Interaction between sleep and growth hormone
Evaluated by manual polysomnography and automatic power spectrum analysis
Corresponding Author
C. Åström
Department of Clinical Neurophysiology, The National Hospital, Rigshospitalet, Copenhagen, Denmark
Christina Åström, University Clinic of Neurology, Hvidovre Hospital, DK-2650 Copenhagen, DenmarkSearch for more papers by this authorCorresponding Author
C. Åström
Department of Clinical Neurophysiology, The National Hospital, Rigshospitalet, Copenhagen, Denmark
Christina Åström, University Clinic of Neurology, Hvidovre Hospital, DK-2650 Copenhagen, DenmarkSearch for more papers by this authorList of terminology in sleep and important abbreviations. Terminology used to describe the sleep pattern followed the international criteria of Rechtschaffen and Kales: Stage 1 to 4 sleep: Stage 1 is the transition from wakefulness to sleep and stages 2–4 are increasing depths of sleep. Delta sleep: = stage 3 + 4, slow wave sleep, “deep sleep”. Stage REM-sleep: Rapid eye movement sleep, referring to the conjugated eye-movements associated with the elaboration of dreams. Sleep onset: The start of first epoch of stage 2 sleep. Sleep latency: The time from lights out, to the beginning of the first stage 2 epoch. REM sleep latency: The time from sleep onset to the beginning of the first REM sleep epoch. Recording time: Time from lights out to final awakening (lights on). WASO: wake time after sleep onset. Total sleep time: Recording time minus sleep latency minus wake time after sleep onset, (TST). Sleep efficiency: Ratio between total sleep time and total recording time. Sleep cycle: First sleep cycle: from first stage 2 to onset of first stage REM. The following sleep cycles: from onset of one REM period to the onset of the next REM period.
Abstract
The relation between nightly growth hormone (GH) secretion and sleep is poorly understood. To examine whether disturbances in GH secretion are reflected in abnormal sleep patterns 8 subjects with isolated GH deficiency and 9 subjects with excess of GH (acromegalics) underwent all night sleep studies, polysomnography. Moreover, the effect of correcting GH concentration on sleep patterns were examined in the same subjects. The results showed that all subjects with GH disturbances had abnormal REM and delta sleep and normalization of GH concentration was followed by correction of the sleep stages. By power spectrum analysis of the sleep EEG it was showed that during low GH concentration the sleep energy was low, and high GH concentration was associated with high sleep energy, and correction of abnormal plasma GH levels resulted in normalization of REM and delta sleep energy per time unit.
Abbreviations:
-
- BMI
-
- Body mass index (kg/m2)
-
- CT
-
- Computer tomography
-
- CDSA
-
- Color density spectral array
-
- EEG
-
- Electroencephalogram
-
- EMG
-
- Electrornyogram
-
- EOG
-
- Electrooculogram
-
- GH
-
- Growth hormone
-
- GHD
-
- Growth hormone deficiency
-
- GRF
-
- Growth hormone releasing factor
-
- GF-1
-
- Insulin-like growth factor 1, same as somatomedine C (SMC)
-
- IGHD
-
- Isolated growth hormone deficiency
-
- MR
-
- Magnetic resonance
-
- OSAS
-
- Obstructive sleep apnea syndrome
-
- TST
-
- Total sleep time (in minutes)
-
- μ2/Hz
-
- Powerdensity
-
- μV2
-
- Power
-
- μV2s
-
- Energy power integrated over time
References
- 1 Marie P. Sur deux cas d'acromégalie. Hypertrophie singulière non congénitale, des extrémités supérieures, inférieures et céphalique. Rev Med Paris 1886: 6: 297–333.
- 2 Reichlin S. Regulation of somatotrophic hormone secretion. In: RO Greep, EB Astwood, E Knobil, eds. Handbook of physiology. Sect 7: Endocrinology Vol IV. The pituitary gland and its neuroendocrine control. Washington DC , Am Physiol Society 1974: 405–448.
