Suicidal Behavior and Non-suicidal Self-Injury in Psychiatric Patients: A Systematic Review. Front Psychiatry 2018, 9:500.
[19]Won E, Kim YK: An Oldie but Goodie: Lithium in the Treatment of Bipolar Disorder through Neuroprotective and Neurotrophic Mechanisms. Int J Mol Sci 2017, 18(12).
[20]Price JL, Drevets WC: Neurocircuitry of mood disorders. Neuropsychopharmacology 2010, 35(1):192-216.
[21]Malhi GS, Bargh DM, Kuiper S, Coulston CM, Das P: Modeling bipolar disorder suicidality. Bipolar Disord 2013, 15(5):559-574.
[22]Ding Y, Lawrence N, Olie E, Cyprien F, le Bars E, Bonafe A, Phillips ML, Courtet P, Jollant F: Prefrontal cortex markers of suicidal vulnerability in mood disorders: a model-based structural neuroimaging study with a translational perspective. Transl Psychiatry 2015, 5:e516.
[23]Takahashi T, Malhi GS, Wood SJ, Yucel M, Walterfang M, Kawasaki Y, Suzuki M, Pantelis C: Gray matter reduction of the superior temporal gyrus in patients with established bipolar I disorder. J Affect Disord 2010, 123(1-3):276-282.
[24]Hibar DP, Westlye LT, Doan NT, Jahanshad N, Cheung JW, Ching CRK, Versace A, Bilderbeck AC, Uhlmann A, Mwangi B et al: Cortical abnormalities in bipolar disorder: an MRI analysis of 6503 individuals from the ENIGMA Bipolar Disorder Working Group. Mol Psychiatry 2018, 23(4):932-942.
[25]Abe C, Ekman CJ, Sellgren C, Petrovic P, Ingvar M, Landen M: Cortical thickness, volume and surface area in patients with bipolar disorder types I and II. J Psychiatry Neurosci 2016, 41(4):240-250.
[26]Hanford LC, Nazarov A, Hall GB, Sassi RB: Cortical thickness in bipolar disorder: a systematic review. Bipolar Disord 2016, 18(1):4-18.
[27]Selvaraj S, Arnone D, Job D, Stanfield A, Farrow TF, Nugent AC, Scherk H, Gruber O, Chen X, Sachdev PS et al: Grey matter differences in bipolar disorder: a meta-analysis of voxel-based morphometry studies. Bipolar Disord 2012, 14(2):135-145.
[28]Savitz JB, Price JL, Drevets WC: Neuropathological and neuromorphometric abnormalities in bipolar disorder: view from the medial prefrontal cortical network. Neurosci Biobehav Rev 2014, 42:132-147.
[29]Maller JJ, Thaveenthiran P, Thomson RH, McQueen S, Fitzgerald PB: Volumetric, cortical thickness and white matter integrity alterations in bipolar disorder type I and II. J Affect Disord 2014, 169:118-127.
[30]Eker C, Simsek F, Yilmazer EE, Kitis O, Cinar C, Eker OD, Coburn K, Gonul AS: Brain regions associated with risk and resistance for bipolar I disorder: a voxel-based MRI study of patients with bipolar disorder and their healthy siblings. Bipolar Disord 2014, 16(3):249-261.
[31]Abé C, Liberg B, Song J, Bergen SE, Petrovic P, Ekman CJ, Sellgren CM, Ingvar M, Landén M: Longitudinal Cortical Thickness Changes in Bipolar Disorder and the Relationship to Genetic Risk, Mania, and Lithium Use. Biological Psychiatry 2020, 87(3):271-281.
[32]Dickerson BC, Wolk DA, Alzheimer's Disease Neuroimaging I: MRI cortical thickness biomarker predicts AD-like CSF and cognitive decline in normal adults. Neurology 2012, 78(2):84-90.
[33]Wagner G, Schultz CC, Koch K, Schachtzabel C, Sauer H, Schlosser RG: Prefrontal cortical thickness in depressed patients with high-risk for suicidal behavior. J Psychiatr Res 2012, 46(11):1449-1455.
