Correlation of Circadian Rhythms and Improvement of Depressive Symptoms in Acute Ischemic Stroke Patients


Cite item

Full Text

Abstract

Objectives::To investigate the correlation between evening melatonin timing secretion, dim light melatonin onset (DLMO), and post-stroke depression (PSD) in acute ischemic stroke patients and their influence on the improvement of depressive symptoms.

Materials and Methods::120 patients with a recent magnetic resonance imaging confirmed stroke were included. Salivary melatonin samples were collected at 5 time points within 1 week after hospitalization (7 p.m.-11 p.m., 1 sample per hour). The circadian phase was defined by calculating DLMO secretion. Post-stroke depressive symptoms were evaluated by the 17-item Hamilton Rating Scale for Depression (HRSD) both on day 7 of hospitalization and 3 months after stroke. Patients were divided into PSD and non-PSD groups based on whether the acute phase HRSD score was ≥8. Similarly, patients were divided into the improved depressive symptoms (IDS) and no improvement in depressive symptoms (non-IDS) groups based on whether the HRSD score at 3 months was lower than at baseline. Neurological recovery at 3 months was assessed using the modified Rankin Scale (mRS).

Results::The difference in DLMO between PSD and non-PSD patients was not statistically significant (p =0.173). In the non-IDS group, there was a significant decrease in melatonin secretion at 10 p.m. (p =0.012), and DLMO was significantly later than in the IDS group (p =0.017). Logistic regression analysis showed that DLMO (OR 1.91, 95%CI:1.13-3.23, p = 0.016) was an independent risk factor for persistent no improvement in depressive symptoms, which was associated with a markedly worse prognosis (p (<0.001).

Conclusion::Our findings suggest possible interventions for the very early identification of non- IDS patients.

About the authors

Yue Ding

Department of Neurology, The Second Affiliated Hospital of Soochow University

Email: info@benthamscience.net

Shengnan Chen

Department of Neurology, The Second Affiliated Hospital of Soochow University

Email: info@benthamscience.net

Qian Sun

Department of Neurology,, The Second Affiliated Hospital of Soochow University,

Email: info@benthamscience.net

Fei Han

Department of Neurology, The Second Affiliated Hospital of Soochow University

Email: info@benthamscience.net

Rui Chen

Department of Respiratory Medicine, The Second Affiliated Hospital of Soochow University

