Correction of depression-associated circadian rhythm abnormalities is associated with lithium response in bipolar disorder.

bipolar disorder chronotype circadian rhythm lithium sleep

Journal

Bipolar disorders
ISSN: 1399-5618
Titre abrégé: Bipolar Disord
Pays: Denmark
ID NLM: 100883596

Informations de publication

Date de publication:
08 2022
Historique:
pubmed: 27 11 2021
medline: 27 11 2021
entrez: 26 11 2021
Statut: ppublish

Résumé

Bipolar disorder (BD) is characterized by episodes of depression and mania and disrupted circadian rhythms. Lithium is an effective therapy for BD, but only 30%-40% of patients are fully responsive. Preclinical models show that lithium alters circadian rhythms. However, it is unknown if the circadian rhythm effects of lithium are essential to its therapeutic properties. In secondary analyses of a multi-center, prospective, trial of lithium for BD, we examined the relationship between circadian rhythms and therapeutic response to lithium. Using standardized instruments, we measured morningness, diurnal changes in mood, sleep, and energy (circadian rhythm disturbances) in a cross-sectional study of 386 BD subjects with varying lithium exposure histories. Next, we tracked symptoms of depression and mania prospectively over 12 weeks in a subset of 88 BD patients initiating treatment with lithium. Total, circadian, and affective mood symptoms were scored separately and analyzed. Subjects with no prior lithium exposure had the most circadian disruption, while patients stable on lithium monotherapy had the least. Patients who were stable on lithium with another drug or unstable on lithium showed intermediate levels of disruption. Treatment with lithium for 12 weeks yielded significant reductions in total and affective depression symptoms. Lithium responders (Li-Rs) showed improvement in circadian symptoms of depression, but non-responders did not. There was no difference between Li-Rs and nonresponders in affective, circadian, or total symptoms of mania. Exposure to lithium is associated with reduced circadian disruption. Lithium response at 12 weeks was selectively associated with the reduction of circadian depressive symptoms. We conclude that stabilization of circadian rhythms may be an important feature of lithium's therapeutic effects. NCT0127253.

Sections du résumé

BACKGROUND
Bipolar disorder (BD) is characterized by episodes of depression and mania and disrupted circadian rhythms. Lithium is an effective therapy for BD, but only 30%-40% of patients are fully responsive. Preclinical models show that lithium alters circadian rhythms. However, it is unknown if the circadian rhythm effects of lithium are essential to its therapeutic properties.
METHODS
In secondary analyses of a multi-center, prospective, trial of lithium for BD, we examined the relationship between circadian rhythms and therapeutic response to lithium. Using standardized instruments, we measured morningness, diurnal changes in mood, sleep, and energy (circadian rhythm disturbances) in a cross-sectional study of 386 BD subjects with varying lithium exposure histories. Next, we tracked symptoms of depression and mania prospectively over 12 weeks in a subset of 88 BD patients initiating treatment with lithium. Total, circadian, and affective mood symptoms were scored separately and analyzed.
RESULTS
Subjects with no prior lithium exposure had the most circadian disruption, while patients stable on lithium monotherapy had the least. Patients who were stable on lithium with another drug or unstable on lithium showed intermediate levels of disruption. Treatment with lithium for 12 weeks yielded significant reductions in total and affective depression symptoms. Lithium responders (Li-Rs) showed improvement in circadian symptoms of depression, but non-responders did not. There was no difference between Li-Rs and nonresponders in affective, circadian, or total symptoms of mania.
CONCLUSIONS
Exposure to lithium is associated with reduced circadian disruption. Lithium response at 12 weeks was selectively associated with the reduction of circadian depressive symptoms. We conclude that stabilization of circadian rhythms may be an important feature of lithium's therapeutic effects.
CLINICAL TRIALS REGISTRY
NCT0127253.

Identifiants

pubmed: 34825444
doi: 10.1111/bdi.13162
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

521-529

Subventions

Organisme : National Institute of Mental Health R25
ID : MH101072
Organisme : NIMH/NIGMS
ID : MH92758
Organisme : The Western Norway Regional Health Authority and the Canadian Institutes of Health Research
ID : 64410
Organisme : VA BLR&D Merit Award
ID : BX003431
Organisme : BLRD VA
ID : I01 BX003431
Pays : United States
Organisme : NIMH NIH HHS
ID : U01 MH092758
Pays : United States

