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Sleep spindle characteristics in overweight adolescents with obstructive sleep apnea syndrome

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Abstract

Sleep spindles may display a sleep protective function. Thus, their activity is also a stable marker of sleep disturbances. We investigated whether spindle activity could be altered in overweight (OW) adolescents with obstructive sleep apnea syndrome (OSAS), compared with OW controls and normal weight (NW) adolescents. We also evaluated spindle characteristics correlation with body mass index (BMI) and OSAS-related sleep parameters. Thirty OW adolescents and 15 NW adolescents (age 14–17 years; all males) underwent polysomnography. Sleep spindles were automatically detected during stage 2 non-rapid eye movement sleep. The spindle activity characteristics involved: number of spindles; mean spindle density; mean maximum spindle amplitude; mean spindle duration; and mean spindle frequency. All adolescents were divided into three groups (18 OW patients with OSAS, 12 OW controls and 15 NW controls). Number of spindles and spindle density were significantly higher, but maximum spindle amplitude and spindle frequency were significantly lower in OSAS patients, as compared in both OW controls and NW controls. In this group, significant correlations were also found between spindle characteristics and OSAS-related sleep parameters (apnea hypopnea index, min SaO2 and total arousal index), but no significant correlations were found between spindles and BMI. The increased spindle number and spindle density in OW adolescents with OSAS might be the EEG responses to multiple brief occlusions or loads applied during inspiration in impaired sleep, an adaptive response to sleep fragmentation and hypoxia.

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References

  1. Silber MH, Ancoli-Israel S, Bonnet MH, et al. The visual scoring of sleep in adults. J Clin Sleep Med. 2007;3(2):121–31.

    PubMed  Google Scholar 

  2. Steriade M, McCarley RW. Brain control of wakefulness and sleep. New York: Springer; 2005.

    Google Scholar 

  3. Schabus M, Dang-Vu TT, Albouy G, et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci USA. 2007;104:13164–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Dang-Vu TT, Salimi A, Boucetta S, et al. Sleep spindles predict stress-related increases in sleep disturbances. Front Hum Neurosci. 2015;. doi:10.3389/fnhum.2015.00068.

    PubMed  PubMed Central  Google Scholar 

  5. Wong TK, Galster P, Lau TS, Lutz JM, Marcus CL. Reliability of scoring arousals in normal children and children with obstructive sleep apnea syndrome. Sleep. 2004;27:1139–45.

    Article  PubMed  Google Scholar 

  6. Madaeva I, Shevyrtalova O, Dolgikh V, Kolesnikova L. Obstructive sleep apnea/hypopnea syndrome in adolescents with essential hypertension. Sleep Med. 2009;10:1167–8.

    Article  PubMed  Google Scholar 

  7. Redline S, Tishler PV, Schluchter M, Aylor J, Clark K, Graham G. Risk factors for sleep-disordered breathing in children. Associations with obesity, race, and respiratory problems. Am J Respir Crit Care Med. 1999;159:1527–32.

    Article  CAS  PubMed  Google Scholar 

  8. Shi Z, Taylor AW, Gill TK, Tuckerman J, Adams R, Martin J. Short sleep duration and obesity among Australian children. BMC Public Health. 2010;10:609.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Silva GE, Goodwin JL, Parthasarathy S, Sherrill DL, Vana KD, Drescher AA. Longitudinal association between short sleep, body weight, and emotional and learning problems in Hispanic and Caucasian children. Sleep. 2011;34:1197–205.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hannon TS, Lee S, Chakravorty S. Sleep-disordered breathing in obese adolescents is associated with visceral adiposity and markers of insulin resistance. Int J Pediatr Obes. 2011;6:157–60.

    Article  PubMed  Google Scholar 

  11. Yuan H, Schwab RJ, Kim C, He J, Shults J, Bradford R. Relationship between body fat distribution and upper airway dynamic function during sleep in adolescents. Sleep. 2013;36:1199–207.

    PubMed  PubMed Central  Google Scholar 

  12. Ondze B, Espa F, Dauvilliers Y, Billiard M, Besset A. Sleep architecture, slow wave activity and sleep spindles in mild sleep disordered breathing. Clin Neurophysiol. 2003;114(5):867–74.

    Article  CAS  PubMed  Google Scholar 

  13. Schönwald SV, Carvalho DZ, de Santa-Helena EL, Lemke N, Gerhardt GJ. Topography-specific spindle frequency changes in obstructive sleep apnea. BMC Neurosci. 2012;13:89.

    Article  PubMed  Google Scholar 

  14. Thompson JL, Drysdale M, Baimel C, Kaur M, MacGowan T, Pitman KA, Borgland SL. Obesity-induced structural and neuronal plasticity in the lateral orbitofrontal cortex. Neuropsychopharmacol. 2017;42(7):1480–90. doi:10.1038/npp.2016.284.

    Article  CAS  Google Scholar 

  15. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, et al. CDC growth charts: United States. Adv Data. 2000;314:1–27.

    Google Scholar 

  16. Ujma PP, Konrad BN, Genzel L, Bleifuss A, Simor P, Pótári A, Körmendi J, Gombos F, Steiger A, Bódizs R, Dresler M. Sleep spindles and intelligence: evidence for a sexual dimorphism. J Neurosci. 2014;34(49):16358–68.

    Article  CAS  PubMed  Google Scholar 

  17. Senaratna CV, English DR, Currier D, Perret JL, Lowe A, Lodge C, Russell M, Sahabandu S, Matheson MC, Hamilton GS, Dharmage SC. Sleep apnoea in Australian men: disease burden, co-morbidities, and correlates from the Australian longitudinal study on male health. BMC Public Health. 2016;16(Suppl 3):1029.

