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Sleep and Breathing

, Volume 15, Issue 3, pp 409–416 | Cite as

Risk factors and consequences of excessive autonomic activation during sleep in children

  • Pablo E. Brockmann
  • Michael S. Urschitz
  • Anke Noehren
  • Christiane Sokollik
  • Martin Schlaud
  • Christian F. Poets
Original Article

Abstract

Purpose

The aim of this study was to assess risk factors for excessive autonomic activation during sleep (EAAS) and its association with sleep problems, impaired behavior, and poor academic performance in primary school children.

Methods

Data from a community-based study on 997 primary school children were used. Based on nocturnal home pulse oximetry, autonomic activation during sleep was defined as a pulse rate increase by more than 20%. Children with ≥35.9 autonomic activations per hour (i.e., ≥the 95th centile) were classified as suffering from EAAS and compared with controls. Sleep problems, impaired behavior, and academic performance were assessed by parental questionnaires and analysis of school reports.

Results

According to the abovementioned definition, EAAS was diagnosed in 52 children (67% male). Risk factors for EAAS were male gender (odds ratio [95% confidence interval]: 2.06 [1.14–3.72]) and presence of symptoms of sleep-disordered breathing (3.48 [1.29–9.43]). Children with EAAS had a higher prevalence of hyperactive behavior (39.2% vs. 26.0%; p = 0.05) and enuresis (5.8% vs. 0.8%; p = 0.017) but not of poor academic performance. The association with hyperactive behavior was confirmed in a subsample (n = 119) using the Strengths and Difficulties Questionnaire. Mean (SD) score of the hyperactive–inattentive scale was 4.5 (2.8) for EAAS and 3.4 (2.7) for non-EAAS (p = 0.04).

Conclusion

EAAS may be a marker of sleep disruption in children and may predict the occurrence of enuresis and hyperactive behavior.

Keywords

Arousal Pulse oximetry Sleep-disordered breathing Snoring Enuresis Attention-deficit hyperactivity disorder 

Notes

Conflicts of interest

The authors have no conflict of interest to declare.