Informations de copyright

© 2021 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Références

Muller JK, Leweke FM. Bipolar disorder: clinical overview. Med Monatsschr Pharm. 2016;39(9):363-369.
Phillips ML, Kupfer DJ. Bipolar disorder diagnosis: challenges and future directions. Lancet. 2013;381(9878):1663-1671.
Pagani L, St. Clair PA, Teshiba TM, et al. Genetic contributions to circadian activity rhythm and sleep pattern phenotypes in pedigrees segregating for severe bipolar disorder. Proc Natl Acad Sci USA. 2016;113(6):E754-E761.
Merikangas KR, Swendsen J, Hickie IB, et al. Real-time mobile monitoring of the dynamic associations among motor activity, energy, mood, and sleep in adults with bipolar disorder. JAMA Psychiatry. 2019;76(2):190-198.
Harvey AG. Sleep and circadian rhythms in bipolar disorder: seeking synchrony, harmony, and regulation. Am J Psychiatry. 2008;165(7):820-829.
Takaesu Y, Inoue Y, Ono K, et al. Circadian rhythm sleep-wake disorders predict shorter time to relapse of mood episodes in euthymic patients with bipolar disorder: a prospective 48-week study. J Clin Psychiatry. 2018;79(1):17m11565.
Gold AK, Sylvia LG. The role of sleep in bipolar disorder. Nat Sci Sleep. 2016;8:207-214.
Steardo Jr L, de Filippis R, Carbone EA, Segura-Garcia C, Verkhratsky A, De Fazio P. Sleep disturbance in bipolar disorder: neuroglia and circadian rhythms. Front Psychiatry. 2019;10:501.
LeGates TA, Fernandez DC, Hattar S. Light as a central modulator of circadian rhythms, sleep and affect. Nat Rev Neurosci. 2014;15(7):443-454.
Takaesu Y. Circadian rhythm in bipolar disorder: a review of the literature. Psychiatry Clin Neurosci. 2018;72(9):673-682.
Boudebesse C, Lajnef M, Geoffroy PA, et al. Chronotypes of bipolar patients in remission: validation of the French version of the circadian type inventory in the FACE-BD sample. Chronobiol Int. 2013;30(8):1042-1049.
Ahn YM, Chang J, Joo YH, Kim SC, Lee KY, Kim YS. Chronotype distribution in bipolar I disorder and schizophrenia in a Korean sample. Bipolar Disord. 2008;10(2):271-275.
Baek JH, Kim JS, Kim MJ, et al. Lifetime characteristics of evening-preference and irregular bed-rise time are associated with lifetime seasonal variation of mood and behavior: comparison between individuals with bipolar disorder and healthy controls. Behav Sleep Med. 2016;14(2):155-168.
Wood J, Birmaher B, Axelson D, et al. Replicable differences in preferred circadian phase between bipolar disorder patients and control individuals. Psychiatry Res. 2009;166(2-3):201-209.
Giglio LM, Magalhaes PV, Andersen ML, Walz JC, Jakobson L, Kapczinski F. Circadian preference in bipolar disorder. Sleep Breath. 2010;14(2):153-155.
Lewis KJS, Richards A, Karlsson R, et al. Comparison of genetic liability for sleep traits among individuals with bipolar disorder I or II and control participants. JAMA Psychiatry. 2020;77(3):303-310.
Ferguson A, Lyall LM, Ward J, et al. Genome-wide association study of circadian rhythmicity in 71,500 UK biobank participants and polygenic association with mood instability. EBioMedicine. 2018;35:279-287.
Takaesu Y, Inoue Y, Ono K, et al. Circadian rhythm sleep-wake disorders as predictors for bipolar disorder in patients with remitted mood disorders. J Affect Disord. 2017;220:57-61.
McCarthy MJ. Missing a beat: assessment of circadian rhythm abnormalities in bipolar disorder in the genomic era. Psychiatr Genet. 2019;29(2):29-36.
Yoshikawa T, Honma S. Lithium lengthens circadian period of cultured brain slices in area specific manner. Behav Brain Res. 2016;314:30-37.
Campos-de-Sousa S, Guindalini C, Tondo L, et al. Nuclear receptor rev-erb-{alpha} circadian gene variants and lithium carbonate prophylaxis in bipolar affective disorder. J Biol Rhythms. 2010;25(2):132-137.
Li J, Lu WQ, Beesley S, Loudon AS, Meng QJ. Lithium impacts on the amplitude and period of the molecular circadian clockwork. PLoS One. 2012;7(3):e33292.
McCarthy MJ, Wei H, Marnoy Z, et al. Genetic and clinical factors predict lithium's effects on PER2 gene expression rhythms in cells from bipolar disorder patients. Transl Psychiatry. 2013;3:e318.
