Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-02T18:48:59.024Z Has data issue: false hasContentIssue false
  • English
  • Français

Fractal biomarker of activity in patients with bipolar disorder

Published online by Cambridge University Press:  01 April 2020

Stefan E. Knapen Open the ORCID record for Stefan E. Knapen [Opens in a new window] ,
Peng Li ,
Rixt F. Riemersma-van der Lek ,
Sanne Verkooijen ,
Marco P. M. Boks ,
Robert A. Schoevers ,
Frank A. J. L. Scheer  and
Kun Hu
Stefan E. Knapen*
Affiliation:
Department of Psychiatry, University of Groningen, University Medical Center Groningen, Research School of Behavioural and Cognitive Neurosciences (BCN), Interdisciplinary Center Psychopathology and Emotion regulation (ICPE), Groningen, The Netherlands Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, Massachusetts, USA Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts, USA
Peng Li
Affiliation:
Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, Massachusetts, USA Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts, USA
Rixt F. Riemersma-van der Lek
Affiliation:
Department of Psychiatry, University of Groningen, University Medical Center Groningen, Research School of Behavioural and Cognitive Neurosciences (BCN), Interdisciplinary Center Psychopathology and Emotion regulation (ICPE), Groningen, The Netherlands
Sanne Verkooijen
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
Marco P. M. Boks
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
Robert A. Schoevers
Affiliation:
Department of Psychiatry, University of Groningen, University Medical Center Groningen, Research School of Behavioural and Cognitive Neurosciences (BCN), Interdisciplinary Center Psychopathology and Emotion regulation (ICPE), Groningen, The Netherlands
Frank A. J. L. Scheer
Affiliation:
Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, Massachusetts, USA Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts, USA
Kun Hu
Affiliation:
Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, Massachusetts, USA Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts, USA
*
Author for correspondence: Stefan E. Knapen, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

The output of many healthy physiological systems displays fractal fluctuations with self-similar temporal structures. Altered fractal patterns are associated with pathological conditions. There is evidence that patients with bipolar disorder have altered daily behaviors.

Methods

To test whether fractal patterns in motor activity are altered in patients with bipolar disorder, we analyzed 2-week actigraphy data collected from 106 patients with bipolar disorder type I in a euthymic state, 73 unaffected siblings of patients, and 76 controls. To examine the link between fractal patterns and symptoms, we analyzed 180-day actigraphy and mood symptom data that were simultaneously collected from 14 patients.

Results

Compared to controls, patients showed excessive regularity in motor activity fluctuations at small time scales (<1.5 h) as quantified by a larger scaling exponent (α1 > 1), indicating a more rigid motor control system. α1 values of siblings were between those of patients and controls. Further examinations revealed that the group differences in α1 were only significant in females. Sex also affected the group differences in fractal patterns at larger time scales (>2 h) as quantified by scaling exponent α2. Specifically, female patients and siblings had a smaller α2 compared to female controls, indicating more random activity fluctuations; while male patients had a larger α2 compared to male controls. Interestingly, a higher weekly depression score was associated with a lower α1 in the subsequent week.

Conclusions

Our results show sex- and scale-dependent alterations in fractal activity regulation in patients with bipolar disorder. The mechanisms underlying the alterations are yet to be determined.

Keywords

Actigraphybipolar disorderfractal patternsmood disorderscale invariancesleep–wake rhythm
Type
Original Articles
Information
Psychological Medicine , Volume 51 , Issue 9 , July 2021 , pp. 1562 - 1569
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Shared senior authorship.