References

  1. 1.
    Gozal D, Daniel JM, Dohanich GP (2001) Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci 21:2442–2450PubMedGoogle Scholar
  2. 2.
    O’Brien LM, Gozal D (2002) Behavioural and neurocognitive implications of snoring and obstructive sleep apnoea in children: facts and theory. Paediatr Respir Rev 3:3–9PubMedCrossRefGoogle Scholar
  3. 3.
    Beebe DW, Gozal D (2002) Obstructive sleep apnea and the prefrontal cortex: towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. J Sleep Res 11:1–16PubMedCrossRefGoogle Scholar
  4. 4.
    Urschitz MS, Eitner S, Guenther A, Eggebrecht E, Wolff J, Urschitz-Duprat PM, Schlaud M, Poets CF (2004) Habitual snoring, intermittent hypoxia, and impaired behavior in primary school children. Pediatrics 114:1041–1048PubMedCrossRefGoogle Scholar
  5. 5.
    Curcio G, Ferrara M, De Gennaro L (2006) Sleep loss, learning capacity and academic performance. Sleep Med Rev 10:323–337PubMedCrossRefGoogle Scholar
  6. 6.
    Blunden SL, Beebe DW (2006) The contribution of intermittent hypoxia, sleep debt and sleep disruption to daytime performance deficits in children: consideration of respiratory and non-respiratory sleep disorders. Sleep Med Rev 10:109–118PubMedCrossRefGoogle Scholar
  7. 7.
    Grigg-Damberger M, Gozal D, Marcus CL, Quan SF, Rosen CL, Chervin RD, Wise M, Picchietti DL, Sheldon SH, Iber C (2007) The visual scoring of sleep and arousal in infants and children. J Clin Sleep Med 3:201–240PubMedGoogle Scholar
  8. 8.
    McNamara F, Issa FG, Sullivan CE (1996) Arousal pattern following central and obstructive breathing abnormalities in infants and children. J Appl Physiol 81:2651–2657PubMedGoogle Scholar
  9. 9.
    Tauman R, O’Brien LM, Mast BT, Holbrook CR, Gozal D (2004) Peripheral arterial tonometry events and electroencephalographic arousals in children. Sleep 27:502–506PubMedGoogle Scholar
  10. 10.
    Brietzke SE, Katz ES, Roberson DW (2007) Pulse transit time as a screening test for pediatric sleep-related breathing disorders. Arch Otolaryngol Head Neck Surg 133:980–984PubMedCrossRefGoogle Scholar
  11. 11.
    Montgomery-Downs HE, Gozal D (2006) Snore-associated sleep fragmentation in infancy: mental development effects and contribution of secondhand cigarette smoke exposure. Pediatrics 117:e496–e502PubMedCrossRefGoogle Scholar
  12. 12.
    Brouillette RT, Morielli A, Leimanis A, Waters KA, Luciano R, Ducharme FM (2000) Nocturnal pulse oximetry as an abbreviated testing modality for pediatric obstructive sleep apnea. Pediatrics 105:405–412PubMedCrossRefGoogle Scholar
  13. 13.
    Rizzoli A, Urschitz MS, Sautermeister J, Miano S, Pagani J, Villa MP, Poets CF (2009) Pulse transit time for scoring subcortical arousal in infants with obstructive sleep apnea. Sleep Breath 13:137–146PubMedCrossRefGoogle Scholar
  14. 14.
    Schlaud M, Urschitz MS, Urschitz-Duprat PM, Poets CF (2004) The German study on sleep-disordered breathing in primary school children: epidemiological approach, representativeness of study sample, and preliminary screening results. Paediatr Perinat Epidemiol 18:431–440PubMedCrossRefGoogle Scholar
  15. 15.
    Gozal D (1998) Sleep-disordered breathing and school performance in children. Pediatrics 102:616–620PubMedCrossRefGoogle Scholar
  16. 16.
    Brouillette R, Hanson D, David R, Klemka L, Szatkowski A, Fernbach S, Hunt C (1984) A diagnostic approach to suspected obstructive sleep apnea in children. J Pediatr 105:10–14CrossRefGoogle Scholar
  17. 17.
    Kromeyer-Hauschild K, Wabitsch M, Kunze D, Geller F, Geiß HC, Hesse V, von Hippel A, Jaeger U, Johnsen D, Korte W, Menner K, Müller G, Müller JM, Niemann-Pilatus A, Remer T, Schaefer F, Wittchen HU, Zabransky S, Zellner K, Ziegler A, Hebebrand J (2001) Perzentile für den Body-mass-Index für das Kinder- und Jugendalter unter Heranziehung verschiedener deutscher Stichproben. Monatsschr Kinderheilkd 149:807–818CrossRefGoogle Scholar
