Diabetes Research and Clinical Practice
Volume 91, Issue 2 , Pages 129-137 , February 2011

Diabetes and sleep: A complex cause-and-effect relationship

  • Mark T.U. Barone

      Affiliations

    • Instituto de Ciências Biomédicas, Universidade de São Paulo (ICB-USP), Brazil
    • Corresponding Author InformationCorresponding author at: Departamento de Fisiologia e Biofísica, Instituto de Ciências Biomédicas, Universidade de São Paulo (ICB-USP), Av. Prof. Lineu Prestes, 1524 (ICB I), Cidade Universitária, 05508-900, São Paulo/SP, Brazil. Tel.: +55 11 3717 1997; fax: +55 11 3091 7254.
  • ,
  • Luiz Menna-Barreto

      Affiliations

    • Escola de Artes, Ciências e Humanidades, Universidade de São Paulo (EACH-USP), Brazil

Received 12 May 2010 ,Revised 26 July 2010 ,Accepted 29 July 2010.

References 

  1. Sicree RJ, Shaw J, Zimmet P. The global burden, diabetes and impaired glucose tolerance. IDF diabetes atlas. 4th ed.. Brussels: International Diabetes Federation; 2009;p. 1–105
  2. Knutson KL, Ryden AM, Mander BA, Van Cauter E. Role of sleep duration and quality in the risk and severity of type 2 diabetes mellitus. Arch Intern Med. 2006;166:1768–1774
  3. Trento M, Broglio F, Riganti F, Basile M, Borgo E, Kucich C, et al. Sleep abnormalities in type 2 diabetes may be associated with glycemic control. Acta Diabetol. 2008;45:225–229
  4. West SD, Nicoll DJ, Stradling JR. Prevalence of obstructive sleep apnoea in men with type 2 diabetes. Thorax. 2006;61:945–950
  5. Villa MP, Multari G, Montesano M, Pagani J, Cervoni M, Midulla F, et al. Sleep apnoea in children with diabetes mellitus: effect of glycaemic control. Diabetologia. 2000;43:696–702
  6. James PT. Obesity: the worldwide epidemic. Clin Dermatol. 2004;22:276–280
  7. Chaput JP, Després JP, Bouchard C, Astrup A, Tremblay A. Sleep duration as a risk factor for the development of type 2 diabetes or impaired glucose tolerance: analyses of the Quebec Family Study. Sleep Med. 2009;10:919–924
  8. Van Cauter E, Splegel K, Tasali E, Leproult R. Metabolic consequences of sleep and sleep loss. Sleep Med. 2008;9:S23–S28
  9. Pillar G, Shehadeh N. Abdominal fat and sleep apnea: the chicken or the egg?. Diabetes Care. 2008;31(Suppl. 2):S303–S309
  10. Spiegel K, Leproult R, Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet. 1999;354:1435–1439
  11. Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E. Sleep loss: a novel risk factor for insulin resistance and type 2 diabetes. J Appl Physiol. 2005;99:2008–2019
  12. Mallon L, Broman JE, Hetta J. High incidence of diabetes in men with sleep complaints or short sleep duration: a 12-year follow-up study of a middle-aged population. Diabetes Care. 2005;28:2762–2767
  13. Gonzalez-Ortiz M, Martinez-Abundis E, Balcazar-Munoz BR, Pascoe-Gonzalez S. Effect of sleep deprivation on insulin sensitivity and cortisol concentration in healthy subjects. Diabetes Nutr Metab. 2000;13:80–83
  14. Gangwisch JE, Heymsfield SB, Boden-Albala B, Bujis RM, Kreier F, Pickering TG, et al. Sleep duration as a risk factor for diabetes incidence in a large US sample. Sleep. 2007;30:1667–1673
  15. Nakajima H, Kaneita Y, Yokoyama E, Harano S, Tamaki T, Ibuka E, et al. Association between sleep duration and hemoglobin A1c level. Sleep Med. 2008;9:745–752
  16. Yaggi HK, Araujo AB, McKinlay JB. Sleep duration as a risk factor for the development of type 2 diabetes. Diabetes Care. 2006;29:657–661