References

Aan het Rot, M., Hogenelst, K., & Schoevers, R. A. (2012). Mood disorders in everyday life: A systematic review of experience sampling and ecological momentary assessment studies. Clinical Psychology Review, 32, 510–523.CrossRefGoogle ScholarPubMed
Altman, E. G., Hedeker, D., Peterson, J. L., & Davis, J. M. (1997). The Altman Self-Rating Mania Scale. Biological psychiatry, 42, 948–955.CrossRefGoogle ScholarPubMed
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders: DSM-IV-TR®. Arlington County, Virginia, US: American Psychiatric Pub.Google Scholar
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5 ®). Arlington County, Virginia, US: American Psychiatric Pub.Google Scholar
Aybek, S., Ionescu, A., Berney, A., Chocron, O., Aminian, K., & Vingerhoets, F. J. G. (2012). Fractal temporal organisation of motricity is altered in major depression. Psychiatry Research, 200, 288–293.CrossRefGoogle ScholarPubMed
Baldessarini, R. J., Tondo, L., Baethge, C. J., Lepri, B., & Bratti, I. M. (2007). Effects of treatment latency on response to maintenance treatment in manic-depressive disorders. Bipolar Disorders, 9, 386–393.CrossRefGoogle ScholarPubMed
Born, C., Amann, B. L., Grunze, H., Post, R. M., & Schärer, L. (2014). Saving time and money: A validation of the self ratings on the prospective NIMH Life-Chart Method (NIMH-LCM). BMC Psychiatry, 14, 130.CrossRefGoogle Scholar
Bos, F. M., Schoevers, R. A., & aan het Rot, M. (2015). Experience sampling and ecological momentary assessment studies in psychopharmacology: A systematic review. European Neuropsychopharmacology, 25, 1853–1864.CrossRefGoogle ScholarPubMed
Bradley, A. J., Webb-Mitchell, R., Hazu, A., Slater, N., Middleton, B., Gallagher, P., … Anderson, K. N. (2017). Sleep and circadian rhythm disturbance in bipolar disorder. Psychological Medicine, 47, 1678–1689.CrossRefGoogle ScholarPubMed
Duffy, J. F., Cain, S. W., Chang, A.-M., Phillips, A. J. K., Munch, M. Y., Gronfier, C., … Czeisler, C. A. (2011). Sex difference in the near-24-hour intrinsic period of the human circadian timing system. Proceedings of the National Academy of Sciences, 108, 15602–15608.CrossRefGoogle ScholarPubMed
First, M. B., & Gibbon, M. (2004). The Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I) and the Structured Clinical Interview for DSM-IV Axis II Disorders (SCID-II). New York.: John Wiley & Sons Inc.Google Scholar
Goldberger, A. L., Amaral, L. A. N., Hausdorff, J. M., Ivanov, P. C., Peng, C., & Stanley, H. E. (2002). Fractal dynamics in physiology: Alterations with disease and aging. Proceedings of the national academy of sciences, 99, 2466–2472.CrossRefGoogle ScholarPubMed
Gould, T. D., & Manji, H. K. (2002). The Wnt signaling pathway in bipolar disorder. The Neuroscientist, 8, 497–511.CrossRefGoogle ScholarPubMed
Harvey, A. G. (2008). Sleep and circadian rhythms in bipolar disorder: Seeking synchrony, harmony, and regulation. The American Journal of Psychiatry, 165, 820–829.CrossRefGoogle ScholarPubMed
Hausdorff, J. M., Mitchell, S. L., Firtion, R., Peng, C. K., Cudkowicz, M. E., Wei, J. Y., & Goldberger, A. L. (1997). Altered fractal dynamics of gait: Reduced stride-interval correlations with aging and Huntington's disease. Journal of Applied Physiology (Bethesda, MD.: 1985), 82, 262–269.CrossRefGoogle ScholarPubMed
