Effect of Sleep-restriction on Salivary Adrenal Hormones in Korean Adolescent

수면제한이 청소년의 타액 호르몬에 미치는 영향

  • Cho, Yoon-Seong (Department of Oriental Internal Medicine, College of Oriental Medicine, Wonkwang University) ;
  • Je, Jun-Tae (Department of Oriental Internal Medicine, College of Oriental Medicine, Wonkwang University) ;
  • Lee, Sang-Kwan (Department of Oriental Internal Medicine, College of Oriental Medicine, Wonkwang University)
  • 조윤성 (원광대학교 한의과대학 한방내과) ;
  • 제준태 (원광대학교 한의과대학 한방내과) ;
  • 이상관 (원광대학교 한의과대학 한방내과)
  • Received : 2011.02.10
  • Accepted : 2011.03.23
  • Published : 2011.04.25

Abstract

The goal of this study was to clarify effects of sleep restriction on a diurnal rhythm of salivary cortisol and DHEA levels in Korean adolescents.83 middle school students were recruited to participate in restricted sleep period group (less than 4h/day) or unrestricted sleep period group (from 6h/day to 7h/day). Both were 14 to 17 years old. They were instructed to keep the sleep-awakening schedule and sampling protocol. Saliva samples of cortisol and DHEA were collected at 8h, 12h, 16h and 20h. Salivary hormones were analysed with salivary cortisol(or DHEA) EIA kit according to a fixed assay protocol. Cortisol levels of restricted sleep period group and unrestricted sleep period group significantly decreased according to the sampling times. Cortisol levels of sleep restricted group was significantly higher than those of usual sleep group at all sampling times. At 8h, DHEA levels of both groups were significantly higher than those at 12h, 16h and 20h. However, DHEA levels of restricted sleep period group did not differ from those of unrestricted sleep period group at all sampling times.Cortisol and DHEA levels of both group showed the typical diurnal rhythm regardless of sleep status. Restricted sleep may increased cortisol release, not DHEA release, which indicated a changed HPA axis.