  18. 18.
    Paavonen EJ, Aronen ET, Moilanen I, Piha J, Rasanen E, Tamminen T, Almqvist F (2000) Sleep problems of school-aged children: a complementary view. Acta Paediatr 89:223–228PubMedCrossRefGoogle Scholar
  19. 19.
    Owens JA, Spirito A, McGuinn M (2000) The Children’s Sleep Habits Questionnaire (CSHQ): psychometric properties of a survey instrument for school-aged children. Sleep 23:1043–1051PubMedGoogle Scholar
  20. 20.
    Urschitz MS, Wolff J, Von Einem V, Urschitz-Duprat PM, Schlaud M, Poets CF (2003) Reference values for nocturnal home pulse oximetry during sleep in primary school children. Chest 123:96–101PubMedCrossRefGoogle Scholar
  21. 21.
    Noehren A, Brockmann PE, Urschitz MU, Sokollok C, Schlaud M, Poets CF (2010) Detection of respiratory events using pulse rate in children with and without obstructive sleep apnea. Pediatr Pulmonol (in press). doi: 10.1002/ppul.21196
  22. 22.
    Bruni O, Ottaviano S, Guidetti V, Romoli M, Innocenzi M, Cortesi F, Giannotti F (1996) The Sleep Disturbance Scale for Children (SDSC). Construction and validation of an instrument to evaluate sleep disturbances in childhood and adolescence. J Sleep Res 5:251–261PubMedCrossRefGoogle Scholar
  23. 23.
    Eitner S, Urschitz MS, Guenther A, Urschitz-Duprat PM, Bohnhorst B, Schlaud M, Poets CF (2007) Sleep problems and daytime somnolence in a German population-based sample of snoring school-aged children. J Sleep Res 16:96–101PubMedCrossRefGoogle Scholar
  24. 24.
    Goodman R (1997) The Strengths and Difficulties Questionnaire: a research note. J Child Psychol Psychiatry 38:581–586PubMedCrossRefGoogle Scholar
  25. 25.
    Klasen H, Woerner W, Wolke D, Meyer R, Overmeyer S, Kaschnitz W, Rothenberger A, Goodman R (2000) Comparing the German versions of the Strengths and Difficulties Questionnaire (SDQ-Deu) and the Child Behavior Checklist. Eur Child Adolesc Psychiatry 9:271–276PubMedCrossRefGoogle Scholar
  26. 26.
    Berg S, Nash S, Cole P, Hoffstein V (1997) Arousals and nocturnal respiration in symptomatic snorers and nonsnorers. Sleep 20:1157–1161PubMedGoogle Scholar
  27. 27.
    Katz ES, Lutz J, Black C, Marcus CL (2003) Pulse transit time as a measure of arousal and respiratory effort in children with sleep-disordered breathing. Pediatr Res 53:580–588PubMedCrossRefGoogle Scholar
  28. 28.
    O’Brien LM, Holbrook CR, Mervis CB, Klaus CJ, Bruner JL, Raffield TJ, Rutherford J, Mehl RC, Wang M, Tuell A, Hume BC, Gozal D (2003) Sleep and neurobehavioral characteristics of 5- to 7-year-old children with parentally reported symptoms of attention-deficit/hyperactivity disorder. Pediatrics 111:554–563PubMedCrossRefGoogle Scholar
  29. 29.
    Owens JA, Maxim R, Nobile C, McGuinn M, Msall M (2000) Parental and self-report of sleep in children with attention-deficit/hyperactivity disorder. Arch Pediatr Adolesc Med 154:549–555PubMedGoogle Scholar
  30. 30.
    Chervin RD, Dillon JE, Bassetti C, Ganoczy DA, Pituch KJ (1997) Symptoms of sleep disorders, inattention, and hyperactivity in children. Sleep 20:1185–1192PubMedGoogle Scholar
  31. 31.
    Owens J, Sangal RB, Sutton VK, Bakken R, Allen AJ, Kelsey D (2009) Subjective and objective measures of sleep in children with attention-deficit/hyperactivity disorder. Sleep Med 10:446–456PubMedCrossRefGoogle Scholar
  32. 32.
    Cortese S, Konofal E, Yateman N, Mouren MC, Lecendreux M (2006) Sleep and alertness in children with attention-deficit/hyperactivity disorder: a systematic review of the literature. Sleep 29:504–511PubMedGoogle Scholar
  33. 33.
    Baeyens D, Roeyers H, Demeyere I, Verte S, Hoebeke P, Vande Walle J (2005) Attention-deficit/hyperactivity disorder (ADHD) as a risk factor for persistent nocturnal enuresis in children: a two-year follow-up study. Acta Paediatr 94:1619–1625PubMedCrossRefGoogle Scholar
  34. 34.
