Sleep, sleep-disordered breathing and lipid homeostasis: Translational evidence from murine models and children

Clinical Lipidology

Volumn 7, Issue 2, 2012, Pages 203-214

  Bhattacharjee, Rakesh ^a   Hakim, Fahed ^a   Gozal, David ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

atherosclerosis; children; intermittent hypoxia; lipids; metabolism; obesity; obstructive sleep apnea; sleep; sleep fragmentation; sleep disordered breathing

Indexed keywords

C REACTIVE PROTEIN; CHOLESTEROL; HEMOGLOBIN; OXYHEMOGLOBIN; TRIACYLGLYCEROL;

ADENOTONSIL HYPERTROPHY; ADIPOSE TISSUE; APNEA HYPOPNEA INDEX; BODY MASS; CARDIOVASCULAR DISEASE; CHILD HEALTH; COGNITIVE DEFECT; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DYSLIPIDEMIA; EVIDENCE BASED MEDICINE; HEMOGLOBIN BLOOD LEVEL; HOMEOSTASIS; HUMAN; HYPERCAPNIA; HYPERTROPHY; HYPOXIA; INSULIN RESISTANCE; LIPID HOMEOSTASIS; LIPID METABOLISM; METABOLIC DISORDER; MORBIDITY; NONHUMAN; OBESITY; OXIDATIVE STRESS; OXYGEN SATURATION; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SLEEP APNEA SYNDROME; SLEEP DISORDERED BREATHING; SOMNOLENCE; TRANSLATIONAL RESEARCH;

EID: 84860184191     PISSN: 17460875     EISSN: 17584302     Source Type: Journal    
DOI: 10.2217/clp.12.11     Document Type: Review

References (94)

1. Montgomery-Downs HE, Gozal D. Toddler behavior following polysomnography: effects of unintended sleep disturbance. Sleep 29(10), 1282-1287 (2006). (Pubitemid 44571981)
2. O'Brien LM. The neurocognitive effects of sleep disruption in children and adolescents. Child Adolesc. Psychiatr. Clin. N. Am. 18(4), 813-823 (2009).
3. O'Brien LM, Gozal D. Neurocognitive dysfunction and sleep in children: from human to rodent. Pediatr. Clin. North Am. 51(1), 187-202 (2004). (Pubitemid 38121630)
4. Chaput JP, Brunet M, Tremblay A. Relationship between short sleeping hours and childhood overweight/obesity: results from the 'Quebec en Forme' Project. Int. J. Obesity (Lond.) 30(7), 1080-1085 (2006). (Pubitemid 43980575)
5. Carter PJ, Taylor BJ, Williams SM, Taylor RW. Longitudinal ana lysis of sleep in relation to BMI and body fat in children: the FLAME study BMJ 342, d2712 (2011).
6. Gangwisch JE, Malaspina D, Babiss LA et al. Short sleep duration as a risk factor for hypercholesterolemia: analyses of the National Longitudinal Study of Adolescent Health. Sleep 33(7), 956-961 (2010).
7. Cappuccio FP, Taggart FM, Kandala NB et al. Meta-ana lysis of short sleep duration and obesity in children and adults. Sleep 31(5), 619-626 (2008). (Pubitemid 351694250)
8. Chen X, Beydoun MA, Wang Y. Is sleep duration associated with childhood obesity? A systematic review and meta-ana lysis. Obesity 16(2), 265-274 (2008). (Pubitemid 351271904)
9. Wing YK, Li SX, Li AM, Zhang J, Kong AP. The effect of weekend and holiday sleep compensation on childhood overweight and obesity. Pediatrics 124(5), e994-e1000 (2009).
10. Spruyt K, Molfese DL, Gozal D. Sleep duration, sleep regularity, body weight, and metabolic homeostasis in school-aged children. Pediatrics 127(2), e345-e352 (2011).
