Impact of obstructive sleep apnea syndrome on endothelial function, arterial stiffening, and serum inflammatory markers: An updated meta-analysis and metaregression of 18 studies

Journal of the American Heart Association

Volumn 4, Issue 11, 2015, Pages

  Wang, Jiayang ^a   Yu, Wenyuan ^a   Gao, Mingxin ^a   Zhang, Fan ^a   Gu, Chengxiong ^a   Yu, Yang ^a   Wei, Yongxiang ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Arterial stiffening; C reactive protein; Endothelial dysfunction; Obstructive sleep apnea

Indexed keywords

C REACTIVE PROTEIN; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; BIOLOGICAL MARKER;

ARTERIAL STIFFNESS; ARTICLE; AUGMENTATION INDEX; CARDIOVASCULAR DISEASE; CARDIOVASCULAR PARAMETERS; CHRONIC INFLAMMATION; DISEASE ASSOCIATION; DISEASE SEVERITY; ENDOTHELIAL DYSFUNCTION; FLOW MEDIATED DILATION; HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PULSE WAVE; SLEEP DISORDERED BREATHING; BLOOD; CARDIOVASCULAR DISEASES; CASE CONTROL STUDY; COMPLICATION; INFLAMMATION; META ANALYSIS; PATHOPHYSIOLOGY; PROGNOSIS; RISK ASSESSMENT; RISK FACTOR; SEVERITY OF ILLNESS INDEX; SLEEP APNEA, OBSTRUCTIVE; UPREGULATION; VASCULAR ENDOTHELIUM; VASODILATATION;

BIOMARKERS; C-REACTIVE PROTEIN; CARDIOVASCULAR DISEASES; CASE-CONTROL STUDIES; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; PROGNOSIS; RISK ASSESSMENT; RISK FACTORS; SEVERITY OF ILLNESS INDEX; SLEEP APNEA, OBSTRUCTIVE; UP-REGULATION; VASCULAR STIFFNESS; VASODILATION;

EID: 85006226137     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.115.002454     Document Type: Article

References (68)

