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Motor activity patterns can distinguish between interepisode bipolar disorder patients and healthy controls

Published online by Cambridge University Press:  04 September 2020

Jakub Schneider Open the ORCID record for Jakub Schneider [Opens in a new window] ,
Eduard Bakštein ,
Marian Kolenič ,
Pavel Vostatek ,
Christoph U. Correll ,
Daniel Novák  and
Filip Španiel
Jakub Schneider*
Affiliation:
Department of Cybernetics, Czech Technical University in Prague, Prague, Czech Republic Applied Neuroscience and Neuroimaging, National Institute of Mental Health, Klecany, Czech Republic
Eduard Bakštein
Affiliation:
Department of Cybernetics, Czech Technical University in Prague, Prague, Czech Republic Applied Neuroscience and Neuroimaging, National Institute of Mental Health, Klecany, Czech Republic
Marian Kolenič
Affiliation:
Applied Neuroscience and Neuroimaging, National Institute of Mental Health, Klecany, Czech Republic
Pavel Vostatek
Affiliation:
MINDPAX, Prague, Czech Republic
Christoph U. Correll
Affiliation:
Department of Psychiatry, The Zucker Hillside Hospital, Northwell Health, Glen Oaks, New York, USA Zucker School of Medicine at Hofstra/Northwell, Department of Psychiatry and Molecular Medicine, Hempstead, New York, USA The Feinstein Institute for Medical Research, Center for Psychiatric Neuroscience, Manhasset, New York, USA Department of Child and Adolescent Psychiatry, Charité Universitätsmedizin Berlin, Berlin, Germany
Daniel Novák
Affiliation:
Department of Cybernetics, Czech Technical University in Prague, Prague, Czech Republic
Filip Španiel
Affiliation:
Applied Neuroscience and Neuroimaging, National Institute of Mental Health, Klecany, Czech Republic
*
*Author for correspondence: Jakub Schneider, Email: schnejak@fel.cvut.cz
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Abstract

Background

Bipolar disorder (BD) is linked to circadian rhythm disruptions resulting in aberrant motor activity patterns. We aimed to explore whether motor activity alone, as assessed by longitudinal actigraphy, can be used to classify accurately BD patients and healthy controls (HCs) into their respective groups.

Methods

Ninety-day actigraphy records from 25 interepisode BD patients (ie, Montgomery–Asberg Depression Rating Scale (MADRS) and Young Mania Rating Scale (YMRS) < 15) and 25 sex- and age-matched HCs were used in order to identify latent actigraphic biomarkers capable of discriminating between BD patients and HCs. Mean values and time variations of a set of standard actigraphy features were analyzed and further validated using the random forest classifier.

Results

Using all actigraphy features, this method correctly assigned 88% (sensitivity = 85%, specificity = 91%) of BD patients and HCs to their respective group. The classification success may be confounded by differences in employment between BD patients and HCs. When motor activity features resistant to the employment status were used (the strongest feature being time variation of intradaily variability, Cohen’s d = 1.33), 79% of the subjects (sensitivity = 76%, specificity = 81%) were correctly classified.

Conclusion

A machine-learning actigraphy-based model was capable of distinguishing between interepisode BD patients and HCs solely on the basis of motor activity. The classification remained valid even when features influenced by employment status were omitted. The findings suggest that temporal variability of actigraphic parameters may provide discriminative power for differentiating between BD patients and HCs while being less affected by employment status.

Keywords

Bipolar disorderclassificationsleepcircadian rhythmactigraphy
Type
Original Research
Information
CNS Spectrums , Volume 27 , Issue 1 , February 2022 , pp. 82 - 92
Copyright
© The Author(s), 2020. Published by Cambridge University Press.

