Sleep loss: A novel risk factor for insulin resistance and Type 2 diabetes

Journal of Applied Physiology

Volumn 99, Issue 5, 2005, Pages 2008-2019

  Spiegel, Karine ^a   Knutson, Kristen ^b   Leproult, Rachel ^b   Tasali, Esra ^b   Van Cauter, Eve ^b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Appetite regulation; Glucose metabolism; Obesity; Obstructive sleep apnea; Sympathovagal balance

Indexed keywords

GHRELIN; LEPTIN;

APPETITE; BREATHING DISORDER; DISEASE EXACERBATION; DISEASE SEVERITY; ENDEMIC DISEASE; FEEDING; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HORMONAL REGULATION; HUMAN; HUNGER; HYPOXIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; NEUROENDOCRINE SYSTEM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OVERNUTRITION; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SLEEP DISORDER; WEIGHT GAIN;

DIABETES MELLITUS, TYPE 2; GLUCARIC ACID; HUMANS; INSULIN RESISTANCE; RISK FACTORS; SLEEP APNEA, OBSTRUCTIVE; SYMPATHETIC NERVOUS SYSTEM; VAGUS NERVE;

EID: 27544478983     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00660.2005     Document Type: Review

References (98)

1. Ahima RS, Saper CB, Flier JS, and Elmquist JK. Leptin regulation of neuroendocrine systems. Front Neuroendocrinol 21: 263-307, 2000.
2. Ayas NT, White DP, Manson JE, Stampfer MJ, Speizer FE, Malhotra A, and Hu FB. A prospective study of sleep duration and coronary heart disease in women. Arch Intern Med 163: 205-209, 2003.
3. Bauer J, Hafner S, Kachele H, Wirsching M, and Dahlbender RW. [The burn-out syndrome and restoring mental health at the working place]. Psychother Psychosom Med Psychol 53: 213-222, 2003.
4. Bergman RN, Ader M, Huecking K, and Van Citters G. Accurate assessment of beta-cell function: the hyperbolic correction. Diabetes 51, Suppl 1: S212-S220, 2002.
5. Bliwise DL. Historical change in the report of daytime fatigue. Sleep 19: 462-464, 1996.
6. Bonnet MH, Berry RB, and Arand DL. Metabolism during normal, fragmented, and recovery sleep. J Appl Physiol 71: 1112-1118, 1991.
7. Boyle PJ, Scott JC, Krentz AJ, Nagy RJ, Comstock E, and Hoffman C. Diminished brain glucose metabolism is a significant determinant for falling rates of systemic glucose utilization during sleep in normal humans. J Clin Invest 93: 529-535, 1994.
8. Buchsbaum MS, Gillin JC, Wu J, Hazlett E, Sicotte N, Dupont RM, and Bunney WEJ. Regional cerebral glucose metabolic rate in human sleep assessed by positron emission tomography. Life Sci 45: 1349-1356, 1989.
9. Burgess HJ, Penev PD, Schneider R, and Van Cauter E. Estimating cardiac autonomic activity during sleep: impedance cardiography, spectral analysis, and Poincare plots. Clin Neurophysiol 115: 19-28, 2004.
10. Chin K, Shimizu K, Nakamura T, Narai N, Masuzaki H, Ogawa Y, Mishima M, Nakao K, and Ohi M. Changes in intra-abdominal visceral fat and serum leptin levels in patients with obstructive sleep apnea syndrome following nasal continuous positive airway pressure therapy. Circulation 100: 706-712, 1999.
11. Chin-Chance C, Polonsky KS, and Schoeller DA. Twenty-four-hour leptin levels respond to cumulative short-term energy imbalance and predict subsequent intake. J Clin Endocrinol Metab 85: 2685-2691, 2000.