1. Dong JY, Zhang YH, Qin LQ.Obstructive sleep apnea and cardiovascular risk:metaanalysis of prospective cohort studies. Atherosclerosis. 2013;229:489-495.
2. Vlachantoni IT, Dikaiakou E, Antonopoulos CN, Stefanadis C, Daskalopoulou SS, Petridou ET. Effects of continuous positive airway pressure (CPAP) treatment for obstructive sleep apnea in arterial stiffness: a meta-analysis. Sleep Med Rev. 2013;17:19-28.
3. Young T, Finn L, Peppard PE, Szklo-Coxe M, Austin D, Nieto FJ, Stubbs R, Hla KM. Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort. Sleep. 2008;31:1071-1078.
4. Marshall NS, Wong KK, Liu PY, Cullen SR, Knuiman MW, Grunstein RR. Sleep apnea as an independent risk factor for all-cause mortality: the Busselton Health Study. Sleep. 2008;31:1079-1085.
5. Punjabi NM, Caffo BS, Goodwin JL, Gottlieb DJ, Newman AB, O'Connor GT, Rapoport DM, Redline S, Resnick HE, Robbins JA, Shahar E, Unruh ML, Samet JM. Sleep-disordered breathing and mortality: a prospective cohort study. PLoS Med. 2009;6:e1000132.
6. Redline S, Yenokyan G, Gottlieb DJ, Shahar E, O'Connor GT, Resnick HE, Diener-West M, Sanders MH, Wolf PA, Geraghty EM, Ali T, Lebowitz M, Punjabi NM. Obstructive sleep apnea-hypopnea and incident stroke: the sleep heart health study. Am J Respir Crit Care Med. 2010;182:269-277.
7. Gottlieb DJ, Yenokyan G, Newman AB, O'Connor GT, Punjabi NM, Quan SF, Redline S, Resnick HE, Tong EK, Diener-West M, Shahar E. Prospective study of obstructive sleep apnea and incident coronary heart disease and heart failure: the sleep heart health study. Circulation. 2010;122:352-360.
8. Wang X, Ouyang Y, Wang Z, Zhao G, Liu L, Bi Y. Obstructive sleep apnea and risk of cardiovascular disease and all-cause mortality: a meta-analysis of prospective cohort studies. Int J Cardiol. 2013;169:207-214.
9. Butt M, Khair OA, Dwivedi G, Shantsila A, Shantsila E, Lip GY. Myocardial perfusion by myocardial contrast echocardiography and endothelial dysfunction in obstructive sleep apnea. Hypertension. 2011;58:417-424.
10. Butt M, Dwivedi G, Khair O, Lip GY. Obstructive sleep apnea and cardiovascular disease. Int J Cardiol. 2010;139:7-16.
11. Napoli C, Ignarro LJ. Nitric oxide and atherosclerosis. Nitric Oxide. 2001;5:88-97.
12. Wada T, Kodaira K, Fujishiro K, Maie K, Tsukiyama E, Fukumoto T, Uchida T, Yamazaki S. Correlation of ultrasound-measured common carotid artery stiffness with pathological findings. Arterioscler Thromb. 1994;14:479-482.
13. Vlachopoulos C, Aznaouridis K, Stefanadis C. Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol. 2010;55:1318-1327.
14. Mitchell GF, Hwang SJ, Vasan RS, Larson MG, Pencina MJ, Hamburg NM, Vita JA, Levy D, Benjamin EJ. Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation. 2010;121:505-511.
15. Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, Ducimetiere P, Benetos A. Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension. 2001;37:1236-1241.
16. Ryan S, Taylor CT, McNicholas WT. Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome. Circulation. 2005;112:2660-2667.
17. Arias MA, Garcia-Rio F, Alonso-Fernandez A, Hernanz A, Hidalgo R, Martinez-Mateo V, Bartolome S, Rodriguez-Padial L. Cpap decreases plasma levels of soluble tumour necrosis factor-receptor 1 in obstructive sleep apnoea. Eur Respir J. 2008;32:1009-1015.
18. 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;16:217-221.
19. 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;46:801-809.
20. Sanders MH. Elevated plasma C-reactive protein and increased cardiovascular/cerebrovascular risk in sleep apnea patients. Article reviewed: elevated Creactive protein in patients with obstructive sleep apnea (a brief rapid communication). Sleep Med. 2002;3:449-450.
21. Wilson AM, Ryan MC, Boyle AJ. The novel role of C-reactive protein in cardiovascular disease: riskmarker or pathogen. Int J Cardiol. 2006;106:291-297.
22. Aderka D. The potential biological and clinical significance of the soluble tumor necrosis factor receptors. Cytokine Growth Factor Rev. 1996;7:231-240.
23. Valgimigli M, Ceconi C, Malagutti P, Merli E, Soukhomovskaia O, Francolini G, Cicchitelli G, Olivares A, Parrinello G, Percoco G, Guardigli G, Mele D, Pirani R, Ferrari R. Tumor necrosis factor-alpha receptor 1 is a major predictor of mortality and new-onset heart failure in patients with acute myocardial infarction: the cytokine-activation and long-term prognosis in myocardial infarction (C-ALPHA) study. Circulation. 2005;111:863-870.