    Article  PubMed  Google Scholar 

  18. Marcus CL, Brooks LJ, Draper KA, et al. Diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics. 2012;130:E714–55.

    Article  PubMed  Google Scholar 

  19. Novelli L, Ferri R, Bruni O. Sleep classification according to AASM and Rechtschaffen and Kales: effects on sleep scoring parameters of children and adolescents. J Sleep Res. 2010;19:238–47.

    Article  PubMed  Google Scholar 

  20. Berry RB, Budhiraja R, Gottlieb DJ, et al. Rules for scoring respiratory events in sleep: update of the 2007 AASM manual for the scoring of sleep and associated events. J Clin Sleep Med. 2012;8(5):597–619.

    PubMed  PubMed Central  Google Scholar 

  21. Bonnet M, Carskadon M, Easton P, Guilleminault C, Harper R, Hayes B, Hirshkowitz M, Ktonas P, Keenan S, Pressman M, Roehrs T, Smith J, Walsh J, Weber S, Westbrook P. EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep 1992;15(2):173–84.

  22. Crowley SJ, Acebo C, Carskadon MA. Sleep, circadian rhythms, and delayed phase in adolescence. Sleep Med. 2007;8:602–12.

    Article  PubMed  Google Scholar 

  23. Himanen S-L, Virkkala J, Huupponen E, Hasan J. Spindle frequency remains slow in sleep apnea patients throughout the night. Sleep Med. 2003;4:361–6.

    Article  PubMed  Google Scholar 

  24. Guilleminault C, Do Kim Y, Chowdhuri S, Horita M. Sleep and daytime sleepiness in upper airway resistance syndrome compared to obstructive sleep apnea syndrome. Eur Respir J. 2001;17:838–47.

    Article  CAS  PubMed  Google Scholar 

  25. Heinzer R, Gaudreau H, De’cary A, Sforza E, et al. Slow-wave activity in sleep apnea patients before and after continuous positive airway pressure treatment. Chest. 2001;119:1807–13.

    Article  CAS  PubMed  Google Scholar 

  26. Schabus M, Hödlmoser K, Gruber G, et al. Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur J Neurosci. 2006;23:1738–46.

    Article  CAS  PubMed  Google Scholar 

  27. Cajochen C, Dijk DJ. Electroencephalographic activity during wakefulness, rapid eye movement and non-rapid eye movement sleep in humans: comparison of their circadian and homeostatic modulation. Sleep Biol Rhythm. 2003;1:85–95.

    Article  Google Scholar 

  28. Tagaya H, Trachsel L, Murck H, Antonijevic I, Steiger A, Holsboer F, Friess E. Temporal EEG dynamics of non-REM sleep episodes in humans. Brain Res. 2000;861(2):233–40.

    Article  CAS  PubMed  Google Scholar 

  29. Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I. Regional slow waves and spindles in human sleep. Neuron. 2011;70:153–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Carvalho DZ, Gerhardt GJ, Dellagustin G, de Santa-Helena EL, Lemke N, Segal AZ, Schönwald SV. Loss of sleep spindle frequency deceleration in obstructive sleep apnea. Clin Neurophysiol. 2014;125(2):306–12.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Pathophysiology, Sleep Center, Scientific Centre for Family Health and Human Reproduction Problems, Timiryazev Str., 16, Irkutsk, 664003, Russia

    Irina Madaeva

  2. Laboratory of Pediatrics and Neurophysiology, Sleep Center, Scientific Centre for Family Health and Human Reproduction Problems, Timiryazev Str., 16, Irkutsk, 664003, Russia

    Olga Berdina

  3. Scientific Centre for Family Health and Human Reproduction Problems, Irkutsk, Russia

    Liubov Rychkova

  4. Children’s Hospital, Scientific Centre for Family Health and Human Reproduction Problems, Irkutsk, Russia

    Olga Bugun

Authors
  1. Irina Madaeva
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  2. Olga Berdina
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  3. Liubov Rychkova
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  4. Olga Bugun
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Contributions

IM substantial contributed to the conception, design and analysis of data for this work, finally approved of the version to be published, and agreed to be accountable for all aspects of the revised work in ensuring that questions related to the accuracy or integrity of any part of the revised work are appropriately investigated and resolved. OB substantial contributed to the acquisition, analysis, and interpretation of data for this work, drafting the work, and agreed to be accountable for all aspects of the revised work in ensuring that questions related to the accuracy or integrity of any part of the revised work are appropriately investigated and resolved. LR substantial contributed to the conception of this work, revising it critically for important intellectual content, and agreed to be accountable for all aspects of the revised work in ensuring that questions related to the accuracy or integrity of any part of the revised work are appropriately investigated and resolved. OB revised the manuscript critically after the first reviewing, finally approved of the version to be published, and agreed to be accountable for all aspects of the revised work in ensuring that questions related to the accuracy or integrity of any part of the revised work are appropriately investigated and resolved.

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Correspondence to Olga Berdina.

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All authors wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

Research involving human participants and/or animals

All procedures performed in this study involving human participants were in accordance with the ethical standards of the national research committee and with the 1964 Helsinki declaration and its later amendments. This study has been approved by the Scientific Centre for Family Health and Human Reproduction Problems Review Board.

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Informed consent was obtained from all individual participants included in the study.

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Madaeva, I., Berdina, O., Rychkova, L. et al. Sleep spindle characteristics in overweight adolescents with obstructive sleep apnea syndrome. Sleep Biol. Rhythms 15, 251–257 (2017). https://doi.org/10.1007/s41105-017-0104-z

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  • DOI: https://doi.org/10.1007/s41105-017-0104-z

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