Hu, K., Harper, D. G., Shea, S. A., Stopa, E. G., & Scheer, F. A. J. L. (2013). Noninvasive fractal biomarker of clock neurotransmitter disturbance in humans with dementia. Scientific Reports, 3, 1–7.CrossRefGoogle ScholarPubMed
Hu, K., Ivanov, P. C., Chen, Z., Carpena, P., & Stanley, H. E. (2001). Effect of trends on detrended fluctuation analysis. Physical Review E, 64, 011114.CrossRefGoogle ScholarPubMed
Hu, K., Ivanov, P. C., Chen, Z., Hilton, M. F., Stanley, H. E., & Shea, S. A. (2004). Non-random fluctuations and multi-scale dynamics regulation of human activity. Physica A: Statistical Mechanics and its Applications, 337, 307–318.CrossRefGoogle ScholarPubMed
Hu, K., Riemersma-van der Lek, R. F., Patxot, M., Li, P., Shea, S. A., Scheer, F. A., & Van Someren, E. J. (2016). Progression of dementia assessed by temporal correlations of physical activity: Results from a 3.5-year, longitudinal randomized controlled trial. Scientific Reports, 6, 27742.CrossRefGoogle ScholarPubMed
Hu, K., Scheer, F. A. J. L., Ivanov, P. C., Buijs, R. M., & Shea, S. A. (2007). The suprachiasmatic nucleus functions beyond circadian rhythm generation. Neuroscience, 149, 508–517.CrossRefGoogle ScholarPubMed
Hu, K., Van Someren, E. J. W., Shea, S. A., & Scheer, F. A. J. L. (2009). Reduction of scale invariance of activity fluctuations with aging and Alzheimer’ s disease: Involvement of the circadian pacemaker. PNAS, 106, 2490–2494.CrossRefGoogle Scholar
Indic, P., Salvatore, P., Maggini, C., Ghidini, S., Ferraro, G., Ross, J., & Murray, G. (2011). Scaling behavior of human locomotor activity amplitude: Association with bipolar disorder. PloS one, 6, e20650.CrossRefGoogle ScholarPubMed
Kaplan, K. A., Talbot, L. S., Gruber, J., & Harvey, A. G. (2012). Evaluating sleep in bipolar disorder: Comparison between actigraphy, polysomnography, and sleep diary. Bipolar Disorders, 14, 870–879.CrossRefGoogle ScholarPubMed
Li, P., Lim, A. S. P., Gao, L., Hu, C., Yu, L., Bennett, D. A., … Hu, K. (2019). More random motor activity fluctuations predict incident frailty, disability, and mortality. 1977, 1–10.Google Scholar
Li, P., Morris, C. J., Patxot, M., Yugay, T., Mistretta, J., Purvis, T. E., … Hu, K. (2017). Reduced tolerance to night shift in chronic shift workers: Insight from fractal regulation. Sleep, 40, zsx092.CrossRefGoogle ScholarPubMed
Li, P., Yu, L., Lim, A. S. P., Buchman, A. S., Scheer, F. A. J. L., Shea, S. A., … Hu, K. (2018). Fractal regulation and incident Alzheimer’ s disease in elderly individuals. Alzheimer's & Dementia, 14, 1114–1125.CrossRefGoogle Scholar
Lim, A. S. P., Myers, A. J., Yu, L., Buchman, A. S., Duffy, J. F., De Jager, P. L., & Bennett, D. A. (2013). Sex difference in daily rhythms of clock gene expression in the aged human cerebral cortex. Journal of Biological Rhythms, 28, 117–129.CrossRefGoogle ScholarPubMed
Milhiet, V., Etain, B., Boudebesse, C., & Bellivier, F. (2011). Circadian biomarkers, circadian genes and bipolar disorders. Journal of Physiology, Paris, 105, 183–189.CrossRefGoogle ScholarPubMed
Murray, C. J. L., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. D., Michaud, C., … Aboyans, V. (2012). Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: A systematic analysis for the Global Burden of Disease Study 2010. The Lancet, 380, 2197–2223.CrossRefGoogle ScholarPubMed
Nicholas, J., Boydell, K., & Christensen, H. (2017). Beyond symptom monitoring: Consumer needs for bipolar disorder self-management using smartphones. European Psychiatry, 44, 210–216.CrossRefGoogle ScholarPubMed