11. Zheng H, Berthoud HR. Neural systems controlling the drive to eat: mind versus metabolism. Physiology (Bethesda) 23, 75-83 (2008).
12. Kong AP, Wing YK, Choi KC et al. Associations of sleep duration with obesity and serum lipid profle in children and adolescents. Sleep Med. 12(7), 659-665 (2011).
13. O'Brien LM, Holbrook CR, Mervis CB et al. Sleep and neurobehavioral characteristics of 5-to 7-year-old children with parentally reported symptoms of attention-defcit/hyperactivity disorder. Pediatrics 111(3), 554-563 (2003). (Pubitemid 36330712)
14. Blunden S, Lushington K, Lorenzen B, Wong J, Balendran R, Kennedy D. Symptoms of sleep breathing disorders in children are underreported by parents at general practice visits. Sleep Breath. 7(4), 167-176 (2003). (Pubitemid 38072288)
15. Kaditis AG, Finder J, Alexopoulos EI et al. Sleep-disordered breathing in 3,680 Greek children. Pediatr. Pulmonol. 37(6), 499-509 (2004). (Pubitemid 38680116)
16. Lofstrand-Tidestrom B, Hultcrantz E. The development of snoring and sleep related breathing distress from 4 to 6 years in a cohort of Swedish children. Int. J. Pediatr. Otorhinolaryngol. 71(7), 1025-1033 (2007). (Pubitemid 46783039)
17. Montgomery-Downs HE, O'Brien LM, Holbrook CR, Gozal D. Snoring and sleep-disordered breathing in young children: subjective and objective correlates. Sleep 27(1), 87-94 (2004). (Pubitemid 43906317)
18. Rosen CL, Larkin EK, Kirchner HL et al. Prevalence and risk factors for sleep-disordered breathing in 8-to 11-year-old children: association with race and prematurity. J. Pediatr. 142(4), 383-389 (2003). (Pubitemid 36521224)
19. Schlaud M, Urschitz MS, Urschitz-Duprat PM, Poets CF. 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(6), 431-440 (2004). (Pubitemid 39540481)
20. Spruyt K, O'Brien LM, Macmillan Coxon AP, Cluydts R, Verleye G, Ferri R. Multidimensional scaling of pediatric sleep breathing problems and bio-behavioral correlates. Sleep Med. 7(3), 269-280 (2006).
21. Gozal D. Sleep-disordered breathing and school performance in children. Pediatrics 102(3 Pt 1), 616-620 (1998). (Pubitemid 28409262)
22. Gozal D, Crabtree VM, Sans Capdevila O, Witcher LA, Kheirandish-Gozal L. C-reactive protein, obstructive sleep apnea, and cognitive dysfunction in school-aged children. Am. J. Respir. Crit. Care Med. 176(2), 188-193 (2007). (Pubitemid 47057856)
23. Ali NJ, Pitson DJ, Stradling JR. Snoring, sleep disturbance, and behaviour in 4-5 year olds. Arch. Dis. Child. 68(3), 360-366 (1993). (Pubitemid 23084587)
24. Chervin RD, Archbold KH, Dillon JE et al. Inattention, hyperactivity, and symptoms of sleep-disordered breathing. Pediatrics 109(3), 449-456 (2002). (Pubitemid 34177508)
25. Chervin RD, Dillon JE, Bassetti C, Ganoczy DA, Pituch KJ. Symptoms of sleep disorders, inattention, and hyperactivity in children. Sleep 20(12), 1185-1192 (1997). (Pubitemid 28082313)
26. Marcotte AC, Thacher PV, Butters M, Bortz J, Acebo C, Carskadon MA. Parental report of sleep problems in children with attentional and learning disorders. J. Dev. Behav. Pediatr. 19(3), 178-186 (1998). (Pubitemid 128456245)
27. Owens J, Spirito A, Marcotte A, McGuinn M, Berkelhammer L. Neuropsychological and behavioral correlates of obstructive sleep apnea syndrome in children: a preliminary study. Sleep Breath. 4(2), 67-78 (2000).