Keywords

References

  1. Zee, P.C., Vitiello, M.V. Circadian Rhythm Sleep Disorder: Irregular Sleep Wake Rhythm Type. Sleep Med Clin. 4(2):213-218, 2009. https://doi.org/10.1016/j.jsmc.2009.01.009
  2. Buckley, T.M., Schatzberg, A.F. On the interactions of the hypothalamic-pituitary-adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rhythm, exemplary sleep disorders. J Clin Endocrinol Metab. 90(5):3106-3114, 2005. https://doi.org/10.1210/jc.2004-1056
  3. Gaillard, R.C., Al-Damluji, S. Stress and the pituitary-adrenal axis. Baillieres Clin Endocrinol Metab. 1(2):319-354, 1987. https://doi.org/10.1016/S0950-351X(87)80066-6
  4. Miller, D.B., O'Callaghan, J.P. Neuroendocrine aspects of the response to stress. Metabolism. 51(6 Suppl 1):5-10, 2002.
  5. Boscaro, M., Barzon, L., Fallo, F., Sonino, N. Cushing's syndrome. Lancet. 357(9258):783-791, 2001. https://doi.org/10.1016/S0140-6736(00)04172-6
  6. Kirschbaum, C., Wolf, O.T., May, M., Wippich, W., Hellhammer, D.H. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci. 58(17):1475-1483, 1996. https://doi.org/10.1016/0024-3205(96)00118-X
  7. Pruessner, J.C., Wolf, O.T., Hellhammer, D.H., Buske-Kirschbaum, A., von Auer, K., Jobst, S., Kaspers, F., Kirschbaum, C. Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 61(26):2539-2549, 1997. https://doi.org/10.1016/S0024-3205(97)01008-4
  8. Weitzman, E.D., Fukushima, D., Nogeire, C., Roffwarg, H., Gallagher, T.F., Hellman, L. Twenty-four hour pattern of the episodic secretion of cortisol in normal subjects. J Clin Endocrinol Metab. 33(1):14-22, 1971. https://doi.org/10.1210/jcem-33-1-14
  9. 한상철, 김미숙. 성인의 청소년기 위험행동이 삶의 질에 미치는 영향. 미래청소년학회지 5(1):201-218, 2008.
  10. 박옥기, 홍성호, 박금수, 정종승, 유진상. 고등학교 3학년 학생에서 특성불안의 고저에 따른 수면양상. 가정의학회지 16:721-730, 1995.
  11. Leproult, R., Copinschi, G., Buxton, O., Van Cauter, E. Sleep loss results in an elevation of cortisol levels the next evening. Sleep. 20(10):865-870, 1997.
  12. Spiegel, K., Leproult, R., Van Cauter, E. Impact of sleep debt on metabolic and endocrine function. Lancet. 354(9188):1435-1439, 1999. https://doi.org/10.1016/S0140-6736(99)01376-8
  13. Spiegel, K., Leproult, R., L'hermite-Balériaux, M., Copinschi, G., Penev, P.D., Van Cauter, E. Leptin levels are dependent on sleep duration: relationships with sympathovagal balance, carbohydrate regulation, cortisol, and thyrotropin. J Clin Endocrinol Metab. 89(11):5762-5771, 2004. https://doi.org/10.1210/jc.2004-1003
  14. Akerstedt, T., Palmblad, J., de la Torre, B., Marana, R., Gillberg, M. Adrenocortical and gonadal steroids during sleep deprivation. Sleep 3(1):23-30, 1980. https://doi.org/10.1093/sleep/3.1.23
  15. Kant, G.J., Genser, S.G., Thorne, D.R., Pfalser, J.L., Mougey, E.H. Effects of 72 hour sleep deprivation on urinary cortisol and indices of metabolism. Sleep. 7(2):142-146, 1984. https://doi.org/10.1093/sleep/7.2.142
  16. Meerlo, P., Sgoifo, A., Suchecki, D. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity, Sleep Med Rev. 12(3):197-210, 2008. https://doi.org/10.1016/j.smrv.2007.07.007
  17. Hucklebridge, F., Hussain, T., Evans, P., Clow, A. The diurnal patterns of the adrenal steroids cortisol and dehydroepiandrosterone (DHEA) in relation to awakening. Psychoneuroendocrinology. 30(1):51-57, 2005. https://doi.org/10.1016/j.psyneuen.2004.04.007
  18. Goodyer, I.M., Herbert, J., Tamplin, A. Psychoendocrine antecedents of persistent first-episode major depression in adolescents: a community-based longitudinal enquiry. Psychol Med. 33(4):601-610, 2003. https://doi.org/10.1017/S0033291702007286
  19. Granger, D.A., Schwartz, E.B., Booth, A., Curran, M., Zakaria, D. Assessing dehydroepiandrosterone in saliva: a simple radioimmunoassay for use in studies of children, adolescents and adults. Psychoneuroendocrinology. 24(5):567-579, 1999. https://doi.org/10.1016/S0306-4530(99)00013-X