Email: info@benthamscience.net

Jie Li

Department of Neurology, The Second Affiliated Hospital of Soochow University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Villa RF, Ferrari F, Moretti A. Post-stroke depression: Mechanisms and pharmacological treatment. Pharmacol Ther 2018; 184: 131-44. doi: 10.1016/j.pharmthera.2017.11.005 PMID: 29128343
  2. Guo J, Wang J, Sun W, Liu X. The advances of post-stroke depression: 2021 update. J Neurol 2022; 269(3): 1236-49. doi: 10.1007/s00415-021-10597-4 PMID: 34052887
  3. Sun S, Li Z, Xiao Q, Tan S, Hu B, Jin H. An updated review on prediction and preventive treatment of post-stroke depression. Expert Rev Neurother 2023; 23(8): 721-39. doi: 10.1080/14737175.2023.2234081 PMID: 37427452
  4. Wang Y, Liao X, Wang C, et al. Impairment of cognition and sleep after acute ischaemic stroke or transient ischaemic attack in Chinese patients: Design, rationale and baseline patient characteristics of a nationwide multicentre prospective registry. Stroke Vasc Neurol 2021; 6(1): 139-44. doi: 10.1136/svn-2020-000359 PMID: 32665365
  5. Ruan W, Yuan X, Eltzschig HK. Circadian rhythm as a therapeutic target. Nat Rev Drug Discov 2021; 20(4): 287-307. doi: 10.1038/s41573-020-00109-w PMID: 33589815
  6. Adamczak-Ratajczak A, Kupsz J, Owecki M, et al. Circadian rhythms of melatonin and cortisol in manifest Huntington’s disease and in acute cortical ischemic stroke. J Physiol Pharmacol 2017; 68(4): 539-46. PMID: 29151070
  7. Tonon AC, Constantino DB, Amando GR, et al. Sleep disturbances, circadian activity, and nocturnal light exposure characterize high risk for and current depression in adolescence. Sleep 2022; 45(7): zsac104. doi: 10.1093/sleep/zsac104 PMID: 35522984
  8. Mondin TC, Cardoso TA, Souza LDM, et al. Mood disorders and biological rhythms in young adults: A large population-based study. J Psychiatr Res 2017; 84: 98-104. doi: 10.1016/j.jpsychires.2016.09.030 PMID: 27716514
  9. Melo MCA, Abreu RLC, Linhares Neto VB, de Bruin PFC, de Bruin VMS. Chronotype and circadian rhythm in bipolar disorder: A systematic review. Sleep Med Rev 2017; 34: 46-58. doi: 10.1016/j.smrv.2016.06.007 PMID: 27524206
  10. de Leeuw M, Verhoeve SI, van der Wee NJA, van Hemert AM, Vreugdenhil E, Coomans CP. The role of the circadian system in the etiology of depression. Neurosci Biobehav Rev 2023; 153: 105383. doi: 10.1016/j.neubiorev.2023.105383 PMID: 37678570
  11. Aggestrup AS, Svendsen SD, Præstegaard A, Løventoft P, Nørregaard L, Knorr UB, et al. Circadian reinforcement therapy in combination with electronic self-monitoring facilitates a safe post-discharge period for patients with major depression. JMIR Ment Health 2023; 19(1): 124. doi: 10.2196/50072 PMID: 37800194
  12. Yu SY, Sun Q, Chen S, et al. Circadian rhythm disturbance in acute ischemic stroke patients and its effect on prognosis. Cerebrovasc Dis 2023; 1-14. doi: 10.1159/000528724 PMID: 37423205
  13. Keijzer H, Smits MG, Peeters T, Looman CWN, Endenburg SC, Gunnewiek JMTK. Evaluation of salivary melatonin measurements for dim light melatonin onset calculations in patients with possible sleep-wake rhythm disorders. Clin Chim Acta 2011; 412(17-18): 1616-20. doi: 10.1016/j.cca.2011.05.014 PMID: 21601566
  14. Pandi-Perumal SR, Smits M, Spence W, et al. Dim light melatonin onset (DLMO): A tool for the analysis of circadian phase in human sleep and chronobiological disorders. Prog Neuropsychopharmacol Biol Psychiatry 2007; 31(1): 1-11. doi: 10.1016/j.pnpbp.2006.06.020 PMID: 16884842
  15. Rahman SA, Kayumov L, Tchmoutina EA, Shapiro CM. Clinical efficacy of dim light melatonin onset testing in diagnosing delayed sleep phase syndrome. Sleep Med 2009; 10(5): 549-55. doi: 10.1016/j.sleep.2008.03.020 PMID: 18725185
  16. Leibenluft E, Feldman-Naim S, Turner EH, Schwartz PJ, Wehr TA. Salivary and plasma measures of dim light melatonin onset (DLMO) in patients with rapid cycling bipolar disorder. Biol Psychiatry 1996; 40(8): 731-5. doi: 10.1016/0006-3223(95)00488-2 PMID: 8894065
  17. Gibbons RD, Clark DC, Kupfer DJ. Exactly what does the Hamilton depression rating scale measure? J Psychiatr Res 1993; 27(3): 259-73. doi: 10.1016/0022-3956(93)90037-3 PMID: 8295158
  18. Nasreddine ZS, Phillips NA, Bédirian V, et al. The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005; 53(4): 695-9. doi: 10.1111/j.1532-5415.2005.53221.x PMID: 15817019
  19. Buysse DJ, Reynolds CF III, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Res 1989; 28(2): 193-213. doi: 10.1016/0165-1781(89)90047-4 PMID: 2748771
  20. Manni R, Cremascoli R, Perretti C, et al. Evening melatonin timing secretion in real life conditions in patients with Alzheimer disease of mild to moderate severity. Sleep Med 2019; 63: 122-6. doi: 10.1016/j.sleep.2019.04.018 PMID: 31622953
