Abstract
Methods of evaluation of substates of sleep and sleepiness differ in, at least, two respects. Although sleepiness has not been separated from other wake and sleep substates using yes-or-no criteria for sleep scoring, it would be consciously perceived and, therefore, assessed with a questionary. However, such subjective method was challenged by the finding suggesting a disconnect between two most widely used subjective and objective indicators of excessive daytime sleepiness (EDS), a score on the Epworth sleepiness scale (ESS) > 10 and a reduced latency to sleep onset (SOL), respectively. We examined whether these two EDS indicators differ in their association with physiological sleepiness, i.e., the polysomnographic indexes of elevated sleep pressure. In the afternoon hours, polysomnographic recordings were obtained throughout 54 50-min and 56 90-min napping attempts of 27 and 28 university students, respectively. Within some but not all 10-min intervals of the 50- or 90-min naps, each EDS indicator was validated against different objective polysomnographic indexes suggesting an association of EDS with elevated sleep pressure. Significant differences in sleep indexes were found between participants with short and longer SOL, but they disappeared right before the appearance of such differences between participants with higher and lower ESS score (usually at the 4th 10-min interval). This mismatch in timing of appearance of significant differences might be a plausible explanation for the lack of significant association between the ESS and SOL. Therefore, the physiologic underpinnings of the ESS can be uncovered despite such a disconnect between these two EDS indicators.
Graphical abstract
Similar content being viewed by others
Data availability
The datasets analyzed during the current study are available from the corresponding author on reasonable request.
References
T.L. Baker, Introduction to sleep and sleep disorders. Med. Clin. N. Am. 69, 1123–1152 (1985)
C. Metzner, A. Schilling, M. Traxdorf, H. Schulze, P. Krauss, Sleep as a random walk: a super-statistical analysis of EEG data across sleep stages. Commun. Biol. 4(1), 1385 (2021). https://doi.org/10.1038/s42003-021-02912-6
E. Olbrich, P. Achermann, T. Wennekers, The sleeping brain as a complex system. Philos. Trans. A Math. Phys. Eng. Sci. 2011(369), 3697–3707 (1952). https://doi.org/10.1098/rsta.2011.0199
J.M. Mullington, C.A. Czeisler, N. Goel, J.M. Krueger, T.J. Balkin, M. Johns, P.J. Shaw, Panel discussion: current status of measuring sleepiness. J. Clin. Sleep Med. 7, S22-25 (2011)
J. Axelsson, M. Ingre, G. Kecklund, M. Lekander, K.P. Wright, T. Sundelin, Sleepiness as motivation: a potential mechanism for how sleep deprivation affects behavior. Sleep (2019). https://doi.org/10.1093/sleep/zsz291
T. Shochat, N. Santhi, P. Herer, D.J. Dijk, A.C. Skeldon, Sleepiness is a signal to go to bed: data and model simulations. Sleep 44(10), zsab123 (2021). https://doi.org/10.1093/sleep/zsab123
A.A. Putilov, O.G. Donskaya, Calibration of an objective alertness scale. Int. J. Psychophysiol. 94(1), 69–75 (2014). https://doi.org/10.1016/j.ijpsycho.2014.07.010
R. Cluydts, E. De Valck, E. Verstraeten, P. Theys, Daytime sleepiness and its evaluation. Sleep Med. Rev. 6, 83–96 (2002)
D.F. Dinges, Sleep debt and scientific evidence. Sleep 27, 1050–1052 (2004)
J. Horne, Is there a sleep debt? Sleep 27, 1047–1049 (2004)
J.A. Horne, C.V. Burley, We know when we are sleepy: subjective versus objective measurements of moderate sleepiness in healthy adults. Biol Psychol. 83, 266–268 (2010)
P.K. Hitchcott, D. Menicucci, S. Frumento, A. Zaccaro, A. Gemignani, The neurophysiological basis of excessive daytime sleepiness: suggestions of an altered state of consciousness. Sleep Breath. 24, 15–23 (2020)