  17. Punjabi NM. The epidemiology of adult obstructive sleep apnea. Proc Am Thorac Soc. 2008;5:136–143
  18. The Report of an American Academy of Sleep Medicine Task Force . Sleep-related breathing disorders in adults: recommendations for syndrome definition and measurement techniques in clinical research. Sleep. 1999;22:667–689
  19. National Center on Sleep Disorders Research and National Heart Lung and Blood Institute of the National Institutes of Health . National sleep disorders research plan, section 5 – sleep disorders: sleep-disordered breathing. 2003;accessed May 12, 2010. Available from: http://www.nhlbi.nih.gov/health/prof/sleep/res_plan/section5/section5a.html
  20. Peppard PE, Young T, Palta M, Dempsey J, Skatrud J. Longitudinal study of moderate weight change and sleep-disordered breathing. JAMA. 2000;284:3015–3021
  21. Vioque J, Torres A, Quiles J. Time spent watching television, sleep duration and obesity in adults living in Valencia, Spain. Int J Obes. 2000;24:1683–1688
  22. Al Mamun A, Lawlor DA, Cramb S, O’Callaghan M, Williams G, Najman J. Do childhood sleeping problems predict obesity in young adulthood? Evidence from a prospective birth cohort study. Am J Epidemiol. 2007;166:1368–1373
  23. Coughlin SR, Mawdsley L, Mugarza JA, Calverley PMA, Wilding JPH. Obstructive sleep apnoea is independently associated with an increased prevalence of metabolic syndrome. Eur Heart J. 2004;25:735–741
  24. Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C. Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004;109:433–438
  25. Shaw JE, Punjabi NM, Wilding JP, Alberti KGMM, Zimmet PZ. Sleep-disordered breathing and type 2 diabetes—a report from the International Diabetes Federation Taskforce on Epidemiology and Prevention. Diabetes Res Clin Pract. 2008;81:2–12
  26. Punjabi NM, Beamer BA. Alterations in glucose disposal in sleep-disordered breathing. Am J Respir Crit Care Med. 2009;179:235–240
  27. Ip MS, Lam B, Ng MM, Lam WK, Tsang KW, Lam KS. Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med. 2002;165:670–676
  28. Punjabi NM, Ahmed MM, Polotsky VY, Beamer BA, O’Donnell CP. Sleep-disordered breathing, glucose intolerance, and insulin resistance. Respir Physiol Neurobiol. 2003;136:167–178
  29. Punjabi NM, Polotsky VY. Disorders of glucose metabolism in sleep apnea. J Appl Physiol. 2005;99:1998–2007
  30. Aronsohn RS, Whitmore H, Van Cauter E, Tasali E. Impact of untreated obstructive sleep apnea on glucose control in type 2 diabetes. Am J Respir Crit Care Med. 2010;181:507–513
  31. Kawakami N, Takatsuka N, Shimizu H. Sleep disturbance and onset of type 2 diabetes. Diabetes Care. 2004;27:282–283
  32. Meisinger C, Heier M, Loewel H. Study MKAC. Sleep disturbance as a predictor of type 2 diabetes mellitus in men and women from the general population. Diabetologia. 2005;48:235–241
  33. Tasali E, Mokhlesi B, Van Cauter E. Obstructive sleep apnea and type 2 diabetes: interacting epidemics. Chest. 2008;133:496–506
  34. Chaput JP, Despres JP, Bouchard C, Tremblay A. Short sleep duration is associated with reduced leptin levels and increased adiposity: results from the Quebec Family Study. Obesity. 2007;15:253–261
  35. Freemantle N, Holmes J, Hockey A, Kumar S. How strong is the association between abdominal obesity and the incidence of type 2 diabetes?. Int J Clin Pract. 2008;62:1391–1396