[34]Mahon K, Burdick KE, Wu J, Ardekani BA, Szeszko PR: Relationship between suicidality and impulsivity in bipolar I disorder: a diffusion tensor imaging study. Bipolar Disord 2012, 14(1):80-89.
[35]Winkler AM, Kochunov P, Blangero J, Almasy L, Zilles K, Fox PT, Duggirala R, Glahn DC: Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 2010, 53(3):1135-1146.
[36]van Heeringen K, Mann JJ: The neurobiology of suicide. Lancet Psychiatry 2014, 1(1):63-72.
[37]Padoa-Schioppa C, Assad JA: Neurons in the orbitofrontal cortex encode economic value. Nature 2006, 441(7090):223-226.
[38]Saleem KS, Kondo H, Price JL: Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J Comp Neurol 2008, 506(4):659-693.
[39]Hou L, Heilbronner U, Degenhardt F, Adli M, Akiyama K, Akula N, Ardau R, Arias B, Backlund L, Banzato CEM et al: Genetic variants associated with response to lithium treatment in bipolar disorder: a genome-wide association study. Lancet 2016, 387(10023):1085-1093.
[40]Lee YJ, Kim YK: The impact of glycogen synthase kinase 3beta gene on psychotic mania in bipolar disorder patients. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(5):1303-1308.
[41]Gigante AD, Young LT, Yatham LN, Andreazza AC, Nery FG, Grinberg LT, Heinsen H, Lafer B: Morphometric post-mortem studies in bipolar disorder: possible association with oxidative stress and apoptosis. Int J Neuropsychopharmacol 2011, 14(8):1075-1089.
[42]Chitty KM, Lagopoulos J, Lee RS, Hickie IB, Hermens DF: A systematic review and meta-analysis of proton magnetic resonance spectroscopy and mismatch negativity in bipolar disorder. Eur Neuropsychopharmacol 2013, 23(11):1348-1363.
[43]Yuksel C, Ongur D: Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol Psychiatry 2010, 68(9):785-794.
[44]Nortje G, Stein DJ, Radua J, Mataix-Cols D, Horn N: Systematic review and voxel-based meta-analysis of diffusion tensor imaging studies in bipolar disorder. J Affect Disord 2013, 150(2):192-200.
[45]Vederine FE, Wessa M, Leboyer M, Houenou J: A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(8):1820-1826.
[46]Muneer A: Bipolar Disorder: Role of Inflammation and the Development of Disease Biomarkers. Psychiatry Investig 2016, 13(1):18-33.
[47]de Sousa RT, Zanetti MV, Talib LL, Serpa MH, Chaim TM, Carvalho AF, Brunoni AR, Busatto GF, Gattaz WF, Machado-Vieira R: Lithium increases platelet serine-9 phosphorylated GSK-3beta levels in drug-free bipolar disorder during depressive episodes. J Psychiatr Res 2015, 62:78-83.
[48]Ngok-Ngam P, Watcharasit P, Thiantanawat A, Satayavivad J: Pharmacological inhibition of GSK3 attenuates DNA damage-induced apoptosis via reduction of p53 mitochondrial translocation and Bax oligomerization in neuroblastoma SH-SY5Y cells. Cell Mol Biol Lett 2013, 18(1):58-74.
[49]Emamghoreishi M, Keshavarz M, Nekooeian AA: Acute and chronic effects of lithium on BDNF and GDNF mRNA and protein levels in rat primary neuronal, astroglial and neuroastroglia cultures. Iran J Basic Med Sci 2015, 18(3):240-246.
[50]Myint AM, Kim YK: Network beyond IDO in psychiatric disorders: revisiting neurodegeneration hypothesis. Prog Neuropsychopharmacol Biol Psychiatry 2014, 48:304-313.
[51]Wang HM, Zhang T, Li Q, Huang JK, Chen RF, Sun XJ: Inhibition of glycogen synthase kinase-3beta by lithium chloride suppresses 6-hydroxydopamine-induced inflammatory response in primary cultured astrocytes. Neurochem Int 2013, 63(5):345-353.
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