12. Coughlin SR, Mawdsley L, Mugarza JA, Calverley PM, and Wilding JP. Obstructive sleep apnoea is independently associated with an increased prevalence of metabolic syndrome. Eur Heart J 25: 735-741, 2004.
13. Danguir J and Nicolaidis S. Dependence of sleep on nutrients' availability. Physiol Behav 22: 735-740, 1979.
14. Dinges DF and Chugh DK. Physiological correlates of sleep deprivation. In: Physiology, Stress, and Malnutrition: Functional Correlates, Nutritional Intervention, edited by Kinney JM and Tucker HN. Philadelphia, PA: Lippincott-Raven, 1997.
15. Dzaja A, Dalal MA, Himmerich H, Uhr M, Pollmacher T, and Schuld A. Sleep enhances nocturnal plasma ghrelin levels in healthy subjects. Am J Physiol Endocrinol Metab 286: E963-E967, 2004.
16. Ekstedt M, Akerstedt T, and Soderstrom M. Microarousals during sleep are associated with increased levels of lipids, cortisol, and blood pressure. Psychosom Med 66: 925-931, 2004.
17. Elmasry A, Lindberg E, Berne C, Janson C, Gislason T, Awad Tageldin M, and Boman G. Sleep-disordered breathing and glucose metabolism in hypertensive men: a population-based study. J Intern Med 249: 153-161, 2001.
18. Estabrooke IV, McCarthy MT, Ko E, Chou TC, Chemelli RM, Yanagisawa M, Saper CB, and Scammell TE. Fos expression in orexin neurons varies with behavioral state. J Neurosci 21: 1656-1662, 2001.
19. Flegal KM, Carroll MD, Kuczmarski RJ, and Johnson CL. Overweight and obesity in the United States: prevalence and trends, 1960-1994. Int J Obes Relat Metab Disord 22: 39-47, 1998.
20. Flegal KM, Carroll MD, Ogden CL, and Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA 288: 1723-1727, 2002.
21. Garcia G, Freeman R, Supiano M, Smith M, Galecki A, and Halter J. Glucose metabolism in older adults: a study including subjects more than 80 years of age. J Am Geriatr Soc 45: 813-817, 1997.
22. Gottlieb DJ, Punjabi NM, Newman AB, Resnick HE, Redline S, Baldwin CM, and Nieto FJ. Association of sleep time with diabetes mellitus and impaired glucose tolerance. Arch Intern Med 165: 863-867, 2005.
23. Gumbiner B, Polonsky KS, Beltz WF, Wallace P, Brechtel G, and Fink RI. Effects of aging on insulin secretion. Diabetes 38: 1549-1556, 1989.
24. Gupta NK, Mueller WH, Chan W, and Meininger JC. Is obesity associated with poor sleep quality in adolescents? Am J Hum Biol 14: 762-768, 2002.
25. Harrison Y and Horne JA. Long-term extension to sleep-are we really chronically sleep deprived? Psychophysiology 33: 22-30, 1996.
26. Harsch IA, Konturek PC, Koebnick C, Kuehnlein PP, Fuchs FS, Pour Schahin S, Wiest GH, Hahn EG, Lohmann T, and Ficker JH. Leptin and ghrelin levels in patients with obstructive sleep apnoea: effect of CPAP treatment. Eur Respir J 22: 251-257, 2003.
27. Harsch IA, Schahin SP, Bruckner K, Radespiel-Troger M, Fuchs FS, Hahn EG, Konturek PC, Lohmann T, and Ficker JH. The effect of continuous positive airway pressure treatment on insulin sensitivity in patients with obstructive sleep apnoea syndrome and type 2 diabetes. Respiration 71: 252-259, 2004.
28. Harsch IA, Schahin SP, Radespiel-Troger M, Weintz O, Jahreiss H, Fuchs FS, Wiest GH, Hahn EG, Lohmann T, Konturek PC, and Ficker JH. Continuous positive airway pressure treatment rapidly improves insulin sensitivity in patients with obstructive sleep apnea syndrome. Am J Respir Crit Care Med 169: 156-162, 2004.