- 3 Guillemin R, Brazeau P, Böhlen P et al. Somatocrinin, the growth hormone-releasing factor. Rec Prog Horm Res 1984: 40: 233–286.
- 4 Burgus R, Ling N, Butcher M, Guillemin R. Primary structure of somatostatin, a hypothalamic peptide that inhibits the secretion of pituitary growth hormone. Proc Natl Acad Sci 1973: 70: 684–688.
- 5 Reichlin S. Somatostatin. N Engl J Med 1983: 309: 1495–1501, 1556–1563.
- 6 Ganong WF. Neuroendocrinology. In: FS. Greenspan PH Forsham, eds. Basic & clinical endocrinology. Los Altos : Lange Medical Publication, 1986: 311–42.
- 7 Ross RJM, Miell JP, Buchanan CR. Consider growth hormone and insulin-like growth factor 1 - avoiding auto-cannibalism. Br Med J 1991: 303: 1147–1148.
- 8 Thorner MO, Vance ML, Horvath E, Korvacs K. Growth hormone family. In: JD Wilson, DW Foster, eds. Williams textbook of endocrinology. The anterior pituitary. Philadelphia : Saunders 1992: 226–236.
- 9 Clifton DK. The anterior pituitary – growth hormone. In: HD Patton, AF Fuchs, B Hille, AM Scher, R Steiner, eds. Textbook of physiology, Vol 2. Philadelphia : Saunders 1989: 1211–1212.
- 10 Takahashi Y, Kipnis DM, Daughaday WH. Growth hormone secretion during sleep. J clin Invest 1968: 47: 2079.
- 11 Wilkinson CW. Endocrine rythms and the pineal gland. In: HD Patton, AF Fuchs, B Hille, AM Scher, R Steiner, eds. Textbook of physiology, Vol 2. Philadelphia : Saunders 1989: 1247–1248.
- 12 Parker DC, Rossman LG. Human growth hormone release in sleep: non-suppression by acute hyperglycemia. J Clin Endocrinol Metab 1971: 32: 65–69.
- 13 Moore RY. Organization and function of a central nervous system circadian oscillator: the suprachiasmatic hypothalamic nucleus. Fed Proc 1983: 42: 2783–2789.
- 14 Moore-Ede MC, Czeisler CA, Richardson GS. Circadian timekeeping in health and disease - clinical implications of circadian rythmicity. N Engl J Med 1983: 309: 530–536.
- 15 Karacan I, Rosenbloom A, Williams RI et al. Slow wave sleep deprivation in relation to plasma growth hormone concentration. Behav Neuropsychiatry 1971: 2: 11–14.
- 16 Shaywitz BA, Finkelstein J, Hellman L et al. Growth hormone in newborn infants during sleep waking periods. Pediatrics 1971: 48: 103.
- 17 Weitzman ED. Circadian rhythms and episodic hormone secretion in man. Annu Rev Med 1976: 27: 225–243.
- 18 Krieger DT. Endocrine Rythms. New York : Raven Press, 1979.
- 19 Sassin JF, Parker DC, Mace JW et al. Human growth hormone release: relation to slow wave sleep and sleep-waking cycles. Science 1969: 165: 513–515.
- 20 Carlson HE, Gillin JC, Gordon P, Snyder F. Absence of sleep-related growth hormone peaks in aged normal subjects. J Clin Endocrinol Metab 1972: 34: 1102.
- 21 Guilhaume A, Benoit O, Gourmelen M. Relationship between sleep stage IV deficit and reversible GH deficiency in psychosocial dwarfism. Pediatr Res 1982: 16: 299–302.
- 22 Weitzman ED, Hellman L. Temporal organization of the 24–hour pattern of hypothalamic-pituitary axis. In: M Ferrin, F Halberg, RM Richart, eds. Biorythms and human renroduction. New York : Wiley, 1974: 371–395.