28. Bonuck K, Parikh S, Bassila M. Growth failure and sleep disordered breathing: a review of the literature. Int. J. Pediatr. Otorhinolaryngol. 70(5), 769-778 (2006).
29. Sans Capdevila O, Crabtree VM, Kheirandish-Gozal L, Gozal D. Increased morning brain natriuretic peptide levels in children with nocturnal enuresis and sleep-disordered breathing: a community-based study. Pediatrics 121(5), e1208-e1214 (2008).
30. Alexopoulos EI, Kaditis AG, Kostadima E, Gourgoulianis K. Resolution of nocturnal enuresis in snoring children after treatment with nasal budesonide. Urology 66(1), 194 (2005).
31. Bhattacharjee R, Kim J, Kheirandish-Gozal L, Gozal D. Obesity and obstructive sleep apnea syndrome in children: a tale of infammatory cascades. Pediatr. Pulmonol. 46(4), 313-323 (2011).
32. Gozal D, Serpero LD, Sans Capdevila O, Kheirandish-Gozal L. Systemic infammation in non-obese children with obstructive sleep apnea. Sleep Med. 9(3), 254-259 (2008). (Pubitemid 351387097)
33. Gozal D, Capdevila OS, Kheirandish-Gozal L. Metabolic alterations and systemic infammation in obstructive sleep apnea among nonobese and obese prepubertal children. Am. J. Respir. Crit. Care Med. 177(10), 1142-1149 (2008). (Pubitemid 351717574)
34. Bhattacharjee R, Kim J, Alotaibi WH, Kheirandish-Gozal L, Capdevila OS, Gozal D. Endothelial dysfunction in non-hypertensive children: potential contributions of obesity and obstructive sleep apnea. Chest 141(3), 682-691 (2012).
35. Bhattacharjee R, Kheirandish-Gozal L, Pillar G, Gozal D. Cardiovascular complications of obstructive sleep apnea syndrome: evidence from children. Prog. Cardiovasc. Dis. 51(5), 416-433 (2009).
36. Amin R, Somers VK, McConnell K et al. Activity-adjusted 24-hour ambulatory blood pressure and cardiac remodeling in children with sleep disordered breathing. Hypertension 51(1), 84-91 (2008). (Pubitemid 350307108)
37. Marcus CL, McColley SA, Carroll JL, Loughlin GM, Smith PL, Schwartz AR. Upper airway collapsibility in children with obstructive sleep apnea syndrome. J. Appl. Physiol. 77(2), 918-924 (1994). (Pubitemid 24258331)
38. Arens R, Marcus CL. Pathophysiology of upper airway obstruction: a developmental perspective. Sleep 27(5), 997-1019 (2004). (Pubitemid 39095735)
39. Wang RC, Elkins TP, Keech D, Wauquier A, Hubbard D. Accuracy of clinical evaluation in pediatric obstructive sleep apnea. Otolaryngol. Head Neck Surg. 118(1), 69-73 (1998). (Pubitemid 28086436)
40. Kaditis AG, Alexopoulos EI, Hatzi F et al. Adiposity in relation to age as predictor of severity of sleep apnea in children with snoring. Sleep Breath. 12(1), 25-31 (2008).
41. Rudnick EF, Walsh JS, Hampton MC, Mitchell RB. Prevalence and ethnicity of sleep-disordered breathing and obesity in children. Otolaryngol. Head Neck Surg. 137(6), 878-882 (2007). (Pubitemid 350117066)
42. Tauman R, Gozal D. Obesity and obstructive sleep apnea in children. Paediatr. Respir. Rev. 7(4), 247-259 (2006). (Pubitemid 44767192)
43. Verhulst SL, Schrauwen N, Haentjens D et al. Sleep-disordered breathing in overweight and obese children and adolescents: prevalence, characteristics and the role of fat distribution. Arch. Dis. Child. 92(3), 205-208 (2007). (Pubitemid 46423787)