29. Hasler G, Buysse DJ, Klaghofer R, Gamma A, Ajdacic V, Eich D, Rossler W, and Angst J. The association between short sleep duration and obesity in young adults: a 13-year prospective study. Sleep 27: 661-666, 2004.
30. Havel PJ. Peripheral signals conveying metabolic information to the brain: short-term and long-term regulation of food intake and energy homeostasis. Exp Biol Med (Maywood) 226: 963-977, 2001.
31. Ip S, Lam K, Ho C, Tsang K, and Lam W. Serum leptin and vascular risk factors in obstructive sleep apnea. Chest 118: 580-586, 2000.
32. Ip SM, Lam N, Ng M, Lam WK, Tsang KW, and Lam KS. Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med 165: 670-676, 2002.
33. Jean-Louis G, Kripke DF, and Ancoli-Israel S. Sleep and quality of well-being. Sleep 23: 1115-1121, 2000.
34. Kahneman D, Krueger AB, Schkade DA, Schwarz N, and Stone AA. A survey method for characterizing daily life experience: the day reconstruction method. Science 306: 1776-1780, 2004.
35. Kamen PW, Krum H, and Tonkin AM. Poincaré plots of heart rate variability allows quantitative display of parasympathetic nervous activity in humans. Clin Sci (Lond) 91: 201-208, 1996.
36. Kolaczynski JW, Considine RV, Ohannesian J, Marco C, Opentanova I, Nyce MR, Myint M, and Caro JF. Responses of leptin to short-term fasting and refeeding in humans: a link with ketogenesis but not ketones themselves. Diabetes 45: 1511-1515, 1996.
37. Kripke DF, Garfinkel L, Wingard DL, Klauber MR, and Marler MR. Mortality associated with sleep duration and insomnia. Arch Gen Psychiatry 59: 131-136, 2002.
38. Kripke DF, Simons RN, Garfinkel L, and Hammond EC. Short and long sleep and sleeping pills. Is increased mortality associated? Arch Gen Psychiatry 36: 103-116, 1979.
39. Kuhn E, Brodan V, Brodanova M, and Rysanek K. Metabolic reflection of sleep deprivation. Act Nerv Super (Praha) 11: 165-174, 1969.
40. Locard E, Mamelle N, Billette A, Miginiac M, Munoz F, and Rey S. Risk factors of obesity in a five year old population. Parental versus environmental factors. Int J Obes Relat Metab Disord 16: 721-729, 1992.
41. Mander B, Colecchia E, Spiegel K, Kim R, Sannar E, and Van Cauter E. Short sleep: a risk factor for insulin resistance and obesity. Diabetes 50, Suppl 2: A45, 2001.
42. Maquet P. Positron emission tomography studies of sleep and sleep disorders. J Neurol 244 (4 Suppl 1): S23-S28, 1997.
43. Maquet P, Dive D, Salmon E, Sadzot B, Franco G, Poirrier R, and Franck G. Cerebral glucose utilization during stage 2 sleep in man. Brain Res 571: 149-153, 1992.
44. 18F]2-fluoro-2-deoxy- D-glucose method. Brain Res 513: 136-143, 1990.
45. Meisinger C, Heier M, Loewel H, and The MONICA/KORA Augsburg Cohort Study. Sleep disturbance as a predictor of type 2 diabetes mellitus in men and women from the general population. Diabetologia 48: 235-241, 2005.
46. Møller N, Jorgensen JOL, Schmitz O, Moller J, Christiansen JS, Alberti KGMM, and Orskov H. Effects of a growth hormone pulse on total and forearm substrate fluxes in humans. Am J Physiol Endocrinol Metab 258: E86-E91, 1990.