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References

Alloy, LB, Ng, TH, Titone, MK, Boland, EM. Circadian rhythm dysregulation in bipolar spectrum disorders. Curr Psychiatry Rep. 2017;19(4):21. doi:10.1007/s11920-017-0772-z.CrossRefGoogle ScholarPubMed
Murray, G, Harvey, A. Circadian rhythms and sleep in bipolar disorder. Bipolar Disord. 2010;12(5):459–472. doi:10.1111/j.1399-5618.2010.00843.x.CrossRefGoogle ScholarPubMed
Gold, A, Sylvia, L. The role of sleep in bipolar disorder. Nat Sci Sleep. 2016;8:207–214. doi:10.2147/NSS.S85754.CrossRefGoogle ScholarPubMed
Geoffroy, PA, Scott, J, Boudebesse, C, et al. Sleep in patients with remitted bipolar disorders: a meta-analysis of actigraphy studies. Acta Psychiatr Scand. 2015;131(2):89–99. doi:10.1111/acps.12367.CrossRefGoogle ScholarPubMed
Geoffroy, PA, Boudebesse, C, Bellivier, F, et al. Sleep in remitted bipolar disorder: a naturalistic case-control study using actigraphy. J Affect Disord. 2014;158:1–7. doi:10.1016/j.jad.2014.01.012.CrossRefGoogle ScholarPubMed
Millar, A, Espie, CA, Scott, J. The sleep of remitted bipolar outpatients: a controlled naturalistic study using actigraphy. J Affect Disord. 2004;80(2–3):145–153. doi:10.1016/S0165-0327(03)00055-7.CrossRefGoogle ScholarPubMed
St-Amand, J, Provencher, MD, Bélanger, L, Morin, CM. Sleep disturbances in bipolar disorder during remission. J Affect Disord. 2013;146(1):112–119. doi:10.1016/j.jad.2012.05.057.CrossRefGoogle ScholarPubMed
Gershon, A, Kaufmann, CN, Depp, CA, et al. Subjective versus objective evening chronotypes in bipolar disorder. J Affect Disord. 2018;225:342–349. doi:10.1016/j.jad.2017.08.055.CrossRefGoogle ScholarPubMed
Kaufmann, CN, Gershon, A, Depp, CA, Miller, S, Zeitzer, JM, Ketter, TA. Daytime midpoint as a digital biomarker for chronotype in bipolar disorder. J Affect Disord. 2018;241:586–591. doi:10.1016/j.jad.2018.08.032.CrossRefGoogle ScholarPubMed
Milhiet, V, Etain, B, Boudebesse, C, Bellivier, F. Circadian biomarkers, circadian genes and bipolar disorders. J Physiol. 2011;105(4–6):183–189. doi:10.1016/j.jphysparis.2011.07.002.Google ScholarPubMed
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. doi:10.1001/jamapsychiatry.2018.3546.CrossRefGoogle ScholarPubMed
Scott, J, Murray, G, Henry, C, et al. Activation in bipolar disorders. JAMA Psychiatry 2017;74(2):189. doi:10.1001/jamapsychiatry.2016.3459.CrossRefGoogle ScholarPubMed
Scott, J. Clinical parameters of circadian rhythms in affective disorders. Eur Neuropsychopharmacol. 2011;21(Suppl. 4):S671–S675. doi:10.1016/j.euroneuro.2011.07.006.CrossRefGoogle ScholarPubMed
Jones, SH, Hare, DJ, Evershed, K. Actigraphic assessment of circadian activity and sleep patterns in bipolar disorder. Bipolar Disord. 2005;7(2):176–186. doi:10.1111/j.1399-5618.2005.00187.x.CrossRefGoogle ScholarPubMed
Salvatore, P, Ghidini, S, Zita, G, et al. Circadian activity rhythm abnormalities in ill and recovered bipolar I disorder patients. Bipolar Disord. 2008;10(2):256–265. doi:10.1111/j.1399-5618.2007.00505.x.CrossRefGoogle ScholarPubMed
Harvey, AG, Schmidt, DA, Scarnà, A, Semler, CN, Goodwin, GM. Sleep-related functioning in euthymic patients with bipolar disorder, patients with insomnia, and subjects without sleep problems. Am J Psychiatry. 2005;162(1):50–57. doi:10.1176/appi.ajp.162.1.50.CrossRefGoogle ScholarPubMed