  20. Brwon, G.L., McGarvey, E.L., Shirtcliff, E.A., Keller, A., Granger, D.A., Flavin, K. Salivary cortisol, dehydroepiandrosterone, and testosterone interrelationships in healthy young males: a pilot study with implications for studies of aggressive behavior. Psychiatry Res. 159(1-2):67-76, 2008. https://doi.org/10.1016/j.psychres.2007.06.012
  21. 許浚著. 원진희 외 8인 점교. 精校東醫寶鑑上.下. 서울, 단촌글방, pp 3-4, 2000.
  22. (懸吐國譯)黃帝內經素問注釋. 上. 서울, 경희대학교출판국, pp 25-29, 1998.
  23. Squire, L.R., Bloom, F.E., McConnell, S.K., Roberts. J.L., Spitzer, N.C., Zigmond, M.J. Fundamental Neuroscience. 2nd ed. China:Academic Press. p 1067, 2002.
  24. Reppert, S.M., Weaver, D.R. Coordination of circadian timing in mammals. Nature. 418(6901):935-941, 2002. https://doi.org/10.1038/nature00965
  25. Johnson, K.L., Rn, C.R. The hypothalamic-pituitary-adrenal axis in critical illness. AACN Clin Issues. 17(1):39-49, 2006. https://doi.org/10.1097/00044067-200601000-00006
  26. Jefferies, W.M. Cortisol and immunity. Med Hypotheses. 34(3):198-208, 1991. https://doi.org/10.1016/0306-9877(91)90212-H
  27. Schleimer, R.P. Interactions between the hypothalamic-pituitary-adrenal axis and allergic inflammation. J Allergy Clin Immunol. 106(5Suppl):S270-274, 2000. https://doi.org/10.1067/mai.2000.110162
  28. Rosmond, R., Dallman, M.F., Bjornatorp, P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab. 83(6):1853-1859, 1998. https://doi.org/10.1210/jc.83.6.1853
  29. de Kloet, E.R. Hormones, brain and stress. Endocr Regul. 37(2):51-68, 2003.
  30. Perez-Neri, I., Montes, S., Ojeda-Lopez, C., Ramirez-Bermudez, J., Rios, C. Modulation of neurotransmitter systems by dehydroepiandrosterone and dehydroepiandrosterone sulfate: mechanism of action and relevance to psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry. 32(5):1118-1130, 2008. https://doi.org/10.1016/j.pnpbp.2007.12.001
  31. Young, A.H., Gallagher, P., Porter, R.J. Elevation of the cortisol- dehydroepiandrosterone ratio in drug-free depressed patients. Am J Psychiatry. 159(7):1237-1239, 2002. https://doi.org/10.1176/appi.ajp.159.7.1237
  32. van Niekerk, J.K., Huppert, F.A., Herbert, J. Salivary cortisol and DHEA: association with measures of cognition and well-being in normal older men, and effects of three months of DHEA supplementation. Psychoneuroendocrinology. 26: 591-612, 2001. https://doi.org/10.1016/S0306-4530(01)00014-2
  33. Erickson, K., Drevets, W., Schulkin, J. Glucocorticoid regulation of diverse cognitive functions in normal and pathological emotional states. Neurosci Biobehav Rev. 27(3):233-246, 2003. https://doi.org/10.1016/S0149-7634(03)00033-2
  34. Dranovsky, A., Hen, R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 59(12):1136-1143, 2006. https://doi.org/10.1016/j.biopsych.2006.03.082
  35. Sapolsky, R.M.. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57(10):925-935, 2000. https://doi.org/10.1001/archpsyc.57.10.925
  36. Roth, T., Roehrs, T., Pies, R. Insomnia: pathophysiology and implications for treatment. Sleep Med Rev. 11(1):71-79, 2007. https://doi.org/10.1016/j.smrv.2006.06.002
  37. Goodyer, I.M., Herbert, J., Altham, P.M. Adrenal steroid secretion and major depression in 8- to 16-year-olds. III: Influence of cortisol/DHEA ratio at presentation on subsequent rates of disappointing life events and persistent major depression. Psychol Med. 28(2):265-273, 1998. https://doi.org/10.1017/S0033291797006314
  38. Shirtcliff, E.A., Essex, M.J. Concurrent and longitudinal associations of basal and diurnal cortisol with mental health symptoms in early adolescence. Dev Psychobio. 50(7):690-703, 2008. https://doi.org/10.1002/dev.20336
  39. 계선자, 이정우, 김명자, 박미석, 유을용. 청소년의 학교생활실태 및 학교생활만족도. 대한가정학회지 39(2):57-72, 2001.
  40. Lee, M. Korean adolescents' "Examination Hell" and their use of free time. New Dir Child Adolesc Dev. (99):9-21, 2008.
  41. Fugita, S.S., Crittenden, K.S. Towards culture- and population-specific norms for self-reported depressive symptomatology. Int J Soc Psychiatry. 36(2):83-92, 1990. https://doi.org/10.1177/002076409003600201