47. Mullington JM, Chan JL, Van Dongen HP, Szuba MP, Samaras J, Price NJ, Meier-Ewert HK, Dinges DF, and Mantzoros CS. Sleep loss reduces diurnal rhythm amplitude of leptin in healthy men. J Neuroendocrinol 15: 851-854, 2003.
48. National Sleep Foundation. 2000 "Sleep in America" Poll. Washington, DC: National Sleep Foundation, 2000.
49. National Sleep Foundation. 2001 "Sleep in America" Poll. Washington, DC: National Sleep Foundation, 2001, Executive summary.
50. National Sleep Foundation. 2002 "Sleep in America" Poll. Washington, DC: National Sleep Foundation, 2002.
51. Nilsson PM, Roost M, Engstrom G, Hedblad B, and Berglund G. Incidence of diabetes in middle-aged men is related to sleep disturbances. Diabetes Care 27: 2464-2469, 2004.
52. Opstad PK and Fonnum F. The effect of sustained military activities on performance decrement and endocrinological changes in man. NATO Seminar on the Human as a Living Element in Military Systems. Toronto, 1983.
53. Otzenberger H, Gronfier C, Simon C, Charloux A, Ehrhart J, Piquard F, and Brandenberger G. Dynamic heart rate variability: a tool for exploring sympathovagal balance continuously during sleep in men. Am J Physiol Heart Circ Physiol 275: H946-H950, 1998.
54. Persson HE and Svanborg E. Sleep deprivation worsens obstructive sleep apnea. Comparison between diurnal and nocturnal polysomonography. Chest 109: 645-650, 1996.
55. Plat L, Byrne MM, Sturis J, Polonsky KS, Mockel J, Fery F, and Van Cauter E. Effects of morning Cortisol elevation on insulin secretion and glucose regulation in humans. Am J Physiol Endocrinol Metab 270: E36-E42, 1996.
56. Plat L, Leproult R, L'Hermite-Baleriaux M, Fery F, Mockel J, Polonsky KS, and Van Cauter E. Metabolic effects of short-term elevations of plasma cortisol are more pronounced in the evening than in the morning. J Clin Endocrinol Metab 84: 3082-3092, 1999.
57. Prigeon RL, Kahn SE, and Porte D Jr. Changes in insulin sensitivity, glucose effectiveness, and B-cell function in regularly exercising subjects. Metabolism 44: 1259-1263, 1995.
58. Punjabi NM, Shahar E, Redline S, Gottlieb DJ, Givelber R, and Resnick HE. Sleep-disordered breathing, glucose intolerance, and insulin resistance: the Sleep Heart Health Study. Am J Epidemiol 160: 521-530, 2004.
59. Punjabi NM, Sorkin JD, Katzel L, Goldberf A, Schwartz A, and Smith PL. Sleep-disordered breathing and insulin resistance in middle aged and overweight men. Am J Respir Crit Care Med 165: 670-676, 2002.
60. Rechtschaffen A and Bergmann BM. Sleep deprivation in the rat by the disk-over-water method. Behav Brain Res 69: 55-63, 1995.
61. Rechtschaffen A, Bergmann BM, Everson CA, Kushida CA, and Gilliland MA. Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep 12: 68-87, 1989.
62. Rechtschaffen A, Gilliland MA, Bergmann BM, and Winter JB. Physiological correlates of prolonged sleep deprivation in rats. Science 221: 182-184, 1983.
63. Reilly J, Armstrong J, Dorosty A, Emmett P, Ness A, Rogers I, Steer C, and Sherriff A. Early life risk factors for obesity in childhood: cohort study. Br Med J doi:10.1136/bmj.38470.670903.E0, 2005.
64. Roehrs T, Shore E, Papineau K, Rosenthal L, and Roth T. A two-week Sleep extension in sleepy normals. Sleep 19: 576-582, 1996.
65. Sanner BM, Kollhosser P, Buechner N, Zidek W, and Tepel M. Influence of treatment on leptin levels in patients with obstructive sleep apnoea. Eur Respir J 23: 601-604, 2004.