- 23 Saini S. Hindmarch PC, Matthews DR, Pringle PJ, Jones J, Preece MA, Brook CGD. Reproducibility of 24-hour serum growth hormone profiles in man. Clinical Endocrinology 1991: 34: 445–462.
- 24 Dement WC, Kleitman N. Cyclic variations of EEG during sleep and their relation to eye movements, body motility and dreaming. Electroenceph Clin Neurophysiol 1957: 9: 673–690.
- 25 A. Rechtschaffen A Kales, eds. A manual of standardized terminology, techniques and scoring systems for sleep stages of human subjects. US Government Printing Office 1968, Washington DC .
- 26 Wu RHK, Thorpy MJ. Effect of growth hormone on sleep EEGs in growth hormone deficient children. Sleep 1988: 11: 425–429.
- 27 Hart TB, Radow SK, Blackard WG, Tucker HG, Cooper KR. Sleep apnea in active acromegaly. Arch Intern Med 1985: 145: 865–866.
- 28 Mezon BJ, West P, MacLean JP, Kryger MH. Sleep apnea in acromegaly. Am J Med 1980: 69: 615–618.
- 29 Perks WH, Horrocks PM, Cooper RA et al. Sleep apnea in acromegaly. Br Med J 1980: 280: 894–897.
- 30 Nicolono J, Marmottant G, Nicolono CH, Pasquier J, Sauvan R, Bert J. Acromegalie at apnee du sommeil. Ann Endocrinol 1981: 42: 205–232.
- 31 Guilleminault C. Disorders of excessive sleepiness. Ann Clin Res 1985: 17: 209–219.
- 32 Pekkarinen T, Partinen M, Pelkonen R, Livanainen M. Sleep apnea and daytime sleepiness in acromegaly. Clin Endocrinol 1987: 27: 649–654.
- 33 Cadieux RJ, Kales A, Santen RJ, Bixler EO, Gorden R. Endoscopic findings in sleep apnea associated with acromegaly. J Clin Endocrinol Metab 1982: 55: 18–22.
- 34
Barnes AJ,
Pallis C,
Joplin GF.
Acromegali and narcolepsy.
Lancet
1979: ii: 332–333.
10.1016/S0140-6736(79)90346-5 Google Scholar
- 35 Bengtson BJ, Brummer R-JM, Eden S, Bosaeus I. Bodycomposition in acromegaly. Clin Endocrinol 1989: 30: 121–130.
- 36 Billiard M. Competition between the two types of sleep, and the recuperative function of REM sleep versus NREM sleep in narcoleptics. In: C Guilleminault, WC Dement, P Passousant, eds. Narcolepsy. New York : Spectrum, 1975; 77–96.
- 37 Agnew HW, Parker JC, Webb W, Williams RL. Amplitude measurement of the sleep electroencephalogram. Electroenceph Clin Neurophysiol 1967: 22: 84–86.
- 38 Smith JR, Karacan I. EEG sleep stage scoring by an automatic hybrid system. Electroenceph Clin Neurophysiol 1971: 31: 231–237.
- 39 Dumermuth G, Walz W, Scollo-Lavizzari G, Kleiner B. Spectral analysis of EEG activity in different sleep stages in normal adults. Europ Neurol 1972: 7: 265–296.
- 40 Kubicki SK, Hermann WH, Laudahn G. Factor analysis and EEG variables. Stuttgart : Gustav Fischer, 1980.
- 41 Borbely AA, Baumann F, Brandies D, Strauch I, Lehmann D. Sleep deprivation: effect on sleep stages and EEG power density in man. Electroenceph Clin Neurophysiol 1981: 51: 483–493.
- 42 Mathis P, Scheffner D, Benninger C. Spectral analysis of EEG: comparison of various spectral parameters. Electroenceph Clin Neurophysiol 1981: 52: 218–221.
- 43 Haykin S, Cadzow JA. Special issue on spectral estimation. Proc IEEE 1982: 70: 881–1136.