A.J. Campbell, A.M. Neill, D.A.R. Scott, Clinical reproducibility of the Epworth Sleepiness Scale for patients with suspected sleep apnea. J. Clin. Sleep Med. 14(5), 791–795 (2018). https://doi.org/10.5664/jcsm.7108
M.W. Johns, A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14, 540–545 (1991)
A. van der Heide, M.K. van Schie, G.J. Lammers, Y. Dauvilliers, I. Arnulf, G. Mayer, C.L. Bassetti, C.L. Ding, P. Lehert, J.G. van Dijk, Comparing treatment effect measurements in narcolepsy: The Sustained attention to response task, Epworth sleepiness scale and maintenance of wakefulness test. Sleep 38(7), 1051–1058 (2015). https://doi.org/10.5665/sleep.4810
V.P. Martin, R. Lopez, Y. Dauvilliers, J.-L. Rouas, P. Philip, J.-A. Micoulaud-Franchi, Sleepiness in adults: an umbrella review of a complex construct. Sleep Med. Rev. 67, 101718 (2023). https://doi.org/10.1016/j.smrv.2022.101718
D.J. Buysse, M.L. Hall, P.J. Strollo, T.W. Kamarck, J. Owens, L. Lee, S.E. Reis, K.A. Matthews, Relationships between the Pittsburgh Sleep Quality Index (PSQI), Epworth Sleepiness Scale (ESS), and clinical/polysomnographic measures in a community sample. J. Clin. Sleep Med. 4(6), 563–571 (2008)
R. Lok, J.M. Zeitzer, Physiological correlates of the Epworth Sleepiness Scale reveal different dimensions of daytime sleepiness. Sleep Adv. 2(1), zpab008 (2021). https://doi.org/10.1093/sleepadvances/zpab008
R.N. Aurora, B. Caffo, C. Crainiceanu, N.M. Punjabi, Correlating subjective and objective sleepiness: revisiting the association using survival analysis. Sleep 34, 1707–1714 (2011)
S.R. Benbadis, E. Mascha, M.C. Perry, B.R. Wolgamuth, L.A. Smolley, D.S. Dinner, Association between the Epworth sleepiness scale and the multiple sleep latency test in a clinical population. Ann. Intern. Med. 130(4 Pt 1), 289–292 (1999)
R.D. Chervin, M.S. Aldrich, The Epworth Sleepiness Scale may not reflect objective measures of sleepiness or sleep apnea. Neurology 52, 125–131 (1999)
M.W. Johns, Sensitivity and specificity of the multiple sleep latency test (MSLT), the maintenance of wakefulness test and the Epworth Sleepiness Scale: failure of the MSLT as a gold standard. J. Sleep Res. 9, 5–11 (2000)
R. Mehra, L. Wang, N. Andrews, W.H.W. Tang, J.B. Young, S. Javaheri, N. Foldvary-Schaefer, Dissociation of objective and subjective daytime sleepiness and biomarkers of systemic inflammation in sleep-disordered breathing and systolic heart failure. J. Clin. Sleep Med. 13(12), 1411–1422 (2017)
L.G. Olson, M.F. Cole, A. Ambrogetti, Correlations among Epworth Sleepiness Scale scores, multiple sleep latency tests and psychological symptoms. J. Sleep Res. 7, 248–253 (1998)
O. Munkhjargal, Y. Oka, S. Tanno, H. Shimizu, Y. Fujino, T. Kira, A. Ooe, M. Eguchi, T. Higaki, Discrepancy between subjective and objective sleepiness in adolescents. Sleep Med. 96, 1–7 (2022). https://doi.org/10.1016/j.sleep.2022.04.025
V.B. Dorokhov, A.I. Taranov, A.M. Narbut, D.S. Sakharov, S.S. Gruzdeva, O.N. Tkachenko, G.N. Arsen’ev, I.S. Blochin, A.A. Putilov, Effects of exposure to a weak extremely low frequency electromagnetic field on daytime sleep architecture and length. Sleep Med. Res. 10, 97–102 (2019)
V.B. Dorokhov, D.S. Sveshnikov, A.N. Puchkova, A.O. Taranov, D.S. Sakharov, S.S. Gruzdeva, O.N. Tkachenko, G.N. Arsen’ev, N.V. Ligun, V.V. Dementienko, Z.B. Bakaeva, E.B. Yakunina, Y.P. Starshinov, V.I. Torshin, O.G. Donskaya, A.A. Putilov, Differential relationship of two measures of sleepiness with the drives for sleep and wake. Sleep Breath 25, 2179–2187 (2021)
Iber C, Ancoli-Israel S, Chesson A, & Quan SF, eds. The AASM manual for the scoring of sleep and associated events: rules, terminology, and technical specification, 1st ed. Westchester, IL: American Academy of Sleep Medicine, 2007.