66. Scheen AJ, Byrne MM, Plat L, Leproult R, and Van Cauter E. Relationships between sleep quality and glucose regulation in normal humans. Am J Physiol Endocrinol Metab 271: E261-E270, 1996.
67. Schoeller DA, Cella LK, Sinha MK, and Caro JF. Entrainment of the diurnal rhythm of plasma leptin to meal timing. J Clin Invest 100: 1882-1887, 1997.
68. Sekine M, Yamagami T, Handa K, Saito T, Nanri S, Kawaminami K, Tokui N, Yoshida K, and Kagamimori S. A dose-response relationship between short sleeping hours and childhood obesity: results of the Toyama Birth Cohort Study. Child Care Health Dev 28: 163-170, 2002.
69. Shimizu K, Chin K, Nakamura T, Masuzaki H, Ogawa Y, Hosokawa R, Niimi A, Hattori N, Nohara R, Sasayama S, Nakao K, Mishima M, and Ohi M. Plasma leptin levels and cardiac sympathetic function in patients with obstructive sleep apnoea-hypopnoea syndrome. Thorax 57: 429-434, 2002.
70. Simon C, Brandenberger G, and Follenius M. Ultradian oscillations of plasma glucose, insulin, and C-peptide in man during continuous enteral nutrition. J Clin Endocrinol Metab 64: 669-674, 1987.
71. Simon C, Brandenberger G, Saini J, Ehrhart J, and Follenius M. Slow oscillations of plasma glucose and insulin secretion rate are amplified during sleep in humans under continuous enteral nutrition. Sleep 17: 333-338, 1994.
72. Simon C, Gronfier C, Schlienger JL, and Brandenberger G. Circadian and ultradian variations of leptin in normal man under continuous enteral nutrition: relationship to sleep and body temperature. J Clin Endocrinol Metab 83: 1893-1899, 1998.
73. Sinton CM, Fitch TE, and Gershenfeld HK. The effects of leptin on REM sleep and slow wave delta in rats are reversed by food deprivation. J Sleep Res 8: 197-203, 1999.
74. Somers VK, Dyken ME, Clary MP, and Abboud FM. Sympathetic neural mechanisms in obstructive sleep apnea. J Clin Invest 96: 1897-1904, 1995.
75. Spiegel K, Leproult R, L'Hermite-Baleriaux M, Copinschi G, Penev PD, and Van Cauter E. Leptin levels are dependent on sleep duration: relationships with sympathovagal balance, carbohydrate regulation, cortisol, and thyrotropin. J Clin Endocrinol Metab 89: 5762-5771, 2004.
76. Spiegel K, Leproult R, and Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet 354: 1435-1439, 1999.
77. Spiegel K, Tasali E, Penev P, and Van Cauter E. Brief communication: sleep curtailment in healthy young men is associated with decreased leptin levels, elevated ghrelin levels, and increased hunger and appetite. Ann Intern Med 141: 846-850, 2004.
78. Svatikova A, Wolk R, Gami AS, Pohanka M, and Somers VK. Interactions between obstructive sleep apnea and the metabolic syndrome. Curr Diab Rep 5: 53-58, 2005.
79. Taheri S, Lin L, Austin D, Young T, and Mignot E. Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med 1: e62, 2004.
80. Taheri S, Zeitzer JM, and Mignot E. The role of hypocretins (orexins) in sleep regulation and narcolepsy. Annu Rev Neurosci 25: 283-313, 2002.
81. Tassone F, Lanfranco F, Gianotti L, Pivetti S, Navone F, Rossetto R, Grottoli S, Gai V, Ghigo E, and Maccario M. Obstructive sleep apnoea syndrome impairs insulin sensitivity independently of anthropometric variables. Clin Endocrinol (Oxf) 59: 374-379, 2003.