24. Nadeem R, Molnar J, Madbouly EM, Nida M, Aggarwal S, Sajid H, Naseem J, Loomba R. Serum inflammatory markers in obstructive sleep apnea: a metaanalysis. J Clin Sleep Med. 2013;9:1003-1012.
25. Manabe S, Okura T, Watanabe S, Higaki J. Association between carotid haemodynamics and inflammation in patients with essential hypertension. J Hum Hypertens. 2005;19:787-791.
26. Moher D, Liberati A, Tetzlaff J, Altman DG; Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264-269.
27. Doonan RJ, Scheffler P, Lalli M, Kimoff RJ, Petridou ET, Daskalopoulos ME, Daskalopoulou SS. Increased arterial stiffness in obstructive sleep apnea: a systematic review. Hypertens Res. 2011;34:23-32.
28. Zeng X, Zhang Y, Kwong JS, Zhang C, Li S, Sun F, Niu Y, Du L. The methodological quality assessment tools for preclinical and clinical studies, systematic review and meta-analysis, and clinical practice guideline: a systematic review. J Evid Based Med. 2015;8:2-10.
29. Tanriverdi H, Evrengul H, Kara CO, Kuru O, Tanriverdi S, Ozkurt S, Kaftan A, Kilic M. Aortic stiffness, flow-mediated dilatation and carotid intima-media thickness in obstructive sleep apnea: non-invasive indicators of atherosclerosis. Respiration. 2006;73:741-750.
30. El Solh AA, Akinnusi ME, Baddoura FH, Mankowski CR. Endothelial cell apoptosis in obstructive sleep apnea: a link to endothelial dysfunction. Am J Respir Crit Care Med. 2007;175:1186-1191.
31. Chung S, Yoon IY, Shin YK, Lee CH, Kim JW, Lee T, Choi DJ, Ahn HJ. Endothelial dysfunction and C-reactive protein in relation with the severity of obstructive sleep apnea syndrome. Sleep. 2007;30:997-1001.
32. Jelic S, Padeletti M, Kawut SM, Higgins C, Canfield SM, Onat D, Colombo PC, Basner RC, Factor P, LeJemtel TH. Inflammation, oxidative stress, and repair capacity of the vascular endothelium in obstructive sleep apnea. Circulation. 2008;117:2270-2278.
33. Kapsimalis F, Varouchakis G, Manousaki A, Daskas S, Nikita D, Kryger M, Gourgoulianis K. 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;186:209-217.
34. Jelic S, Lederer DJ, Adams T, Padeletti M, Colombo PC, Factor P, Le Jemtel TH. Endothelial repair capacity and apoptosis are inversely related in obstructive sleep apnea. Vasc Health Risk Manag. 2009;5:909-920.
35. Bayram NA, Ciftci B, Keles T, Durmaz T, Turhan S, Bozkurt E, Peker Y. Endothelial function in normotensive men with obstructive sleep apnea before and 6 months after CPAP treatment. Sleep. 2009;32:1257-1263.
36. Chung S, Yoon IY, Lee CH, Kim JW. The association of nocturnal hypoxemia with arterial stiffness and endothelial dysfunction in male patients with obstructive sleep apnea syndrome. Respiration. 2010;79:363-369.
37. Drager LF, Diegues-Silva L, Diniz PM, Bortolotto LA, Pedrosa RP, Couto RB, Marcondes B, Giorgi DM, Lorenzi-Filho G, Krieger EM. Obstructive sleep apnea, masked hypertension, and arterial stiffness in men. Am J Hypertens. 2010;23:249-254.
38. Panoutsopoulos A, Kallianos A, Kostopoulos K, Seretis C, Koufogiorga E, Protogerou A, Trakada G, Kostopoulos C, Zakopoulos N, Nikolopoulos I. Effect of CPAP treatment on endothelial function and plasma CRP levels in patients with sleep apnea. Med Sci Monit. 2012;18:CR747-CR751.
39. Bruno RM, Rossi L, Fabbrini M, Duranti E, Di Coscio E, Maestri M, Guidi P, Frenzilli G, Salvetti A, Taddei S, Bonanni E, Ghiadoni L. Renal vasodilating capacity and endothelial function are impaired in patients with obstructive sleep apnea syndrome and no traditional cardiovascular risk factors. J Hypertens. 2013;31:1456-1464.
40. Noda A, Nakata S, Fukatsu H, Yasuda Y, Miyao E, Miyata S, Yasuma F, Murohara T, Yokota M, Koike Y. Aortic pressure augmentation as a marker of cardiovascular risk in obstructive sleep apnea syndrome. Hypertens Res. 2008;31:1109-1114.
41. 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;265:1275-1279.
42. Jones A, Vennelle M, Connell M, McKillop G, Newby DE, Douglas NJ, Riha RL. Arterial stiffness and endothelial function in obstructive sleep apnoea/hypopnoea syndrome. Sleep Med. 2013;14:428-432.
43. Korkmaz M, Korkmaz H, Kucuker F, Ayyildiz SN, Cankaya S. Evaluation of the association of sleep apnea-related systemic inflammation with CRP, ESR, and neutrophil-to-lymphocyte ratio. Med Sci Monit. 2015;21:477-481.
44. Andaku DK, D'Almeida V, Carneiro G, Hix S, Tufik S, Togeiro SM. Sleepiness, inflammation and oxidative stress markers in middle-aged males with obstructive sleep apnea without metabolic syndrome: a cross-sectional study. Respir Res. 2015;16:3.
45. Ciccone MM, Scicchitano P, Zito A, Cortese F, Boninfante B, Falcone VA, Quaranta VN, Ventura VA, Zucano A, Di Serio F, Damiani MF, Resta O. Correlation between inflammatory markers of atherosclerosis and carotid intima-media thickness in obstructive sleep apnea. Molecules. 2014;19:1651-1662.
46. Hoyos CM, Melehan KL, Liu PY, Grunstein RR, Phillips CL. Does obstructive sleep apnea cause endothelial dysfunction? A critical review of the literature. Sleep Med Rev. 2015;20:15-26.
47. Celermajer DS. Reliable endothelial function testing: at our fingertips? Circulation. 2008;117:2428-2430.
48. Seif F, Patel SR, Walia H, Rueschman M, Bhatt DL, Gottlieb DJ, Lewis EF, Patil SP, Punjabi NM, Babineau DC, Redline S, Mehra R. Association between obstructive sleep apnea severity and endothelial dysfunction in an increased background of cardiovascular burden. J Sleep Res. 2013;22:443-451.
49. Lavie L, Lavie P. Coronary collateral circulation in sleep apnea: a cardioprotective mechanism? Chest. 2010;137:511-512.
50. Montero D, Walther G, Perez-Martin A, Vicente-Salar N, Roche E, Vinet A. Vascular smooth muscle function in type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetologia. 2013;56:2122-2133.
51. Ignarro LJ, Lippton H, Edwards JC, Baricos WH, Hyman AL, Kadowitz PJ, Gruetter CA. Mechanism of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: evidence for the involvement of S-nitrosothiols as active intermediates. J Pharmacol Exp Ther. 1981;218:739-749.
52. Buchner NJ, Quack I, Stegbauer J, Woznowski M, Kaufmann A, Rump LC. Treatment of obstructive sleep apnea reduces arterial stiffness. Sleep Breath. 2012;16:123-133.
53. Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med. 2002;165:1217-1239.
54. Shahar E, Whitney CW, Redline S, Lee ET, Newman AB, Nieto FJ, O'Connor GT, Boland LL, Schwartz JE, Samet JM. 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.
55. Clearfield MB. C-reactive protein: a new risk assessment tool for cardiovascular disease. J Am Osteopath Assoc. 2005;105:409-416.
56. O'Leary DH, Polak JF. Intima-media thickness: a tool for atherosclerosis imaging and event prediction. Am J Cardiol. 2002;90:18L-21L.
57. O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med. 1999;340:14-22.
58. Torzewski M, Rist C, Mortensen RF, Zwaka TP, Bienek M, Waltenberger J, Koenig W, Schmitz G, Hombach V, Torzewski J. C-reactive protein in the arterial intima: role of C-reactive protein receptor-dependent monocyte recruitment in atherogenesis. Arterioscler Thromb Vasc Biol. 2000;20:2094-2099.
59. Lagrand WK, Visser CA, Hermens WT, Niessen HW, Verheugt FW, Wolbink GJ, Hack CE. C-reactive protein as a cardiovascular risk factor: more than an epiphenomenon? Circulation. 1999;100:96-102.
60. Pasceri V, Willerson JT, Yeh ET. Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation. 2000;102:2165-2168.
61. Zwaka TP, Hombach V, Torzewski J. C-reactive protein-mediated low density lipoprotein uptake by macrophages: implications for atherosclerosis. Circulation. 2001;103:1194-1197.
62. Sharma SK, Mishra HK, Sharma H, Goel A, Sreenivas V, Gulati V, Tahir M. 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;9:149-156.
63. Lavie L, Lavie P. Molecular mechanisms of cardiovascular disease in OSAHS: the oxidative stress link. Eur Respir J. 2009;33:1467-1484.
64. Thomas SR, Chen K, Keaney JF Jr. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J Biol Chem. 2002;277:6017-6024.
65. Tanaka T, Nakamura H, Yodoi J, Bloom ET. Redox regulation of the signaling pathways leading to eNOS phosphorylation. Free Radic Biol Med. 2005;38:1231-1242.
66. Laursen JB, Somers M, Kurz S, McCann L, Warnholtz A, Freeman BA, Tarpey M, Fukai T, Harrison DG. Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation. 2001;103:1282-1288.
67. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci USA. 1998;95:9220-9225.
68. Lavie L. Oxidative stress-a unifying paradigm in obstructive sleep apnea and comorbidities. Prog Cardiovasc Dis. 2009;51:303-312.