M. Frigo, S.G. Johnson, The design and implementation of FFTW3. Proc. IEEE 93, 216–231 (2005)
T. Roenneberg, A. Wirz-Justice, M. Merrow, Life between clocks: daily temporal patterns of human chronotypes. J. Biol. Rhythms 18, 80–90 (2003)
D.J. Buysse, C.F. Reynolds, T.H. Monk, S.R. Berman, D.J. Kupfer, The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 28, 193–213 (1989)
N. Marcoen, M. Vandekerckhove, D. Neu, N. Pattyn, O. Mairesse, Individual differences in subjective circadian flexibility. Chronobiol. Int. 32, 1246–1253 (2015)
A.A. Putilov, V.B. Dorokhov, M.G. Poluektov, Evening chronotype, late weekend sleep times and social jetlag as possible causes of sleep curtailment after maintaining perennial DST: ain’t they as black as they are painted? Chronobiol. Int. 37, 82–100 (2020)
A.A. Putilov, E.G. Verevkin, Simulation of the ontogeny of social jet lag: a shift in just one of the parameters of a model of sleep-wake regulating process accounts for the delay of sleep phase across adolescence. Front. Physiol. 9(1529), 1–11 (2018). https://doi.org/10.3389/fphys.2018.01529
T.B. Kendzerska, P.M. Smith, R. Brignardello-Petersen, R.S. Leung, G.A. Tomlinson, Evaluation of the measurement properties of the Epworth sleepiness scale: a systematic review. Sleep Med. Rev. 18, 321–331 (2014)
O. Mairesse, D. Neu, Tired of blunt tools? Sharpening the clinical assessment of fatigue and sleepiness. Psychiatry Res. 238, 100–108 (2016)
T. Åkerstedt, M. Gillberg, Subjective and objective sleepiness in the active individual. Int. J. Neurosci. 52, 29–37 (1990)
T.H. Monk, A visual analogue scale technique to measure global vigor and affect. Psychiatry Res. 27, 89–99 (1989)
A.A. Borbély, F. Baumann, D. Brandeis, I. Strauch, D. Lehmann, Sleep deprivation; effect on sleep stages and EEG power density in man. Electroenceph. Clin. Neurophysiol. 51, 483–493 (1981)
A.A. Borbély, S. Daan, A. Wirz-Justice, T. Deboer, The two-process model of sleep regulation: a reappraisal. J. Sleep Res. 25, 131–143 (2016)
D. Carmelli, D.L. Bliwise, G.E. Swan, T. Reed, A genetic analysis of the Epworth Sleepiness Scale in 1560 World War II male veteran twins in the NAS-NRC Twin Registry. J. Sleep Res. 10(1), 53–58 (2001). https://doi.org/10.1046/j.1365-2869.2001.00241.x
Acknowledgements
The authors are very grateful to Dr. Dmitry S. Sveshnikov, Dr. Zarina V. Bakaeva, Dr. Olga V. Mankaeva, and Prof. Vladimir I. Torshin from the Medical Institute at the Peoples' Friendship University for help in organization of the survey and polysomnographic recordings of their students. The North-Caucasus Federal University provided technical and other similar support to AAP.
Funding
The Russian Science Foundation funded RAE (Grant #22-72-10061).
Author information
Authors and Affiliations
Contributions
Conceptualization AAP; funding acquisition EBY, and VBD; data curation VBD, EBY, ANP, DES, EOG, AOT, ONT, NVL, GNA, AER, AEM, VVD, and AAP, resources AAP, DSS, and VBD; project administration AAP and VBD; supervision AAP; software DES, ANP, and AAP; investigation VBD, ANP, and AAP; methodology AAP, VBD, and ANP; sleep scoring: ANP and EOG; spectra calculation: DES; validation AAP; visualization AAP; writing—review and editing AAP, VBD, EBY, ANP, DES, EOG, AOT, ONT, NVL, GNA, AER, AEM, and VVD.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests. The funders had no role in the design of the study, the collection, analyses, or interpretation of data, the writing of the manuscript, and the decision to publish the results.
Additional information
Brain Physiology Meets Complex Systems. Guest editors: Thomas Penzel, Teemu Myllylä, Oxana V. Semyachkina-Glushkovskaya, Alexey Pavlov, Anatoly Karavaev.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dorokhov, V.B., Yakunina, E.B., Puchkova, A.N. et al. Can physiological sleepiness underlie consciously perceived sleepiness assessed with the Epworth sleepiness scale?. Eur. Phys. J. Spec. Top. 232, 569–582 (2023). https://doi.org/10.1140/epjs/s11734-023-00771-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1140/epjs/s11734-023-00771-2