McCarthy MJ, Wei H, Nievergelt CM, et al. Chronotype and cellular circadian rhythms predict the clinical response to lithium maintenance treatment in patients with bipolar disorder. Neuropsychopharmacology. 2019;44(3):620-628.
Scott J, Hennion V, Meyrel M, Bellivier F, Etain B. An ecological study of objective rest-activity markers of lithium response in bipolar-I-disorder. Psychol Med. 2020;1-9.
Federoff M, McCarthy MJ. Sleep and circadian rhythm disruption is corrected by lithium in a case of bipolar disorder with familial BRCA1 mutation. Bipolar Disord. 2021;23(1):101-103.
McCarthy MJ, Fernandes M, Kranzler HR, Covault JM, Welsh DK. Circadian clock period inversely correlates with illness severity in cells from patients with alcohol use disorders. Alcohol Clin Exp Res. 2013;37(8):1304-1310.
Oedegaard KJ, Alda M, Anand A, et al. The Pharmacogenomics of Bipolar Disorder study (PGBD): identification of genes for lithium response in a prospective sample. BMC Psychiatry. 2016;16:129.
Lin Y, Maihofer AX, Stapp E, et al. Clinical predictors of non-response to lithium treatment in the Pharmacogenomics of Bipolar Disorder (PGBD) study. Bipolar Disord. 2021.
Akiskal HS, Akiskal KK, Haykal RF, Manning JS, Connor PD. TEMPS-A: progress towards validation of a self-rated clinical version of the Temperament Evaluation of the Memphis, Pisa, Paris, and San Diego Autoquestionnaire. J Affect Disord. 2005;85(1-2):3-16.
Brown FM. Psychometric equivalence of an improved Basic Language Morningness (BALM) scale using industrial population within comparisons. Ergonomics. 1993;36(1-3):191-197.
Altman EG, Hedeker DR, Janicak PG, Peterson JL, Davis JM. The Clinician-Administered Rating Scale for Mania (CARS-M): development, reliability, and validity. Biol Psychiatry. 1994;36(2):124-134.
Rush AJ, Trivedi MH, Ibrahim HM, et al. The 16-Item Quick Inventory of Depressive Symptomatology (QIDS), clinician rating (QIDS-C), and self-report (QIDS-SR): a psychometric evaluation in patients with chronic major depression. Biol Psychiatry. 2003;54(5):573-583.
Cuschieri S. The STROBE guidelines. Saudi J Anaesth. 2019;13(Suppl 1):S31-S34.
Jones SE, Lane JM, Wood AR, et al. Genome-wide association analyses of chronotype in 697,828 individuals provides insights into circadian rhythms. Nat Commun. 2019;10(1):343.
Gonzalez R, Tamminga CA, Tohen M, Suppes T. The relationship between affective state and the rhythmicity of activity in bipolar disorder. J Clin Psychiatry. 2014;75(4):e317-e322.
Wu JC, Kelsoe JR, Schachat C, et al. Rapid and sustained antidepressant response with sleep deprivation and chronotherapy in bipolar disorder. Biol Psychiatry. 2009;66(3):298-301.
International Consortium on Lithium Genetics, Amare AT, Schubert KO, Hou L, et al. Association of Polygenic Score for Schizophrenia and HLA antigen and inflammation genes with response to lithium in bipolar affective disorder: a genome-wide association study. JAMA Psychiatry. 2018;75(1):65-74.
Amare AT, Vaez A, Hsu Y-H, et al. Bivariate genome-wide association analyses of the broad depression phenotype combined with major depressive disorder, bipolar disorder or schizophrenia reveal eight novel genetic loci for depression. Mol Psychiatry. 2020;25(7):1420-1429.
Amare AT, Schubert KO, Hou L, et al. Association of polygenic score for major depression with response to lithium in patients with bipolar disorder. Mol Psychiatry. 2021;26(6):2457-2470.
Lyall LM, Wyse CA, Graham N, et al. Association of disrupted circadian rhythmicity with mood disorders, subjective wellbeing, and cognitive function: a cross-sectional study of 91 105 participants from the UK Biobank. Lancet Psychiatry. 2018;5(6):507-514.
Chrobak AA, Tereszko A, Dembinska-Krajewska D, et al. The role of affective temperaments assessed by the Temperament Evaluation of Memphis, Pisa and San Diego-Autoquestionnaire (TEMPS-A) in the relationship between morningness-eveningness and bipolarity. J Affect Disord. 2018;232:83-88.