Gershon, A, Thompson, WK, Eidelman, P, McGlinchey, EL, Kaplan, KA, Harvey, AG. Restless pillow, ruffled mind: sleep and affect coupling in interepisode bipolar disorder. J Abnorm Psychol. 2012;121(4):863–873. doi:10.1037/a0028233.CrossRefGoogle ScholarPubMed
Ritter, PS, Marx, C, Lewtschenko, N, et al. The characteristics of sleep in patients with manifest bipolar disorder, subjects at high risk of developing the disease and healthy controls. J Neural Transm. 2012;119(10):1173–1184. doi:10.1007/s00702-012-0883-y.CrossRefGoogle ScholarPubMed
McKenna, BS, Drummond, SPA, Eyler, LT. Associations between circadian activity rhythms and functional brain abnormalities among euthymic bipolar patients: a preliminary study. J Affect Disord. 2014;164:101–106. doi:10.1016/j.jad.2014.04.034.CrossRefGoogle ScholarPubMed
Sebela, A, Kolenic, M, Farkova, E, Novak, T, Goetz, M. Decreased need for sleep as an endophenotype of bipolar disorder: an actigraphy study. Chronobiol Int. 2019;36(9):1227–1239. doi:10.1080/07420528.2019.1630631.CrossRefGoogle Scholar
Bei, B, Wiley, JF, Trinder, J, Manber, R. Beyond the mean: a systematic review on the correlates of daily intraindividual variability of sleep/wake patterns. Sleep Med Rev. 2016;28:108–124. doi:10.1016/j.smrv.2015.06.003CrossRefGoogle ScholarPubMed
Krane-Gartiser, K, Henriksen, TEG, Morken, G, Vaaler, A, Fasmer, OB. Actigraphic assessment of motor activity in acutely admitted inpatients with bipolar disorder. PLoS One. 2014;9(2). doi:10.1371/journal.pone.0089574.CrossRefGoogle ScholarPubMed
Mullin, BC, Harvey, AG, Hinshaw, SP. A preliminary study of sleep in adolescents with bipolar disorder, ADHD, and non-patient controls. Bipolar Disord. 2011;13(4):425–432. doi:10.1111/j.1399-5618.2011.00933.x.CrossRefGoogle ScholarPubMed
Faedda, GL, Ohashi, K, Hernandez, M, et al. Actigraph measures discriminate pediatric bipolar disorder from attention-deficit/hyperactivity disorder and typically developing controls. J Child Psychol Psychiatry Allied Discip. 2016;57(6):706–716. doi:10.1111/jcpp.12520.CrossRefGoogle ScholarPubMed
Krane-Gartiser, K, Scott, J, Nevoret, C, et al. Which actigraphic variables optimally characterize the sleep-wake cycle of individuals with bipolar disorders? Acta Psychiatr Scand. 2019;139(3):0–2. doi:10.1111/acps.13003.CrossRefGoogle ScholarPubMed
Janney, CA, Fagiolini, A, Swartz, HA, Jakicic, JM, Holleman, RG, Richardson, CR. Are adults with bipolar disorder active? Objectively measured physical activity and sedentary behavior using accelerometry. J Affect Disord. 2014;152 –154(1):498–504. doi:10.1016/j.jad.2013.09.009.CrossRefGoogle ScholarPubMed
Gonçalves, BSB, Adamowicz, T, Louzada, FM, Moreno, CR, Araujo, JF. A fresh look at the use of nonparametric analysis in actimetry. Sleep Med Rev. 2015;20:84–91. doi:10.1016/j.smrv.2014.06.002.CrossRefGoogle Scholar
Gonzalez, R, Suppes, T, Zeitzer, J, et al. The association between mood state and chronobiological characteristics in bipolar I disorder: a naturalistic, variable cluster analysis-based study. Int J Bipolar Disord. 2018;6(1):5. doi:10.1186/s40345-017-0113-5.CrossRefGoogle ScholarPubMed