    Neveus T (2003) The role of sleep and arousal in nocturnal enuresis. Acta Paediatr 92:1118–1123PubMedCrossRefGoogle Scholar
  35. 35.
    Bader G, Neveus T, Kruse S, Sillen U (2002) Sleep of primary enuretic children and controls. Sleep 25:579–583PubMedGoogle Scholar
  36. 36.
    Neveus T, Stenberg A, Lackgren G, Tuvemo T, Hetta J (1999) Sleep of children with enuresis: a polysomnographic study. Pediatrics 103:1193–1197PubMedCrossRefGoogle Scholar
  37. 37.
    Hunsballe JM (2000) Increased delta component in computerized sleep electroencephalographic analysis suggests abnormally deep sleep in primary monosymptomatic nocturnal enuresis. Scand J Urol Nephrol 34:294–302PubMedCrossRefGoogle Scholar
  38. 38.
    Yakinci C, Mungen B, Durmaz Y, Balbay D, Karabiber H (1997) Autonomic nervous system functions in children with nocturnal enuresis. Brain Dev 19:485–487PubMedCrossRefGoogle Scholar
  39. 39.
    Fujiwara J, Kimura S, Tsukayama H, Nakahara S, Haibara S, Fujita M, Isobe N, Tamura K (2001) Evaluation of the autonomic nervous system function in children with primary monosymptomatic nocturnal enuresis—power spectrum analysis of heart rate variability using 24-hour Holter electrocardiograms. Scand J Urol Nephrol 35:350–356PubMedCrossRefGoogle Scholar
  40. 40.
    Unalacak M, Aydin M, Ermis B, Ozeren A, Sogut A, Demirel F, Unluoglu I (2004) Assessment of cardiac autonomic regulation in children with monosymptomatic nocturnal enuresis by analysis of heart rate variability. Tohoku J Exp Med 204:63–69PubMedCrossRefGoogle Scholar
  41. 41.
    Harrington C, Kirjavainen T, Teng A, Sullivan CE (2002) Altered autonomic function and reduced arousability in apparent life-threatening event infants with obstructive sleep apnea. Am J Respir Crit Care Med 165:1048–1054PubMedGoogle Scholar
  42. 42.
    Aljadeff G, Gozal D, Schechtman VL, Burrell B, Harper RM, Ward SL (1997) Heart rate variability in children with obstructive sleep apnea. Sleep 20:151–157PubMedGoogle Scholar
  43. 43.
    Bohnhorst B, Peter CS, Poets CF (2000) Pulse oximeters’ reliability in detecting hypoxemia and bradycardia: comparison between a conventional and two new generation oximeters. Crit Care Med 28:1565–1568PubMedCrossRefGoogle Scholar
  44. 44.
    Pitson DJ, Stradling JR (1998) Autonomic markers of arousal during sleep in patients undergoing investigation for obstructive sleep apnoea, their relationship to EEG arousals, respiratory events and subjective sleepiness. J Sleep Res 7:53–59PubMedCrossRefGoogle Scholar
  45. 45.
    Woerner W, Becker A, Friedrich C, Klasen H, Goodman R, Rothenberger A (2002) Normierung und Evaluation der deutschen Elternversion des Strengths and Difficulties Questionnaire (SDQ): Ergebnisse einer repräsentativen Felderhebung. Z Kinder Jugendpsychiatr Psychother 30:105–112PubMedCrossRefGoogle Scholar
  46. 46.
    O’Brien LM, Gozal D (2007) Potential usefulness of noninvasive autonomic monitoring in recognition of arousals in normal healthy children. J Clin Sleep Med 3:41–47PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Pablo E. Brockmann
    • 1
    • 2
  • Michael S. Urschitz
    • 1
    • 6
  • Anke Noehren
    • 3
  • Christiane Sokollik
    • 4
  • Martin Schlaud
    • 5
  • Christian F. Poets
    • 1
  1. 1.Working Group on Pediatric Sleep Medicine, Department of NeonatologyUniversity Children’s HospitalTuebingenGermany
  2. 2.Department of PediatricsPontificia Universidad Catolica de ChileSantiago de ChileChile
  3. 3.Department of CardiologyKrankenhaus an der WeserHamelnGermany
  4. 4.Department of PediatricsUniversity Children’s HospitalTuebingenGermany
  5. 5.Department of Epidemiology and Health ReportingRobert Koch InstituteBerlinGermany
  6. 6.Working Group on Pediatric Sleep Medicine, Department of NeonatologyUniversity Children’s Hospital TuebingenTuebingenGermany

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