82. Thomas M, Balkin T, Sing H, Wesensten N, and Belenky G. PET imaging studies of sleep deprivation and sleep: implications for behavior and sleep function. In: 14th European Congress on Sleep Research. Madrid, Spain: Blackwell Science, 1998, p. 1-332.
83. Tiemeier B, Pelzer E, Jonck L, Moller HJ, and Rao ML. Plasma catecholamines and selective slow wave sleep deprivation. Neuropsychobiology 45: 81-86, 2002.
84. Van Cauter E, Blackman JD, Roland D, Spire JP, Refetoff S, and Polonsky KS. Modulation of glucose regulation and insulin secretion by circadian rhythmicity and sleep. J Clin Invest 88: 934-942, 1991.
85. Van Cauter E, Desir D, Decoster C, Fery F, and Balasse EO. Nocturnal decrease in glucose tolerance during constant glucose infusion. J Clin Endocrinol Metab 69: 604-611, 1989.
86. Van Cauter E, Knutson K, Leproult R, and Spiegel K. The impact of sleep deprivation on hormones and metabolism [Online]. Medscape Neurol Neurosurg 7, 2005. http://www.medscape.com/viewarticle/502825.
87. Van Cauter E, Polonsky KS, and Scheen AJ. Roles of circadian rhythmicity and sleep in human glucose regulation. Endocr Rev 18: 716-738, 1997.
88. VanHelder T and Radomski M. Sleep deprivation and the effect on exercise performance. Sports Med 7: 235-247, 1989.
89. VanHelder T, Symons JD, and Radomski MW. Effects of sleep deprivation and exercise on glucose tolerance. Aviat Space Environ Med 64: 487-492, 1993.
90. Vgontzas AN, Papanicolaou DA, Bixler EO, Hopper K, Lotsikas A, Lin HM, Kales A, and Chrousos GP. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia [see comments]. J Clin Endocrinol Metab 85: 1151-1158, 2000.
91. Vioque J, Torres A, and Quiles J. Time spent watching television, sleep duration and obesity in adults living in Valencia, Spain. Int J Obes Relat Metab Disord 24: 1683-1688, 2000.
92. Vondra K, Brodan V, Bass A, Kuhn E, Teisinger J, Andel M, and Veselkova A. Effects of sleep deprivation on the activity of selected metabolic enzymes in skeletal muscle. Eur J Appl Physiol 47: 41-46, 1981.
93. Vorona R, Winn M, Babineau T, Eng B, Feldman H, and Ware J. Overweight and obese patients in a primary care population report less sleep than patients with a normal body mass index. Arch Intern Med 165: 25-30, 2005.
94. Watanabe T, Mano T, Iwase S, Sugiyama Y, Okada H, Takeuchi S, Furui H, and Kobayashi F. Enhanced muscle sympathetic nerve activity during sleep apnea in the elderly. J Auton Nerv Syst 37: 223-226, 1992.
95. Wehr TA, Moul DE, Barbato G, Giesen HA, Seidel JA, Barker C, and Bender C. Conservation of photoperiod-responsive mechanisms in humans. Am J Physiol Regul Integr Comp Physiol 265: R846-R857, 1993.
96. Weikel JC, Wichniak A, Ising M, Brunner H, Friess E, Held K, Mathias S, Schmid DA, Uhr M, and Steiger A. Ghrelin promotes slow-wave sleep in humans. Am J Physiol Endocrinol Metab 284: E407-E415, 2003.
97. Yoshida Y, Fujiki N, Nakajima T, Ripley B, Matsumura H, Yoneda H, Mignot E, and Nishino S. Fluctuation of extracellular hypocretin-1 (orexin A) levels in the rat in relation to the light-dark cycle and sleep-wake activities. Eur J Neurosci 14: 1075-1081, 2001.
98. Young T, Palta M, Dempsey J, Skatrud J, Weber S, and Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 328: 1230-1235, 1993.