  42. Sung, H., Lubin, B., Yi, J. Reliability and validity of the Korean Youth Depression Adjective Check List (Y-DACL). Adolescence. 27(107):527-533, 1992.
  43. 이미리. 청소년의 우울증 수준에 있어서 문화적 차이와 일상생활 활동 경험과의 관계 : 한국과 미국 고등학교 3학년생의 비교. 한국아동학회지 17(1):137-152, 1996.
  44. 송동호, 이홍식, 김찬형, 김지웅, 민성길, Kim Larissa. 한국 및 러시아 한국계 청소년 우울증의 사회심리적 위험요인에 대한 횡문화 비교 연구. 신경정신의학, 38(5):944-955, 1999.
  45. 김귀봉, 김영수, 강성구, 박주영, 김영호. 청소년의 부정적 건강행동과 심리적 요인과의 인과적 모형. 한국스포츠심리학회지 11(2):133-150, 1999.
  46. Van Cauter, E., Holmback, U., Knutson, K., Leproult, R., Miller, A., Nedeltcheva, A., Pannain, S., Penev, P., Tasali, E., Spiegel, K. Impact of sleep and sleep loss on neuroendocrine and metabolic function. Horm Res. 67(1):2-9, 2007. https://doi.org/10.1159/000097543
  47. Trenell MI, Marshall NS, Rogers NL. Sleep and metabolic control: waking to a problem? Clin Exp Pharmacol Physiol. 34(1-2):1-9, 2007. https://doi.org/10.1111/j.1440-1681.2007.04541.x
  48. Pilcher JJ, Huffcutt AI. Effects of sleep deprivation on performance: a meta-analysis. Sleep. 19(4):318-326, 1996. https://doi.org/10.1093/sleep/19.4.318
  49. 김준호, 왕성근, 김정란. 24시간 수면 박탈의 정신생리적 변화와 카페인의 효과. 생물치료정신의학, 10(1):45-57, 2004.
  50. Dinges, D.F., Pack, F., Williams, K., Gillen, K.A., Powell, J.W., Ott, G.E., Aptowicz, C., Pack, A.I. Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4-5 hours per night. Sleep. 20(4):267-277, 1997.
  51. Van Dongen, H.P., Maislin, G., Mullington, J.M., Dinges, D.F. The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep. 26(2):117-126, 2003. https://doi.org/10.1093/sleep/26.2.117
  52. Vining, R.F., McGinley, R.A., Maksvytis, J.J., Ho, K.Y. Salivary cortisol: a better measure of adrenal cortical function than serum cortisol. Ann Clin Biochem. 20(6):329-335, 1983. https://doi.org/10.1177/000456328302000601
  53. Kirschbaum, C., Hellhammer, D.H. Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinology. 19(4):313-333, 1994. https://doi.org/10.1016/0306-4530(94)90013-2
  54. Meulenberg, P.M., Hofman, J.A. The effect of oral contraceptive use and pregnancy on the daily rhythm of cortisol and cortisone. Clin Chim Acta. 190(3):211-221, 1990. https://doi.org/10.1016/0009-8981(90)90175-R
  55. Patel, R.S., Shaw, S.R., Macintyre, H., McGarry, G.W., Wallace, A.M. Production of gender-specific morning salivary cortisol reference intervals using internationally accepted procedures. Clin Chem Lab Med. 42(2):1424-1429, 2004.
  56. Goodyer, I.M., Park, R.J., Netherton, C.M., Herbert, J. Possible role of cortisol and dehydroepiandrosterone in human development and psychopathology. Br J Psychiatry. 179: 243-249, 2001. https://doi.org/10.1192/bjp.179.3.243
  57. Fries, E., Dettenborn, L., Kirschbaum, C. The cortisol awakening response (CAR): facts and future directions. Int J Psychophysiol. 72(1):67-73, 2009. https://doi.org/10.1016/j.ijpsycho.2008.03.014
  58. Webb, W.B., Agnew, H.W. Are we chronically sleep deprived? Bull Psychon Soc. 6(1):47-48, 1975. https://doi.org/10.3758/BF03333140
  59. Pruessner, J.C., Gaab, J., Hellhammer, D.H., Lintz, D., Schommer, N., Kirschbaum, C. Increasing correlations between personality traits and cortisol stress responses obtained by data aggregation. Psychoneuroendocrinology. 22(8):615-625, 1997. https://doi.org/10.1016/S0306-4530(97)00072-3
  60. Rohleder, N., Joksimovic, L., Wolf, J.M., Kirschbaum, C. Hypocortisolism and increased glucocorticoid sensitivity of pro-Inflammatory cytokine production in Bosnian war refugees with posttraumatic stress disorder. Biol Psychiatry. 55(7):745-751, 2004. https://doi.org/10.1016/j.biopsych.2003.11.018
  61. Oskis, A., Loveday, C., Hucklebridge, F., Thorn, L., Clow, A. Diurnal patterns of salivary cortisol across the adolescent period in healthy females. Psychoneuroendocrinology. 34(3):307-316, 2009. https://doi.org/10.1016/j.psyneuen.2008.09.009