- 44 Samson-Dollfus [!], Nogues B, Menard JF, Bertoldi-Lefever I, Geffroy D. Delta, theta, alpha and beta power spectrum of sleep electroencephalogram in infants aged two to eleven months. Sleep 1983: 6: 376–383.
- 45 Sinha AK, Smythe H, Zarcone VP, Barchas JD, Dement WC. Human sleep electroencephalogram: a damped oscillatory phenomenon. J Theor Biol 1972: 35: 387–393.
- 46 Church MW, March JD, Hibi S, Benson K, Cavness C, Feinberg I. Changes in frequency and amplitude of delta activity during sleep. Electroenceph Clin Neurophysiol 1975: 39: 1–7.
- 47 Feinberg I, March JD, Fein G, Floyd TC, Walker JM, Price L. Period and amplitude analysis of 0.5–3 c/sec activity in NREM sleep of young adults. Electroenceph Clin Neurophysiol 1978: 44: 202–213.
- 48 Dumermuth G, Lance B, Lehmann D, Meir CA, Dinkelmann R, Molinari L. Spectral analysis of all night sleep EEG in health adults. Eur Neurol 1983: 22: 322–339.
- 49 Lehmann D, Ozaki H, Pal I. Averaging of spectral power and phase via vector diagram best fits without reference electrode or reference channel. Electroenceph Clin Neurophysiol 1986: 64: 350–363.
- 50 Achermann P, Borbely AA. Dynamics of EEG slow wave activity during physiological sleep after administration of benzodiazepine hypnotics. Human Neurobiol 1987: 6: 203–210.
- 51 Dumermuth G, Molinari L. Spectral analysis of EEG background activity. In: AS Gevins, A Remond, eds. Handbook of electroencephalography and clinical neurophysiology, Vol 1. Methods of analysis of brain electrical and magnetic signals. New York : Elsevier, 1987: 85–129.
- 52 Kuwahara H, Higashi H, Mizuki Y, Matsunari S., Tanaka M, Inanaga K. Automatic real time analysis of human sleep stages by a interval histogram method. Electroenceph Clin Neurophysiol 1988: 70: 220–229.
- 53 Brunet D, Nish D, Maclean AW, Coulter M. Knowles JB. The time course of process S: comparison of visually scored slow wave sleep and power spectral analysis. Electroencephal Clin Neurophysiol 1988: 70: 278–280.
- 54 Salinsky M, Goins S, Sutula D, Roscoe D, Weber S. Comparison of sleep staging by polygraph and color density spectral array. Sleep 1988: 11: 131–138.
- 55 Borbely AA, Achermann P, Trachsel L, Tobler I. Sleep initiation and initial sleep intensity: interaction of ho-meostatic and circadian mechanisms. J Biol Rhythms 1989: 4: 149–160.
- 56 Dijk DJ, Brunner PD, Borbely AA. Time course of EEG density during long sleep in humans. Am J Physiol 1990: 258: R650–661.
- 57 Williams RL, Karacan I, Hurch C. Electroencephalography of human sleep: clinical applications. New York : Wiley, 1974.
- 58 Giwercman B, Giwercman A, Kastrup K, Skakkebæk N. Age- and sex-related variation in plasma concentration of somatomedin C in normal children and adults. Ugeskr Lzger 1987: 149: 1320–1323.
- 59 Lindholm J, Giwercman B, Giwercman A, Astrup J, Bjerre P, Skakkebæk NE. Investigation of the criteria for assessing the outcome of treatment in acromegaly. Clinical Endocrinology 1987: 27: 553–562.
- 60 Lopes de Silva F. EEG analysis: theory and practice. Basic statistical properties: sampling, probability distributions, correlation functions, and spectra. In: E. Niedermeyer F Lopes de Silva, eds. Electroencephalography: basic principles, clinical applications and related fields. Baltimore : Urban & Schwarzenberg, 1987: 871–897.
- 61 Makhoul J. Linear prediction. Proc IEEE 1975: 63: 561–580.
- 62 Dempster AP. Covariance selection. Biometrics 1972: 28: 157–175.
- 63 L Sachs, ed. Applied statistics. A handbook of technics. New York : Springer Verlag, 1978.
- 64 Whittaker J. Graphical models in applied multivariate statistics. New York : Wiley, 1990.
- 65 Roffwarg HP, Muzio JN, Dement WC. Ontogenic development of the human sleep cycle. Science 1966: 152: 604–619.
- 66
Duffy FH.
Topographic mapping of brain electrical activity.
Boston
,
MA
: Butterworth, 1986.
10.1016/B978-0-409-90008-8.50031-6 Google Scholar
- 67 Jonkman EJ, Van Huffelen AC, Pfurtscheller G. Quantitative EEG. In: FH Lopes de Silva, W Storm van Leeuwen, A Remand, eds. Clinical applications of computer analysis of EEG and other neurophysiological signals. Amsterdam : Elsevier 1986: 209–220.
- 68 Nistico G, De Sarro GB, Bagetta G, Muller EE. Behavioural and electrocortical spectrum power effect of growth hormone releasing factor in rats. Neuropharmacol 1987: 26: 75–78.
- 69 Nuwer MR. Quantitative EEG: techniques and problems of frequency analysis and topographic mapping. J Clin Neurophysiol 1988: 5: 1–43.
- 70 Huttenlocher PR. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 1979: 163: 195–205.
- 71 Orr WC, Vogel GW, Stahl ML, Griffiths WJ, Seely JR. Sleep pattern in growth hormone deficient children and age-matched controls: developmental consideration. Neuroendocrinology 1977: 24: 347–352.
- 72 Taylor BJ, Brook CGD. Sleep in growth disorders. Arch Dis Child 1986: 61: 754–760.
- 73 ÅStröm C, Trojaborg W. Relationship of Age to Power Spectrum Analysis of EEG During Sleep. J Clin Neurophysiol 1992: 9: 424–430.
- 74 Smith JR, Karacan I, Yang M. Ontogeny of delta activity during human sleep. Electroenceph Clin Neurophysiol 1977: 43: 229–237.
- 75 Ehlers CL, Kupfer DJ. Effects of age on delta and REM sleep parameters. Electroenceph Clin Neurophysiol 1989: 72: 118–125.
- 76 Dijk DJ, Beersma DGM, Van Den Hoofdakker RH. All night spectral analysis of EEG sleep in young adult and middle-aged male subjects. Neurobiology of Aging 1989: 10: 677–682.
- 77 Kimura F, Tsai CW. Ultradian rhythm of growth hormone secretion and sleep in adult male rat. J Physiol 1984: 353: 305–315.
- 78 Ehlers CL, Reed TK, Henriksen SJ. Effects of corticotropinreleasing factor and growth hormone releasing factor on sleep and activity in rats. Neuroendocrinology 1986: 42: 467–474.
- 79 ÅStröm C, Jochumsen PL. Decrease in delta sleep in growth hormone deficiency assessed by a new power spectrum analysis. Sleep 1989: 12: 508–515.
- 80 Hewerth J. Autopsy in growth hormone deficiency. J Endocrinol 1944: 3: 397–400.
- 81 ÅStröm C, Trojaborg W. Effect of growth hormone on human sleep energy. Clinical Endocrinology 1992: 36: 241–245.
- 82 ÅStröm C. Sleep and growth hormone. In: J Horne, ed. Sleep 90. Bochum : Pontenagel Press, 1990: 457–459.
- 83 ÅStröm C, Lindholm J. Growth hormone deficient young adults have decreased deep sleep. Neuroendocrinology 1990: 51: 82–84.
- 84 ÅStröm C, Christensen L, Gjerris F, Trojaborg W. Sleep in acromegaly before and after treatment with adenomectomy. Neuroendocrinology 1991: 53: 328–331.
- 85 Lugaresi E, Coccacna G, [!]. Mantovani Hypersomnia with periodic apnea. New York : Spectrum, 1978: 91–94.
- 86 Olesen J. Classification and diagnostic criteria for headache disorders, cranial neuralgias and facial pain. Cephalalgia 1988: 8 [!](suppl 7): 59.
- 87 Linfoot JA, Garcia JF, Wei W, Fink R, Sarin J, Born JL, Lawrence JH. Human growth hormone levels in cerebrospinal fluid. J Clin Endocr 1970: 31: 230–232.
- 88 Nicolini A, Buonaguidi R, Ferdechini M, Carpi A. Relationship between the circulating levels of adenohypophyseal hormones in blood and in cerebrospinal fluid. J Neurol Neurosurg and Psychiat 1984: 47: 710–714.
- 89 Gjerris A, Gjerris F, Soelberg-Sørensen P et al. Do concentrations of neurotransmitters measured in lumbar cerebrospinal fluid reflect the concentrations at brain level. Acta Neurochir 1988: 91: 55–59.
- 90 Jørcensen KD. Comparison of the pharmacological properties of pituitary and biosynthetic human growth hormone. Demonstration of barbital sleep effects of human growth hormone in rats. Acta Endocrinol 1987: 114: 124–131.
- 91 ÅStröm C, Pedersen SA, Lindholm J. The influence of growth hormone on sleep in adults with growth hormone deficiency. Clinical Endocrinology 1990: 33: 495–500.
- 92 Drucker-Colin RR, Spanis CW, Hunyadi J, Sassin JF, McGaugh JL. Growth hormone effects on sleep and wakefulness in the rat. Neuroendocrinology 1975: 18: 1–8.
- 93 Stern WC, Morgane PJ. Sleep and memory: effects of growth hormone on sleep, brain neurochemistry and behavior. In: RR Drucker-Colin, JL McGaugh, eds. Neurobiology of sleep and memory. New York : Academic Press, 1977: 373–400.
- 94 Obal F, Alföldi P, Cady A, Johannsen L, Sary G, Krueger JM. Growth hormone releasing factor enhances sleep in rats and rabbits. Am J Physiol 1988: 255: 310–316.
- 95 Mendelson WB, Slater S, Gold P, Gillin CJ. The effect of growth hormone administration on human sleep: a dose response study. Biological Psychiatry 1980: 15: 613–618.
- 96 Hoddes ES. Effect of growth hormone. Sleep 1979: 1: 287–292.
- 97 Greenberg R, Pearlman C. An approach to the adaptive role of REM sleep. Perspect Biol Med 1974: 17: 513–519.
- 98 Garry P, Rousel B, Cohen R et al. Diurnal administration of human growth hormone releasing factor does not modify sleep and sleep related growth hormone secretion in normal young men. Acta Endocrinol 1985: 110: 158–163.
- 99 Nissley PS. Growth factors. In: KL Backer, ed. Principles and practice of endocrinology and metabolism. Philadelphia Lippencott, 1990: 1315–1321.
- 100 Jouvet M. The role of monoamines and acetylcholine containing neurons in the regulation of the sleep-waking cycle. Science 1975: 189: 55–58.
- 101
Sakai K.
Central mechanism of paradoxical sleep.
Exp Brain Res
1984: 8: 3–18.
10.1007/978-3-642-69554-4_1 Google Scholar
- 102 Ghigo E, Mazza E, Imperiale E. Effect of the enhancement of the cholinergic activity on growth hormone secretion in children. J Endocrinol Invest 1989: 12 (suppl 2): 13.
- 103 Sallanon M, Denoyer M, Chastrette N, Cespuglio R, Jouvet M. Possible involvement of hypothalamic structures in sleep waking regulation. 10th Congr. ESRS book, 1990 May: 48.