  21. Duarte Faria A, Cardoso TA, Campos Mondin T, et al. Biological rhythms in bipolar and depressive disorders: A community study with drug-naïve young adults. J Affect Disord 2015; 186: 145-8. doi: 10.1016/j.jad.2015.07.004 PMID: 26241662
  22. Kwah LK, Diong J. National Institutes of Health Stroke Scale (NIHSS). J Physiother 2014; 60(1): 61. doi: 10.1016/j.jphys.2013.12.012 PMID: 24856948
  23. Broderick JP, Adeoye O, Elm J. Evolution of the modified rankin scale and its use in future stroke trials. Stroke 2017; 48(7): 2007-12. doi: 10.1161/STROKEAHA.117.017866 PMID: 28626052
  24. Cosin C, Sibon I, Poli M, et al. Circadian sleep/wake rhythm abnormalities as a risk factor of a poststroke apathy. Int J Stroke 2015; 10(5): 710-5. doi: 10.1111/ijs.12433 PMID: 25545189
  25. Fang H, Tu S, Sheng J, Shao A. Depression in sleep disturbance: A review on a bidirectional relationship, mechanisms and treatment. J Cell Mol Med 2019; 23(4): 2324-32. doi: 10.1111/jcmm.14170 PMID: 30734486
  26. Howell SN, Griesbach GS. Sleep-wake disturbances in supra-and infratentorial stroke: an analysis of post-acute sleep architecture and apnea. Sleep Med 2021; 88: 81-6. doi: 10.1016/j.sleep.2021.10.013 PMID: 34740169
  27. Cai H, Wang XP, Yang GY. Sleep disorders in stroke: An update on management. Aging Dis 2021; 12(2): 570-85. doi: 10.14336/AD.2020.0707 PMID: 33815883
  28. Dong L, Brown DL, Chervin RD, Case E, Morgenstern LB, Lisabeth LD. Pre-stroke sleep duration and post-stroke depression. Sleep Med 2021; 77: 325-9. doi: 10.1016/j.sleep.2020.04.025 PMID: 32828696
  29. Liu F, Yang Y, Wang S, et al. Impact of sleep duration on depression and anxiety after acute ischemic stroke. Front Neurol 2021; 12: 630638. doi: 10.3389/fneur.2021.630638 PMID: 33841304
  30. Itani O, Jike M, Watanabe N, Kaneita Y. Short sleep duration and health outcomes: A systematic review, meta-analysis, and meta-regression. Sleep Med 2017; 32: 246-56. doi: 10.1016/j.sleep.2016.08.006 PMID: 27743803
  31. Koo DL, Nam H, Thomas RJ, Yun CH. Sleep disturbances as a risk factor for stroke. J Stroke 2018; 20(1): 12-32. doi: 10.5853/jos.2017.02887 PMID: 29402071
  32. Zhao F, Yue Y, Li L, et al. Clinical practice guidelines for post-stroke depression in China. Rev Bras Psiquiatr 2018; 40(3): 325-34. doi: 10.1590/1516-4446-2017-2343 PMID: 29412338
  33. Meng H, Liu T, Borjigin J, Wang MM. Ischemic stroke destabilizes circadian rhythms. J Circadian Rhythms 2008; 6(0): 9. doi: 10.1186/1740-3391-6-9 PMID: 18922153
  34. Voultsios A, Kennaway DJ, Dawson D. Salivary melatonin as a circadian phase marker: Validation and comparison to plasma melatonin. J Biol Rhythms 1997; 12(5): 457-66. doi: 10.1177/074873049701200507 PMID: 9376644
  35. Sun W, Miao J, Song Y, et al. Systemic low-grade inflammation and depressive symptomology at chronic phase of ischemic stroke: The chain mediating role of fibrinogen and neutrophil counts. Brain Behav Immun 2022; 100: 332-41. doi: 10.1016/j.bbi.2021.10.011 PMID: 34728390
  36. Pawluk H, Kołodziejska R, Grześk G. Increased oxidative stress markers in acute ischemic stroke patients treated with thrombolytics. Int J Mol Sci 2022; 23(24): 15625. doi: 10.3390/ijms232415625 PMID: 36555265
  37. Sletten TL, Magee M, Murray JM, et al. Efficacy of melatonin with behavioural sleep-wake scheduling for delayed sleep-wake phase disorder: A double-blind, randomised clinical trial. PLoS Med 2018; 15(6): e1002587. doi: 10.1371/journal.pmed.1002587 PMID: 29912983
  38. Yawoot N, Govitrapong P, Tocharus C, Tocharus J. Ischemic stroke, obesity, and the anti‐inflammatory role of melatonin. Biofactors 2021; 47(1): 41-58. doi: 10.1002/biof.1690 PMID: 33135223
  39. Yao D, Li R, Hao J, et al. Melatonin alleviates depression-like behaviors and cognitive dysfunction in mice by regulating the circadian rhythm of AQP4 polarization. Transl Psychiatry 2023; 13(1): 310. doi: 10.1038/s41398-023-02614-z PMID: 37802998
  40. Gunata M, Parlakpinar H, Acet HA. Melatonin: A review of its potential functions and effects on neurological diseases. Rev Neurol 2020; 176(3): 148-65. doi: 10.1016/j.neurol.2019.07.025 PMID: 31718830
  41. Maiese K. Cognitive impairment and dementia: Gaining insight through circadian clock gene pathways. Biomolecules 2021; 11(7): 1002. doi: 10.3390/biom11071002 PMID: 34356626
  42. Vasey C, McBride J, Penta K. Circadian rhythm dysregulation and restoration: The role of melatonin. Nutrients 2021; 13(10): 3480. doi: 10.3390/nu13103480 PMID: 34684482
  43. Robinson RG, Price TR. Post-stroke depressive disorders: A follow-up study of 103 patients. Stroke 1982; 13(5): 635-41. doi: 10.1161/01.STR.13.5.635 PMID: 7123596
  44. Vataja R, Pohjasvaara T, Leppävuori A, et al. Magnetic resonance imaging correlates of depression after ischemic stroke. Arch Gen Psychiatry 2001; 58(10): 925-31. doi: 10.1001/archpsyc.58.10.925 PMID: 11576030

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers