Serum inflammatory markers in obstructive sleep apnea: A meta-analysis

Journal of Clinical Sleep Medicine

Volumn 9, Issue 10, 2013, Pages 1003-1012

  Nadeem, Rashid ^a,b   Molnar, Janos ^b   Madbouly, Essam M ^a   Nida, Mahwish ^c   Aggarwal, Saurabh ^a   Sajid, Hassan ^d   Naseem, Jawed ^e   Loomba, Rohit ^f  

^a James A Lovell Federal Health Care Center   (United States)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY OF KARACHI   (Pakistan)

^f CHILDREN S HOSPITAL OF WISCONSIN   (United States)

Author keywords

CRP; ICAM; IL 6; IL 8; Inflammatory markers; Obstructive sleep apnea; Selectins; TNF ; VCAM

Indexed keywords

BIOLOGICAL MARKER; C REACTIVE PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; SELECTIN; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; ATHEROSCLEROSIS; BODY MASS; DISEASE MARKER; EMBASE; HUMAN; HYPERTENSION; MEDLINE; META ANALYSIS; SEPTIC SHOCK; SLEEP DISORDER; SLEEP DISORDERED BREATHING; SYSTEMATIC REVIEW;

CRP; ICAM; IL-6; IL-8; INFLAMMATORY MARKERS; OBSTRUCTIVE SLEEP APNEA; SELECTINS; TNF-Α; VCAM;

ADULT; AGED; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CELL ADHESION MOLECULES; DISEASE PROGRESSION; FEMALE; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; INTERLEUKIN-8; MALE; MIDDLE AGED; POLYSOMNOGRAPHY; SELECTINS; SENSITIVITY AND SPECIFICITY; SEVERITY OF ILLNESS INDEX; SLEEP APNEA, OBSTRUCTIVE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84888188114     PISSN: 15509389     EISSN: 15509397     Source Type: Journal    
DOI: 10.5664/jcsm.3070     Document Type: Article

References (88)

1. Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 1993;32:1230-5. (Pubitemid 23115702)
2. Guilleminault C, Tilkian A, Dement WC. The sleep apnea syndromes. Annu Rev Med 1976;27:465-84.
3. Somers VK, Dyken ME, Clary MP, Abboud FM. Sympathetic neural mechanisms in obstructive sleep apnea. J Clin Invest 1995;96:1897-904.
4. Kato M, Roberts-Thomson P, Phillips BG, et al. Impairment of endothelium-dependent vasodilation of resistance vessels in patients with obstructive sleep apnea. Circulation 2000;102:2607-10.
5. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med 1999;340:115-26.
6. Glass CK, Witztum JL. Atherosclerosis: the road ahead. Cell 2001;104:503-16. (Pubitemid 32201946)
7. Nieto FJ, Young TB, Lind BK, et al. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep Heart Health. JAMA 2000;283:1829-36. (Pubitemid 30207619)
8. Peppard PE, Young T, Palta M, et al. Prospective study of the association between sleep-disordered breathing and hypertension. N Engl J Med 2000;342:1378-84. (Pubitemid 30262394)
9. Shahar E, Whitney CW, Redline S, et al. Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 2001;163:19-25. (Pubitemid 32095247)
10. Peker Y, Hedner J, Norum J, Kraiczi H, Carlson J. Increased incidence of cardiovascular disease in middle-aged men with obstructive sleep apnea: a 7-year follow-up. Am J Respir Crit Care Med 2002;166:159-65. (Pubitemid 34765451)
11. Imadojemu VA, Gleeson K, Gray KS, Sinoway LI, Leuenberger UA. Obstructive sleep apnea during sleep is associated with peripheral vasoconstriction. Am J Respir Crit Care Med 2002;165:61-6. (Pubitemid 34053358)
12. Sajkov D, Wang T, Saunders NA, Bune AJ, McEvoy RD. Continuous positive airway pressure treatment improves pulmonary hemodynamics in patients with obstructive sleep apnea. Am J Respir Crit Care Med 2002; 166:152-8. (Pubitemid 34084449)
13. Amin RS, Kimball TR, Bean JA, et al. Left ventricular hypertrophy and abnormal ventricular geometry in children and adolescents with obstructive sleep apnea. Am J Respir Crit Care Med 2002;165:1395-9. (Pubitemid 34522943)
14. Sekosan M, Zakkar M, Wenig BL, Olopade CO, Rubenstein I. Inflammation in the uvula mucosa of patients with obstructive sleep apnea. Laryngoscope 1996;106:1018-20. (Pubitemid 26287248)
15. Bergeron C, Kimoff J, Hamid Q. Images in allergy and immunology: obstructive sleep apnea syndrome and inflammation. J Allergy Clin Immunol 2005;116:1393-6. (Pubitemid 41740957)
16. Puig F, Rico F, Almendros I, Montserrat JM, Navajas D, Farre R. Vibration enhances interleukin-8 release in a cell model of snoring induced airway inflammation. Sleep 2005;28:1312-6. (Pubitemid 41437893)
17. Ursavaş A, Karadaǧ M, Rodoplu E, Yilmaztepe A, Oral HB, Gözü RO. Circulating ICAM-1 and VCAM-1 levels in patients with obstructive sleep apnea syndrome. Respiration 2007;74:525-32. (Pubitemid 47206882)
18. Von Känel R, Loredo JS, Ancoli-Israel S, Mills PJ, Natarajan L, Dimsdale JE. Association between polysomnographic measures of disrupted sleep and prothrombotic factors. Chest 2007;131:733-9. (Pubitemid 46446864)
19. Punjabi NM, Beamer BA. C-reactive protein is associated with sleep disordered breathing independent of adiposity. Sleep 2007;30:29-34. (Pubitemid 46095380)
20. De la Pena Bravo M, Serpero LD, Barcelo A, et al. Inflammatory proteins in patients with obstructive sleep apnea with and without daytime sleepiness. Sleep Breath 2007;11:177-85. (Pubitemid 47307847)
21. Minoguchi K, Tazaki T, Yokoe T, et al. Elevated production of tumor necrosis factor-α by monocytes in patients with obstructive sleep apnea syndrome. Chest 2004;126:1473-9. (Pubitemid 39525019)
22. Ciftci TU, Korturk O, Bukan N, et al. The relationship between serum cytokine levels with obesity and obstructive sleep apnea syndrome. Cytokine 2004;28:87-91. (Pubitemid 39302489)
23. 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; 82:1313-6. (Pubitemid 27200394)
24. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Endocrinol Metab 2000; 85:1151-8. (Pubitemid 32269364)
25. Young T, Skatrud J, Peppard PE. Risk factors for obstructive sleep apnea in adults. JAMA 2004;291:2013-6. (Pubitemid 38544284)
26. Yokoe T, Minoguchi K, Matsuo H, et al. Elevated levels of C-reactive protein and interleukin-6 in patients with obstructive sleep apnea syndrome are decreased by nasal continuous positive airway pressure. Circulation 2003;107:1129-34. (Pubitemid 36297204)
27. Shamsuzzaman AS, Winnicki M, Lanfranchi P, et al. Elevated C-reactive protein in patients with obstructive sleep apnea. Circulation 2002;105:2462-4. (Pubitemid 34568964)
28. Kokturk O, Ciftci TU, Mollarecep E, Ciftci B. Elevated C-reactive protein levels and increased cardiovascular risk in patients with obstructive sleep apnea syndrome. Int Heart J 2005; 46:801-9.
29. 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;20:200-2. (Pubitemid 33210383)
30. Barceló A, Barbé F, Llompart E, et al. Effects of obesity on C-reactive protein level and metabolic disturbances in male patients with obstructive sleep apnea. Am J Respir Crit Care Med 2004;117:118-21. (Pubitemid 38953732)
31. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Circadian interleukin-6 secretion and quantity and depth of sleep. J Clin Endocrinol Metab 1999;84:2603-7. (Pubitemid 30641979)
32. Castell J, Gomez-Lechion M, David M. Acute phase response of human hepatocyte: regulation of acute-phase protein synthesis by interleukin-6. Hepatology 1990;12:1179-86.
33. Meier-Ewert HK, Ridker PM, Rifai N, et al. Absence of diurnal variation of C-reactive protein concentrations in healthy human subjects. Clin Chem 2001;47:426-30. (Pubitemid 32222455)
34. Ridker PM. High-sensitivity C-reactive protein: potential adjunct for global risk assessment in the primary prevention of cardiovascular disease. Circulation 2001;103:1813-8. (Pubitemid 32291421)
35. Danesh J, Whincup P, Walker M, et al. Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. BMJ 2000;321:199-204. (Pubitemid 30459555)
36. Lindahl B, Toss H, Siegbahn A, et al. Markers of myocardial damage and inflammation in relation to long-term mortality in unstable coronary artery disease. FRISC Study Group. Fragmin during Instability in Coronary Artery Disease. N Engl J Med 2000;343:1139-47.
37. Ridker PM, Rifai N, Pfeffer MA, et al. Long-term effects of pravastatin on plasma concentration of C-reactive protein. The Cholesterol and Recurrent Events (CARE) Investigators. Circulation 1999;100:230-5. (Pubitemid 29340127)
38. Jialal I, Devaraj S, Venugopal SK. C-reactive protein: risk marker or mediator in atherothrombosis? Hypertension 2004; 44:6-11. (Pubitemid 38823477)
39. Calabro P, Willerson JT, Yeh ET. Inflammatory cytokines stimulated C-reactive protein production by human coronary artery smooth muscle cells. Circulation 2003;108:1930-2. (Pubitemid 37296536)
40. Devaraj S, Xu DY, Jialal I. C-reactive protein increases plasminogen activator inhibitor-1 expression and activity in human aortic endothelial cells: implications for the metabolic syndrome and atherothrombosis. Circulation 2003;107:398-404.
41. Han KH, Hong KH, Park JH, et al. C-reactive protein promotes monocyte chemoattractant protein-I-mediated chemotaxis through upregulating CC chemokine receptor 2 expression in human monocytes. Circulation 2004;109:2566-71. (Pubitemid 38720558)
42. Hartmann G, Tschop M, Fischer R, et al. High altitude increases circulating interleukin-6, interleukin-1 receptor antagonist and C-Reactive Protein. Cytokine 2000;12:246-52. (Pubitemid 30449882)
43. Roytblat L, Rachinsky M, Fisher A, et al. Raised interleukin-6 levels in obese patients. Obes Res 2000;8:673-5.
44. Yudkin JS, kumari M, Humphries SE, Mohamed-Ali V. Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 2000;148:209-14.
45. Harris TB, Ferruci L, Tracy RP, et al. Association of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am J Med 1999;106:506-12. (Pubitemid 29231100)
46. Peled N, Greenberg A, Pillar G, et al. Contributions of hypoxia and respiratory disturbance index to sympathetic activation and blood pressure in obstructive sleep apnea syndrome. Am J Hypertens 1998;11:1284-9. (Pubitemid 28541042)
47. Hartmann G, Tschop M, Fischer R, et al. High altitude increases circulating interleukin-6, interleukin-1 receptor antagonist and C-reactive protein. Cytokine 2000;12:246-52. (Pubitemid 30449882)
48. Imoberdorf R, Garlick PJ, McNurlan MA, et al. Enhanced synthesis of albumin and fibrinogen at high altitude. J Appl Physiol 2001;90:528-37. (Pubitemid 32118912)
49. Guilleminault C, Kirisoglu C, Ohayon MM. C-reactive protein and sleep-disordered breathing. Sleep 2004;27:1507-11. (Pubitemid 40041619)
50. Aderka D. The potential biological and clinical significance of the soluble tumor necrosis factor receptors. Cytokine Growth Factor Rev 1996;7:231-40. (Pubitemid 27200307)
51. Brockhaus M, Schoenfeld H, Schlaeger E, Hunziker W, Lesslauer W, Loetscher H. Identification of two types of tumor necrosis factor receptors on human cell lines by monoclonal antibodies. Proc Natl Acad Sci U S A 1990;87:3127-31.
52. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13.
53. Bhushan B, Guleria R, Misra A, Pandey RM, Luthra K, Vikram NK. Obstructive sleep apnoea correlates with C-reactive protein in obese Asian Indians. Nutr Metab Cardiovasc Dis 2009;19:184-9.
54. Liu Z, Xu Y, Hua Q, Wang Y, Liu R, Yang Z. Additive effects of obstructive sleep apnea syndrome and hypertension on inflammatory reaction. Afr J Biotechnol 2011;10:11738-44.
55. Sackett DL, Straus SE, Richardson WS, Rosenberg W, Haynes RB. Evidence-based medicine-How to practice and teach EBM (2nd edn). Oxford: Churchill Livingstone, 2000: 173-175.
56. Carneiro G, Togeiro SM, Ribeiro-Filho FF, et al. Continuous positive airway pressure therapy improves hypoadiponectinemia in severe obese men with obstructive sleep apnea without changes in insulin resistance. Metab Syndr Relat Disord 2009;7:537-42.
57. Chien MY, Lee P, Tsai YF, Yang PC, Wu YT. C-reactive protein and heart rate recovery in middle-aged men with severe obstructive sleep apnea. Sleep Breath 2012;16:629-37.
58. Dziewas R, Ritter M, Kruger L, et al. C-reactive protein and fibrinogen in acute stroke patients with and without sleep apnea. Cerebrovasc Dis 2007;24:412-7. (Pubitemid 350014965)
59. Guasti L, Marino F, Cosentino M, et al. Cytokine production from peripheral blood mononuclear cells and polymorphonuclear leukocytes in patients studied for suspected obstructive sleep apnea. Sleep Breath 2011;15:3-11.
60. Harsch IA, Bergmann T, Koebnick C, et al. Adiponectin, resistin and subclinical inflammation - the metabolic burden in Launois Bensaude Syndrome, a rare form of obesity. J Physiol Pharmacol 2007;58 Suppl 1:65-76. (Pubitemid 350022259)
61. Hayashi M, Fujimoto K, Urushibata K, Takamizawa A, Kinoshita O, Kubo K. Hypoxia-sensitive molecules may modulate the development of atherosclerosis in sleep apnoea syndrome. Respirology 2006;11:24-31.
62. Iesato K, Tatsumi K, Saibara T, et al. Decreased lipoprotein lipase in obstructive sleep apnea syndrome. Circ J 2007;71:1293-8. (Pubitemid 47195349)
63. Kapsimalis F, Varouchakis G, Manousaki A, et al. Association of sleep apnea severity and obesity with insulin resistance, C-reactive protein, and leptin levels in male patients with obstructive sleep apnea. Lung 2008;186:209-17.
64. Meng S, Fang L, Wang CQ, Wang LS, Chen MT, Huang XH. Impact of obstructive sleep apnoea on clinical characteristics and outcomes in patients with acute coronary syndrome following percutaneous coronary intervention. J Int Med Res 2009;37:1343-53.
65. Sariman N, Levent E, Cubuk R, Yurtlu S, Benli Aksungar F. Bronchial hyperreactivity and airway wall thickening in obstructive sleep apnea patients. Sleep Breath 2011;15:341-50.
66. Steiropoulos P, Papanas N, Nena E, et al. Inflammatory markers in middle-aged obese subjects: does obstructive sleep apnea syndrome play a role? Mediators Inflamm 2010;2010:675320. http://dx.doi.org/10.1155/2010/675320.
67. Thomopoulos C, Tsioufis C, Dimitriadis K, et al. Obstructive sleep apnoea syndrome is associated with enhanced sub-clinical inflammation and asymmetric dimethyl-arginine levels in hypertensives. J Hum Hypertens 2009;23:65-7.
68. Yumino D, Tsurumi Y, Takagi A, Suzuki K, Kasanuki H. Impact of obstructive sleep apnea on clinical and angiographic outcomes following percutaneous coronary intervention in patients with acute coronary syndrome. Am J Cardiol 2007;99:26-30 (Pubitemid 44969334)
69. Arias MA, García-Río F, Alonso-Fernández A, et al. CPAP decreases plasma levels of soluble tumour necrosis factor-alpha receptor 1 in obstructive sleep apnoea. Eur Respir J 2008;32:1009-15.
70. Dyugovskaya L, Lavie P, Lavie L. Phenotypic and functional characterization of blood gammadelta T cells in sleep apnea. Am J Respir Crit Care Med 2003;168:242-9. (Pubitemid 36920981)
71. Drager LF, Lopes HF, Maki-Nunes C, et al. The impact of obstructive sleep apnea on metabolic and inflammatory markers in consecutive patients with metabolic syndrome. PLoS One 2010;5:e12065.
72. Guven SF, Turkkani MH, Ciftci B, Ciftci TU, Erdogan Y. The relationship between high-sensitivity C-reactive protein levels and the severity of obstructive sleep apnea. Sleep Breath 2012;16:217-21.
73. Sharma SK, Mishra HK, Sharma H, et al. Obesity, and not obstructive sleep apnea, is responsible for increased serum hs-CRP levels in patients with sleep-disordered breathing in Delhi. Sleep Med 2008;9:149-56.
74. Ryan S, Nolan GM, Hannigan E, Cunningham S, Taylor C, McNicholas WT. Cardiovascular risk markers in obstructive sleep apnoea syndrome and correlation with obesity. Thorax 2007;62,509-14. (Pubitemid 46910129)
75. Fornadi K, Lindner A, Czira ME, et al. Lack of association between objectively assessed sleep disorders and inflammatory markers among kidney transplant recipients. Int Urol Nephrol 2012;44:607-17.
76. Muraki I, Tanigawa T, Yamagishi K, et al. Nocturnal intermittent hypoxia and C reactive protein among middle-aged community residents: a cross-sectional survey. Thorax 2010;65,523-7.
77. Yao M, Tachibana N, Okura M, et al. The relationship between sleep-disordered breathing and high-sensitivity C-reactive protein in Japanese men. Sleep 2006;29,661-5.
78. Taheri S, Austin D, Lin L, Nieto FJ, Young T, Mignot E. Correlates of serum C-reactive protein (CRP)-no association with sleep duration or sleep disordered breathing. Sleep 2007;30,991-6. (Pubitemid 47221899)
79. Sahlman J, Miettinen K, Peuhkurinen K, et al.; Kuopio Sleep Apnoea Group. The activation of the inflammatory cytokines in overweight patients with mild obstructive sleep apnoea. J Sleep Res 2010;19:341-8.
80. Constantinidis J, Ereliadis S, Angouridakis N, Konstantinidis I, Vital V, Angouridaki C. Cytokine changes after surgical treatment of obstructive sleep apnoea syndrome. Eur Arch Otorhinolaryngol 2008;265:1275-9.
81. Mehra R, Storfer-Isser A, Kirchner HL, et al. Soluble interleukin 6 receptor: a novel marker of moderate to severe sleep-related breathing disorder. Arch Intern Med 2006;166:1725-31. (Pubitemid 44414460)
82. Zamarron-Sanz C, Ricoy-Galbaldon J, Gude-Sampedro F, Riveiro-Riveiro A. Plasma levels of vascular endothelial markers in obstructive sleep apnea. Arch Med Res 2006;37:552-5.
83. Priou P, Gagnadoux F, Tesse A, et al. Endothelial dysfunction and circulating microparticles from patients with obstructive sleep apnea. Am J Pathol 2010;177;974-83.
84. Alberti A, Sarchielli P, Gallinella E, et al. Plasma cytokine levels in patients with obstructive sleep apnea syndrome: a preliminary study. J Sleep Res 2003;12:305-11. (Pubitemid 38010437)
85. Kanbay A, Kaya E, Buyukoglan H, et al. Serum gamma-glutamyl transferase activity is an independent predictor for cardiovascular disease in obstructive sleep apnea syndrome. Respir Med 2011;105:637-42.
86. Kobayashi K, Nishimura Y, Shimada T, et al. Effect of continuous positive airway pressure on soluble CD40 ligand in patients with obstructive sleep apnea syndrome. Chest 2006;129:632-7.
87. Li NF, Yao XG, Zhu J, et al. Higher levels of plasma TNF-alpha and neuropeptide Y in hypertensive patients with obstructive sleep apnea syndrome. Clin Exp Hypertens 2010;32:54-60.
88. Cartier A, Cote M, Lemieux I, et al. Age-related differences in inflammatory markers in men: contribution of visceral adiposity. Metabolism 2009;58:1452-8.