44. Wang Y, Lobstein T Worldwide trends in childhood overweight and obesity. Int. J. Pediatr. Obes. 1(1), 11-25 (2006).
45. Lobstein T, Jackson-Leach R. Child overweight and obesity in the USA: prevalence rates according to IOTF defnitions. Int. J. Pediatr. Obes. 2(1), 62-64 (2007). (Pubitemid 46745352)
46. Ievers-Landis CE, Redline S. Pediatric sleep apnea: implications of the epidemic of childhood overweight. Am. J. Respir. Crit. Care Med. 175(5), 436-441 (2007). (Pubitemid 46354244)
47. Redline S, Tishler PV, Schluchter M, Aylor J, Clark K, Graham G. Risk factors for sleep-disordered breathing in children. Associations with obesity, race, and respiratory problems. Am. J. Respir. Crit. Care Med. 159(5 Pt 1), 1527-1532 (1999). (Pubitemid 29227864)
48. Bhattacharjee R, Kheirandish-Gozal L, Spruyt K et al. Adenotonsillectomy outcomes in treatment of obstructive sleep apnea in children: a multicenter retrospective study Am. J. Respir. Crit. Care Med. 182(5), 676-683 (2010).
49. Goodwin JL, Vasquez MM, Silva GE, Quan SF. Incidence and remission of sleep-disordered breathing and related symptoms in 6-to 17-year old children-the Tucson Children's Assessment of Sleep Apnea Study J. Pediatr. 157(1), 57-61 (2010).
50. Dayyat E, Kheirandish-Gozal L, Sans Capdevila O, Maarafeya MM, Gozal D. Obstructive sleep apnea in children: relative contributions of body mass index and adenotonsillar hypertrophy. Chest 136(1), 137-144 (2009).
51. Canapari CA, Hoppin AG, Kinane TB, Thomas BJ, Torriani M, Katz ES. Relationship between sleep apnea, fat distribution, and insulin resistance in obese children. J. Clin. Sleep Med. 7(3), 268-273 (2011).
52. Dayyat E, Kheirandish-Gozal L, Gozal D. Childhood obstructive sleep apnea: one or two distinct disease entities? Sleep Med. Clin. 2(3), 433-444 (2007).
53. Capdevila OS, Kheirandish-Gozal L, Dayyat E, Gozal D. Pediatric obstructive sleep apnea: complications, management, and long-term outcomes. Proc. Am. Thorac. Soc. 5(2), 274-282 (2008). (Pubitemid 351237887)
54. Tauman R, O'Brien LM, Ivanenko A, Gozal D. Obesity rather than severity of sleep-disordered breathing as the major determinant of insulin resistance and altered lipidemia in snoring children. Pediatrics 116(1), e66-e73 (2005).
55. Sinha R, Fisch G, Teague B et al. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity N. Engl. J. Med. 346(11), 802-810 (2002). (Pubitemid 34984653)
56. Srinivasan SR, Myers L, Berenson GS. Predictability of childhood adiposity and insulin for developing insulin resistance syndrome (syndrome X) in young adulthood: the Bogalusa Heart Study. Diabetes 51(1), 204-209 (2002). (Pubitemid 34517999)
57. Steinberger J, Moorehead C, Katch V, Rocchini AP. Relationship between insulin resistance and abnormal lipid profle in obese adolescents. J. Pediatr. 126(5 Pt 1), 690-695 (1995).