  36. Pallayova M, Donic V, Tomori Z. Beneficial effects of severe sleep apnea therapy on nocturnal glucose control in persons with type 2 diabetes mellitus. Diabetes Res Clin Pract. 2008;81:e8–e11
  37. Leproult R, Copinschi G, Buxton O, VanCauter E. Sleep loss results in an elevation of cortisol levels the next evening. Sleep. 1997;20:865–870
  38. Smith ML, Niedermaier ONW, Hardy SM, Decker MJ, Strohl KP. Role of hypoxemia in sleep apnea-induced sympathoexcitation. J Auton Nerv Syst. 1996;56:184–190
  39. Narkiewicz K, Somers VK. Sympathetic nerve activity in obstructive sleep apnoea. Acta Physiol. 2003;177:385–390
  40. Leuenberger UA, Hogeman CS, Quraishi S, Linton-Frazier L, Gray KS. Short-term intermittent hypoxia enhances sympathetic responses to continuous hypoxia in humans. J Appl Physiol. 2007;103:835–842
  41. Xie AL, Skatrud JB, Puleo DS, Morgan BJ. Exposure to hypoxia produces long-lasting sympathetic activation in humans. J Appl Physiol. 2001;91:1555–1562
  42. Somers VK, Dyken ME, Clary MP, Abboud FM. Sympathetic neural mechanisms in obstructive sleep-apnea. J Clin Invest. 1995;96:1897–1904
  43. Straznicky NE, Eikelis N, Lambert EA, Esler MD. Mediators of sympathetic activation in metabolic syndrome obesity. Curr Hypertens Rep. 2008;10:440–447
  44. Dijk DJ. Slow-wave sleep, diabetes, and the sympathetic nervous system. Proc Natl Acad Sci USA. 2008;105:1107–1108
  45. Sandoval DA, Davis SN. Leptin – metabolic control and regulation. J Diabetes Complications. 2003;17:108–113
  46. Balbo M, Leproult R, Van Cauter E. Impact of sleep and its disturbances on hypothalamo–pituitary–adrenal axis activity. Int J Endocrinol. 2010;2010:1–16
  47. Qi D, Rodrigues B. Glucocorticoids produce whole body insulin resistance with changes in cardiac metabolism. Am J Physiol Endocrinol Metab. 2007;292:E654–E667
  48. Roberge C, Carpentier AC, Langlois MF, Baillargeon JP, Ardilouze JL, Maheux P, et al. Adrenocortical dysregulation as a major player in insulin resistance and onset of obesity. Am J Physiol Endocrinol Metab. 2007;293:E1465–E1478
  49. Buckley TM, Schatzberg AF. Review: 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. 2005;90:3106–3114
  50. Gale SM, Castracane VD, Mantzoros CS. Energy homeostasis, obesity and eating disorders: recent advances in endocrinology. J Nutr. 2004;134:295–298
  51. Farooqi IS, Jebb SA, Langmack G, Lawrence E, Cheetham CH, Prentice AM, et al. Effects of recombinant leptin therapy in a child with congenital leptin deficiency. N Engl J Med. 1999;341:879–884
  52. Prieur X, Tung YCL, Griffin JL, Farooqi IS, O’Rahilly S, Coll AP. Leptin regulates peripheral lipid metabolism primarily through central effects on food intake. Endocrinology. 2008;149:5432–5439
  53. Martin SS, Qasim A, Reilly MP. Leptin resistance – a possible interface of inflammation and metabolism in obesity-related cardiovascular disease. J Am Coll Cardiol. 2008;52:1201–1210
  54. Chen K, Li FH, Li J, Cai H, Strom S, Bisello A, et al. Induction of leptin resistance through direct interaction of C-reactive protein with leptin. Nat Med. 2006;12:425–432
  55. Ip MSM, Lam KSL, Ho CM, Tsang KWT, Lam WK. Serum leptin and vascular risk factors in obstructive sleep apnea. Chest. 2000;118:580–586
  56. Gil-Campos M, Aguilera CM, Canete R, Gil A. Ghrelin: a hormone regulating food intake and energy homeostasis. Br J Nutr. 2006;96:201–226