Peng, C. K., Buldyrev, S.V., Havlin, S., Simons, M., Stanley, H. E., & Goldberger, A. L. (1994). Mosaic organization of DNA nucleotides. Physical Review. E, Statistical Physics, Plasmas, Fluids, and Related Interdisciplinary Topics, 49, 1685–1689.CrossRefGoogle ScholarPubMed
Peng, C. K., Havlin, S., Hausdorff, J. M., Mietus, J. E., Stanley, H. E., & Goldberger, A. L. (1995). Fractal mechanisms and heart rate dynamics. Long-range correlations and their breakdown with disease. Journal of Electrocardiology 28(Suppl), 59–65.CrossRefGoogle ScholarPubMed
Peng, C. K., Mietus, J. E., Liu, Y., Lee, C., Hausdorff, J. M., Stanley, H. E., … Lipsitz, L. A. (2002). Quantifying fractal dynamics of human respiration: Age and gender effects. Annals of Biomedical Engineering, 30, 683–692.CrossRefGoogle ScholarPubMed
Phillips, M. L., & Kupfer, D. J. (2013). Bipolar disorder 2 bipolar disorder diagnosis: Challenges and future directions. The Lancet, 381, 1663–1671.CrossRefGoogle Scholar
Pittman-Polletta, B. R., Scheer, F. A. J. L., Butler, M. P., Shea, S. A., & Hu, K. (2013). The role of the circadian system in fractal neurophysiological control. Biological Reviews, 88, 873–894.CrossRefGoogle ScholarPubMed
Rush, A. J., Carmody, T., & Reimitz, P. (2000). The Inventory of Depressive Symptomatology (IDS): Clinician (IDS-C) and Self-Report (IDS-SR) ratings of depressive symptoms. International Journal of Methods in Psychiatric Research, 9, 45–59.CrossRefGoogle Scholar
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (MINI): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59, 22–33.Google ScholarPubMed
Swanson, L. M., Burgess, H. J., Huntley, E. D., Bertram, H., Mooney, A., Zollars, J., … Arnedt, J. T. (2017). Relationships between circadian measures, depression, and response to antidepressant treatment: A preliminary investigation. 252, 262–269.Google ScholarPubMed
Van Bergen, A. H., Verkooijen, S., Vreeker, A., Abramovic, L., Hillegers, M. H., Spijker, A. T., … Boks, M. P. M. (2018). The characteristics of psychotic features in bipolar disorder. Psychological Medicine, 49, 2036–2048.CrossRefGoogle ScholarPubMed
Van Borkulo, C., Boschloo, L., Borsboom, D., Penninx, B. W. J. H., Lourens, J. W., & Schoevers, R. A. (2015). Association of symptom network structure with the course of longitudinal depression. JAMA Psychiatry, 72, 1219–1226.CrossRefGoogle Scholar
Van Someren, E. J., Swaab, D. F., Colenda, C. C., Cohen, W., McCall, W. V., & Rosenquist, P. B. (1999). Bright light therapy: Improved sensitivity to its effects on rest-activity rhythms in Alzheimer patients by application of nonparametric methods. Chronobiology International, 16, 505–518.CrossRefGoogle ScholarPubMed
Verkooijen, S., van Bergen, A. H., Knapen, S. E., Vreeker, A., Abramovic, L., Pagani, L., … Ophoff, R. A. (2017). An actigraphy study investigating sleep in bipolar I patients, unaffected siblings and controls. Journal of Affective Disorders, 208, 248–254.CrossRefGoogle ScholarPubMed
Wichers, M. (2014). The dynamic nature of depression: A new micro-level perspective of mental disorder that meets current challenges. Psychological Medicine, 44, 1349–1360.CrossRefGoogle ScholarPubMed
Supplementary material: File

Knapen et al. supplementary material

Tables S1-S5

Download Knapen et al. supplementary material(File)
File 51.8 KB