De Crescenzo, F, Economou, A, Sharpley, AL, Gormez, A, Quested, DJ. Actigraphic features of bipolar disorder: a systematic review and meta-analysis. Sleep Med Rev. 2017;33:58–69. doi:10.1016/j.smrv.2016.05.003.CrossRefGoogle ScholarPubMed
Ng, TH, Chung, KF, Ho, FYY, Yeung, WF, Yung, KP, Lam, TH. Sleep-wake disturbance in interepisode bipolar disorder and high-risk individuals: a systematic review and meta-analysis. Sleep Med Rev. 2015;20:46–58. doi:10.1016/j.smrv.2014.06.006.CrossRefGoogle ScholarPubMed
Kaplan, KA, Talbot, LS, Gruber, J, Harvey, AG. Evaluating sleep in bipolar disorder: comparison between actigraphy, polysomnography, and sleep diary. Bipolar Disord. 2012;14(8):870–879. doi:10.1111/bdi.12021.CrossRefGoogle ScholarPubMed
Montgomery, SA, Åsberg, M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134(4):382–389. doi:10.1192/bjp.134.4.382.CrossRefGoogle ScholarPubMed
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry. 1978;133(5):429–435. doi:10.1192/bjp.133.5.429.CrossRefGoogle ScholarPubMed
APA. Diagnostic and Statistical Manual of Mental Disorders : DSM-5. Arlington, VA, Washington, DC: American Psychiatric Association; 2013.Google Scholar
Tohen, M, Frank, E, Bowden, CL, et al. The International Society For Bipolar Disorders (ISBD) task force report on the nomenclature of course and outcome in bipolar disorders. Bipolar Disord. 2009;11(5):453–473. doi:10.1111/j.1399-5618.2009.00726.x.CrossRefGoogle ScholarPubMed
Lecrubier, Y, Sheehan, D, Weiller, E, et al. The mini international neuropsychiatric interview (mini). a short diagnostic structured interview: reliability and validity according to the CIDI. Eur Psychiatry. 1997;12(5):224–231. doi:10.1016/S0924-9338(97)83296-8.CrossRefGoogle Scholar
Macfadden, W, Alphs, L, Haskins, JT, et al. A randomized, double-blind, placebo-controlled study of maintenance treatment with adjunctive risperidone long-acting therapy in patients with bipolar I disorder who relapse frequently. Bipolar Disord. 2009;11(8):827–839. doi:10.1111/j.1399-5618.2009.00761.x.CrossRefGoogle ScholarPubMed
Juda, M, Vetter, C, Roenneberg, T. The Munich chronotype questionnaire for shift-workers (MCTQShift). J Biol Rhythm. 2013;28(2):130–140. doi:10.1177/0748730412475041.CrossRefGoogle Scholar
Cornelissen, G. Cosinor-based rhythmometry. Theor Biol Med Model. 2014;11(1):16. doi:10.1186/1742-4682-11-16.CrossRefGoogle ScholarPubMed
Witting, W, Kwa, IH, Eikelenboom, P, Mirmiran, M, Swaab, DF. Alterations in the circadian rest-activity rhythm in aging and Alzheimer’s disease. Biol Psychiatry. 1990;27(6):563–572. doi:10.1016/0006-3223(90)90523-5.CrossRefGoogle ScholarPubMed
Vostatek, P. Mindpax sleep classification. Mindpax White-papers. 2018;1–6. https://www.mindpax.me/assets/docs/Validation_study_appendix.pdf.Google Scholar
Boudebesse, C, Leboyer, M, Begley, A, et al. Comparison of five actigraphy scoring methods with bipolar disorder. Behav Sleep Med. 2013;11(4):275–282. doi:10.1080/15402002.2012.685997.CrossRefGoogle ScholarPubMed
Kosmadopoulos, A, Sargent, C, Darwent, D, Zhou, X, Roach, GD. Alternatives to polysomnography (PSG): a validation of wrist actigraphy and a partial-PSG system. Behav Res Methods 2014;46(4):1032–1041. doi:10.3758/s13428-013-0438-7.CrossRefGoogle Scholar