58. Sung RY, Tong PC, Yu CW et al. High prevalence of insulin resistance and metabolic syndrome in overweight/obese preadolescent Hong Kong Chinese children aged 9-12 years. Diabetes Care 26(1), 250-251 (2003). (Pubitemid 36929031)
59. Invitti C, Guzzaloni G, Gilardini L, Morabito F, Viberti G. Prevalence and concomitants of glucose intolerance in European obese children and adolescents. Diabetes Care 26(1), 118-124 (2003). (Pubitemid 36929003)
60. Punjabi NM, Sorkin JD, Katzel LI, Goldberg AP, Schwartz AR, Smith PL. Sleep-disordered breathing and insulin resistance in middle-aged and overweight men. Am. J. Respir. Crit. Care Med. 165(5), 677-682 (2002). (Pubitemid 34194756)
61. Strohl KP. Diabetes and sleep apnea. Sleep 19(10 Suppl.), S225-S228 (1996). (Pubitemid 27138535)
62. Grunstein RR. Metabolic aspects of sleep apnea. Sleep 19(10 Suppl.), S218-S220 (1996). (Pubitemid 27138533)
63. 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. 165(5), 670-676 (2002). (Pubitemid 34194755)
64. Davies RJ, Turner R, Crosby J, Stradling JR. Plasma insulin and lipid levels in untreated obstructive sleep apnoea and snoring; their comparison with matched controls and response to treatment. J. Sleep Res. 3(3), 180-185 (1994). (Pubitemid 24311373)
65. Kaditis AG, Alexopoulos EI, Damani E et al. Obstructive sleep-disordered breathing and fasting insulin levels in nonobese children. Pediatr. Pulmonol. 40(6), 515-523 (2005). (Pubitemid 41720708)
66. Verhulst SL, Schrauwen N, Haentjens D et al. Sleep-disordered breathing and the metabolic syndrome in overweight and obese children and adolescents. J. Pediatr. 150(6), 608-612 (2007). (Pubitemid 46755804)
67. Alexopoulos EI, Gletsou E, Kostadima E et al. Effects of obstructive sleep apnea severity on serum lipid levels in Greek children with snoring. Sleep Breath. 15(4), 625-631 (2011).
68. Redline S, Storfer-Isser A, Rosen CL et al. Association between metabolic syndrome and sleep-disordered breathing in adolescents. Am. J. Respir. Crit. Care Med. 176(4), 401-408 (2007). (Pubitemid 47267475)
69. Bhushan B, Khalyfa A, Spruyt K et al. Fatty-acid binding protein 4 gene polymorphisms and plasma levels in children with obstructive sleep apnea. Sleep Med. 12(7), 666-671 (2011).
70. Drager LF, Jun JC, Polotsky VY. Metabolic consequences of intermittent hypoxia: relevance to obstructive sleep apnea. Best Pract. Res. Clin. Endocrinol. Metab. 24(5), 843-851 (2010).
71. Li J, Thorne LN, Punjabi NM et al. Intermittent hypoxia induces hyperlipidemia in lean mice. Circ. Res. 97(7), 698-706 (2005). (Pubitemid 41416339)
72. Li J, Grigoryev DN, Ye SQ et al. Chronic intermittent hypoxia upregulates genes of lipid biosynthesis in obese mice. J. Appl. Physiol. 99(5), 1643-1648 (2005). (Pubitemid 41547158)
73. Li J, Savransky V, Nanayakkara A, Smith PL, O'Donnell CP, Polotsky VY. Hyperlipidemia and lipid peroxidation are dependent on the severity of chronic intermittent hypoxia. J. Appl. Physiol. 102(2), 557-563 (2007). (Pubitemid 46220883)
74. Savransky V, Nanayakkara A, Li J et al. Chronic intermittent hypoxia induces atherosclerosis. Am. J. Respir. Crit. Care Med. 175(12), 1290-1297 (2007). (Pubitemid 46905755)
75. Miyazaki M, Kim YC, Gray-Keller MP, Attie AD, Ntambi JM. The biosynthesis of hepatic cholesterol esters and triglycerides is impaired in mice with a disruption of the gene for stearoyl-CoA desaturase 1. J. Biol. Chem. 275(39), 30132-30138 (2000).