Auteurs

Monica Federoff (M)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.

Michael J McCarthy (MJ)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.
Department of Psychiatry, VA San Diego Healthcare System, La Jolla, California, USA.

Amit Anand (A)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

Wade H Berrettini (WH)

University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA.

Holli Bertram (H)

University of Michigan, Ann Arbor, Michigan, USA.

Abesh Bhattacharjee (A)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.
Department of Psychiatry, VA San Diego Healthcare System, La Jolla, California, USA.

Cynthia V Calkin (CV)

Dalhousie University, Halifax, Canada.

Carla Conroy (C)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

William H Coryell (WH)

University of Iowa, Iowa City, Iowa, USA.

Nicole D'Arcangelo (N)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

Anna DeModena (A)

Department of Psychiatry, VA San Diego Healthcare System, La Jolla, California, USA.

Carrie Fisher (C)

Departments of Psychiatry and Medical and Molecular Genetics, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, Indiana, USA.

Scott Feeder (S)

Mayo Clinic, Rochester, Minnesota, USA.

Nicole Frazier (N)

University of Michigan, Ann Arbor, Michigan, USA.

Mark A Frye (MA)

Mayo Clinic, Rochester, Minnesota, USA.

Keming Gao (K)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

Julie Garnham (J)

Dalhousie University, Halifax, Canada.

Elliot S Gershon (ES)

University of Chicago, Chicago, Illinois, USA.

Ney Alliey-Rodriguez (N)

University of Chicago, Chicago, Illinois, USA.

Kara Glazer (K)

Department of Psychiatry and Behavioral Sciences, The Johns Hopkins School of Medicine, Baltimore, Maryland, USA.

Fernando Goes (F)

Department of Psychiatry and Behavioral Sciences, The Johns Hopkins School of Medicine, Baltimore, Maryland, USA.

Toyomi Karberg (T)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

Gloria Harrington (G)

University of Michigan, Ann Arbor, Michigan, USA.

Petter Jakobsen (P)

NORMENT, Division of Psychiatry, Haukeland University Hospital, Bergen, Norway.
Department of Clinical Medicine, University of Bergen, Norway.

Masoud Kamali (M)

University of Michigan, Ann Arbor, Michigan, USA.

Marisa Kelly (M)

University of Michigan, Ann Arbor, Michigan, USA.

Susan G Leckband (SG)

Department of Psychiatry, VA San Diego Healthcare System, La Jolla, California, USA.

Falk Lohoff (F)

University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA.

Adam X Maihofer (AX)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.

Melvin G McInnis (MG)

University of Michigan, Ann Arbor, Michigan, USA.

Francis Mondimore (F)

Department of Psychiatry and Behavioral Sciences, The Johns Hopkins School of Medicine, Baltimore, Maryland, USA.

Gunnar Morken (G)

Division of Psychiatry, St. Olav University Hospital of Trondheim and Department of Neuroscience, Faculty of Medicine, Norwegian University of Science and Technology, Trondheim, Norway.

John I Nurnberger (JI)

Departments of Psychiatry and Medical and Molecular Genetics, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, Indiana, USA.

Ketil J Oedegaard (KJ)

NORMENT, Division of Psychiatry, Haukeland University Hospital, Bergen, Norway.
Department of Clinical Medicine, University of Bergen, Norway.

Megan Ritchey (M)

Department of Psychiatry and Behavioral Sciences, The Johns Hopkins School of Medicine, Baltimore, Maryland, USA.

Kelly Ryan (K)

University of Michigan, Ann Arbor, Michigan, USA.

Martha Schinagle (M)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

Helle Schoeyen (H)

Department of Clinical Medicine, University of Bergen, Norway.
Clinic of Adult Psychiatry, Stavanger University Hospital, Stavanger, Norway.

Candice Schwebel (C)

University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA.

Martha Shaw (M)

University of Chicago, Chicago, Illinois, USA.

Paul D Shilling (PD)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.

Claire Slaney (C)

Dalhousie University, Halifax, Canada.

Andrea Stautland (A)

Department of Clinical Medicine, University of Bergen, Norway.

Bruce Tarwater (B)

University of Iowa, Iowa City, Iowa, USA.

Joseph R Calabrese (JR)

Department of Psychiatry, Case Western Reserve University, Cleveland, Ohio, USA.

Martin Alda (M)

Dalhousie University, Halifax, Canada.

Caroline M Nievergelt (CM)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.

Peter P Zandi (PP)

Department of Psychiatry and Behavioral Sciences, The Johns Hopkins School of Medicine, Baltimore, Maryland, USA.

John R Kelsoe (JR)

Department of Psychiatry, University of California San Diego, La Jolla, California, USA.

Classifications MeSH