Santisteban, JA, Brown, TG, Gruber, R. Association between the Munich chronotype questionnaire and wrist actigraphy. Sleep Disord. 2018;2018:1–7. doi:10.1155/2018/5646848.CrossRefGoogle ScholarPubMed
Holm, S. Board of the Foundation of the Scandinavian Journal of Statistics. A simple sequentially rejective multiple test procedure. Scand J Stat. 1979;6(2):65–70.Google Scholar
Breiman, L. Random Forests. Berkley, VA: Statistics Department University of California; 2001:1–33. doi:10.1023/A:1010933404324.Google Scholar
Roenneberg, T, Kuehnle, T, Juda, M, et al. Epidemiology of the human circadian clock. Sleep Med Rev. 2007;11(6):429–438. doi:10.1016/j.smrv.2007.07.005.CrossRefGoogle ScholarPubMed
Ortiz, A, Bradler, K, Hintze, A. Episode forecasting in bipolar disorder: is energy better than mood? Bipolar Disord. (2018);20:470–476. doi:10.1111/bdi.12603.CrossRefGoogle Scholar
Bullock, B, Murray, G. Reduced amplitude of the 24 hour activity rhythm. Clin Psychol Sci. 2014;2(1):86–96. doi:10.1177/2167702613490158.CrossRefGoogle Scholar
Gershon, A, Ram, N, Johnson, SL, Harvey, AG, Zeitzer, JM. Daily actigraphy profiles distinguish depressive and interepisode states in bipolar disorder. Clin Psychol Sci. 2016;4(4):641–650. doi:10.1177/2167702615604613.CrossRefGoogle ScholarPubMed
Shou, H, Cui, L, Hickie, I, et al. Dysregulation of objectively assessed 24-hour motor activity patterns as a potential marker for bipolar I disorder: results of a community-based family study. Transl Psychiatry. 2017;7(8):e1211. doi:10.1038/tp.2017.136.CrossRefGoogle ScholarPubMed
Carr, O, Saunders, KEA, Tsanas, A, et al. Variability in phase and amplitude of diurnal rhythms is related to variation of mood in bipolar and borderline personality disorder. Sci Rep. 2018;8(1):1–11. doi:10.1038/s41598-018-19888-9.CrossRefGoogle ScholarPubMed
Grierson, AB, Hickie, IB, Naismith, SL, Hermens, DF, Scott, EM, Scott, J. Circadian rhythmicity in emerging mood disorders: state or trait marker? Int J Bipolar Disord. 2016;4(1):3. doi:10.1186/s40345-015-0043-z.CrossRefGoogle ScholarPubMed
Judd, LL. The long-term natural history of the weekly symptomatic status of bipolar I disorder. Arch Gen Psychiatry. 2002;59(6):530–537. doi:10.1001/archpsyc.59.6.530.CrossRefGoogle ScholarPubMed
Monti, JM. The effect of second-generation antipsychotic drugs on sleep parameters in patients with unipolar or bipolar disorder. Sleep Med. 2016;23:89–96. doi:10.1016/j.sleep.2016.04.020.CrossRefGoogle ScholarPubMed
Hwang, JY, Choi, JW, Kang, SG, Hwang, SH, Kim, SJ, Lee, YJ. Comparison of the effects of quetiapine XR and lithium monotherapy on actigraphy-measured circadian parameters in patients with bipolar II depression. J Clin Psychopharmacol. 2017;37(3):351–354. doi:10.1097/JCP.0000000000000699.CrossRefGoogle ScholarPubMed
Hossain, S, Mainali, P, Bhimanadham, NN, Imran, S, Ahmad, N, Patel, RS. Medical and psychiatric comorbidities in bipolar disorder: insights from national inpatient population-based study. Cureus. 2019;11(9):e5636. doi:10.7759/cureus.5636.Google ScholarPubMed
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