  57. Knutson KL, Van Cauter E. Associations between sleep loss and increased risk of obesity and diabetes. Ann N Y Acad Sci. 2008;1129:287–304
  58. Spiegel K, Leproult R, L’Hermite-Baleriaux M, Copinschi G, Penev PD, Van Cauter E. Leptin levels are dependent on sleep duration: relationships with sympathovagal balance, carbohydrate regulation, cortisol, and thyrotropin. J Clin Endocrinol Metab. 2004;89:5762–5771
  59. Spiegel K, Tasali E, Penev P, 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. 2004;141:846–850
  60. Nedeltcheva AV, Kilkus JM, Imperial J, Kasza K, Schoeller DA, Penev PD. Sleep curtailment is accompanied by increased intake of calories from snacks. Am J Clin Nutr. 2009;89:126–133
  61. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw. 2006;17:4–12
  62. Meier-Ewert HK, Ridker PM, Rifai N, Regan MM, Price NJ, Dinges DF, et al. Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. J Am Coll Cardiol. 2004;43:678–683
  63. Liu H, Liu J, Xiong S, Shen G, Zhang Z, Xu Y. The change of interleukin-6 and tumor necrosis factor in patients with obstructive sleep apnea syndrome. J Tongji Med Univ. 2000;20:200–202
  64. Alberti A, Sarchielli P, Gallinella E, Floridi A, Floridi A, Mazzotta G, et al. Plasma cytokine levels in patients with obstructive sleep apnea syndrome: a preliminary study. J Sleep Res. 2003;12:305–311
  65. Shamsuzzaman ASM, Winnicki M, Lanfranchi P, Wolk R, Kara T, Accurso V, et al. Elevated c-reactive protein in patients with obstructive sleep apnea. Circulation. 2002;105:2462–2464
  66. Teramoto S, Yamamoto H, Ouchi Y. Increased C-reactive protein and increased plasma interleukin-6 may synergistically affect the progression of coronary atherosclerosis in obstructive sleep apnea syndrome. Circulation. 2003;107:E40–E140
  67. Vgontzas AN, Papanicolaou DA, Bixler EO, Hopper K, Lotsikas A, Lin HM, et al. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Clin Endocrinol Metab. 2000;85:1151–1158
  68. Kapsimalis F, Richardson G, Opp MR, Kryger M. Cytokines and normal sleep. Curr Opin Pulm Med. 2005;11:481–484
  69. Pillar G, Schuscheim G, Weiss R, Malhotra A, McCowen KC, Shlitner A, et al. Interactions between hypoglycemia and sleep architecture in children with type 1 diabetes mellitus. J Pediatr. 2003;142:163–168
  70. Jauch-Chara K, Schmid SM, Hallschmid M, Born J, Schultes B. Altered neuroendocrine sleep architecture in patients with type 1 diabetes. Diabetes Care. 2008;31:1183–1188
  71. Hayashino Y, Yamazaki S, Nakayama T, Sokejima S, Fukuhara S. Relationship between diabetes mellitus and excessive sleepiness during driving. Exp Clin Endocrinol Diabetes. 2008;116:1–5
  72. Fruehwald-Schultes B, Kern W, Born J, Fehm HL, Peters A. Hyperinsulinemia causes activation of the hypothalamus–pituitary–adrenal axis in humans. Int J Obes Relat Metab Disord. 2001;25(1):S38–S40
  73. Chan O, Inouye K, Riddell MC, Vranic M, Matthews SG. Diabetes and the hypothalamo–pituitary–adrenal (HPA) axis. Minerva Endocrinol. 2003;28:87–102
  74. Vgontzas AN, Zoumakis E, Bixler EO, Lin HM, Follett H, Kales A, et al. Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines. J Clin Endocrinol Metab. 2004;89:2119–2126
  75. Vgontzas AN, Papanicolaou DA, Bixler EO, Kales A, Tyson K, Chrousos GP. Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab. 1997;82:1313–1316

PII: S0168-8227(10)00388-8

doi: 10.1016/j.diabres.2010.07.011

Diabetes Research and Clinical Practice
Volume 91, Issue 2 , Pages 129-137 , February 2011