76. Ntambi JM, Miyazaki M. Regulation of stearoyl-CoA desaturases and role in metabolism. Prog. Lipid Res. 43(2), 91-104 (2004). (Pubitemid 37487985)
77. Li J, Nanayakkara A, Jun J, Savransky V, Polotsky VY. Effect of defciency in SREBP cleavage-activating protein on lipid metabolism during intermittent hypoxia. Physiol. Genomics 31(2), 273-280 (2007). (Pubitemid 350014405)
78. Savransky V, Jun J, Li J et al. Dyslipidemia and atherosclerosis induced by chronic intermittent hypoxia are attenuated by defciency of stearoyl coenzyme A desaturase. Circ. Res. 103(10), 1173-1180 (2008).
79. Li J, Bosch-Marce M, Nanayakkara A et al. Altered metabolic responses to intermittent hypoxia in mice with partial defciency of hypoxia-inducible factor-1alpha. Physiol. Genomics 25 (3), 450-457 (2006). (Pubitemid 43764766)
80. Langin D. Adipose tissue lipolysis as a metabolic pathway to defne pharmacological strategies against obesity and the metabolic syndrome. Pharmacol. Res. 53(6), 482-491 (2006). (Pubitemid 43767551)
81. Jun J, Reinke C, Bedja D et al. Effect of intermittent hypoxia on atherosclerosis in apolipoprotein E-defcient mice. Atherosclerosis 209(2), 381-386 (2010).
82. Prabhakar NR, Kumar GK. Mechanisms of sympathetic activation and blood pressure elevation by intermittent hypoxia. Respir. Physiol. Neurobiol. 174(1-2), 156-161 (2010).
83. Bartness TJ, Vaughan CH, Song CK. Sympathetic and sensory innervation of brown adipose tissue. Int. J. Obes. (Lond.) 34(Suppl. 1), S36-S42 (2010).
84. Drager LF, Li J, Shin MK et al. Intermittent hypoxia inhibits clearance of triglyceride-rich lipoproteins and inactivates adipose lipoprotein lipase in a mouse model of sleep apnoea. Eur. Heart J. 33(6), 783-790 (2012).
85. Dallinga-Thie GM, Franssen R, Mooij HL et al. The metabolism of triglyceride-rich lipoproteins revisited: new players, new insight. Atherosclerosis 211(1), 1-8 (2010).
86. Mahley RW, Huang Y. Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing. J. Clin. Invest. 117(1), 94-98 (2007). (Pubitemid 46048456)
87. Wang H, Eckel RH. Lipoprotein lipase: from gene to obesity Am. J. Physiol. Endocrinol. Metab. 297(2), E271-E288 (2009).
88. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, infammation and immunity Nat. Rev. Immunol. 6(10), 772-783 (2006). (Pubitemid 44453463)
89. Polotsky VY, Li J, Punjabi NM et al. Intermittent hypoxia increases insulin resistance in genetically obese mice. J. Physiol. 552(Pt 1), 253-264 (2003). (Pubitemid 37265483)
90. Fox CS, Massaro JM, Hoffmann U et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study Circulation 116(1), 39-48 (2007). (Pubitemid 47016245)
91. Thorne A, Lonnqvist F, Apelman J, Hellers G, Arner P. A pilot study of long-term effects of a novel obesity treatment: omentectomy in connection with adjustable gastric banding. Int. J. Obes. Relat. Metab. Disord. 26(2), 193-199 (2002). (Pubitemid 34151196)
92. Klein S, Fontana L, Young VL et al. Absence of an effect of liposuction on insulin action and risk factors for coronary heart disease. N. Engl. J. Med. 350(25), 2549-2557 (2004). (Pubitemid 38758542)
93. Gharib SA, Khalyfa A, Abdelkarim A et al. Intermittent hypoxia activates temporally coordinated transcriptional programs in visceral adipose tissue. J. Mol. Med. (Berl.) doi:10.1007/s00109-011-0830-7 (2011) (Epub ahead of print).
94. Puri V, Ranjit S, Konda S et al. Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc. Natl Acad. Sci. USA 105(22), 7833-7838 (2008). (Pubitemid 351872724)