Endothelial dysfunction in the microcirculation of patients with obstructive sleep apnea

American Journal of Respiratory and Critical Care Medicine

Volumn 182, Issue 12, 2010, Pages 1540-1545

  Patt, Brian T ^a   Jarjoura, David ^a   Haddad, Diane N ^a   Sen, Chandan K ^a   Roy, Sashwati ^a   Flavahan, Nicholas A ^b   Khayat, Rami N ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelial function; Microcirculation; Obstructive sleep apnea

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; PEROXYNITRITE;

ADULT; ARTERY BLOOD FLOW; ARTERY DILATATION; ARTICLE; BRACHIAL ARTERY; CARDIOVASCULAR RISK; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MICROCIRCULATION; PRIORITY JOURNAL; SKIN BIOPSY; SLEEP APNEA SYNDROME;

ADULT; BODY MASS INDEX; BRACHIAL ARTERY; ENDOTHELIUM, VASCULAR; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROCIRCULATION; NITRIC OXIDE SYNTHASE TYPE II; POLYMERASE CHAIN REACTION; RNA; SLEEP APNEA, OBSTRUCTIVE; SUPEROXIDE DISMUTASE; ULTRASONOGRAPHY, DOPPLER, COLOR; VASODILATION;

EID: 78650213191     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201002-0162OC     Document Type: Article

References (54)

1. McNicholas WT, Bonsigore MR. Sleep apnoea as an independent risk factor for cardiovascular disease: current evidence, basic mechanisms and research priorities. Eur Respir J 2007;29:156-178. (Pubitemid 46092013)
2. Campos-Rodriguez F, Pena-Grinan N, Reyes-Nunez N, De la Cruz-Moron I, Perez-Ronchel J, De la Vega-Gallardo F, Fernandez-Palacin A. Mortality in obstructive sleep apnea-hypopnea patients treated with positive airway pressure. Chest 2005;128:624-633.
3. Doherty LS, Kiely JL, Swan V, McNicholas WT. Long-term effects of nasal continuous positive airway pressure therapy on cardiovascular outcomes in sleep apnea syndrome. Chest 2005;127(6):2076-2084.
4. Marin JM, Carrizo SJ, Vicente E, Agusti AG. Long-term cardiovascular outcomes in men with obstructive sleep apnoea-hypopnoea with or without treatment with continuous positive airway pressure: an observational study. Lancet 2005;365(9464):1046-1053. (Pubitemid 40386782)
5. Brooks D, Horner RL, Kozar LF, Render-Teixeira CL, Phillipson EA. Obstructive sleep apnea as a cause of systemic hypertension: Evidence from a canine model. J Clin Invest 1997;99(1):106-109. (Pubitemid 27058300)
6. Young T, Peppard P, Palta M, Hla KM, Finn L, Morgan B, Skatrud J. Population-based study of sleep-disordered breathing as a risk factor for hypertension. Arch Intern Med 1997;157(16):1746-1752. (Pubitemid 27327411)
7. Nieto FJ, Young TB, Lind BK, Shahar E, Samet JM, Redline S, D'Agostino RB, Newman AB, Lebowitz MD, Pickering TG. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep Heart Health Study. JAMA 2000;283(14):1829-1836.
8. Drager LF, Bortolotto LA, Figueiredo AC, Krieger EM, Lorenzi GF. Effects of continuous positive airway pressure on early signs of atherosclerosis in obstructive sleep apnea. Am J Respir Crit Care Med 2007;176(7):706-712.
9. Minoguchi K, Yokoe T, Tazaki T, Minoguchi H, Tanaka A, Oda N, Okada S, Ohta S, Naito H, Adachi M. Increased carotid intima-media thickness and serum inflammatory markers in obstructive sleep apnea. Am J Respir Crit Care Med 2005;172(5):625-630.
10. Drager LF, Bortolotto LA, Lorenzi MC, Figueiredo AC, Krieger EM, Lorenzi-Filho G. Early signs of atherosclerosis in obstructive sleep apnea. Am J Respir Crit Care Med 2005;172(5):613-618. (Pubitemid 41232973)
11. 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(1):26-30.
12. Peker Y, Hedner J, Kraiczi H, Loth S. Respiratory disturbance index: an independent predictor of mortality in coronary artery disease. Am J Respir Crit Care Med 2000;162(1):81-86.
13. 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 2009.
14. West SD, Nicoll DJ, Wallace TM, Matthews DR, Stradling JR. Effect of CPAP on insulin resistance and HbA1c in men with obstructive sleep apnoea and type 2 diabetes. Thorax 2007;62(11):969-974.
15. Arzt M, Young T, Finn L, Skatrud JB, Bradley TD. Association of sleep-disordered breathing and the occurrence of stroke. Am J Respir Crit Care Med 2005;172(11):1447-1451.
16. Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM, Mohsenin V. Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med 2005;353(19):2034-2041. (Pubitemid 41609096)
17. Bassetti CL, Milanova M, Gugger M. Sleep-disordered breathing and acute ischemic stroke: diagnosis, risk factors, treatment, evolution, and long-term clinical outcome. Stroke 2006;37(4):967-972.
18. Good DC, Henkle JQ, Gelber D, Welsh J, Verhulst S. Sleep-disordered breathing and poor functional outcome after stroke. Stroke 1996;27(2):252-259.
19. Brevetti G, Silvestro A, Schiano V, Chiariello M. Endothelial dysfunction and cardiovascular risk prediction in peripheral arterial disease: additive value of flow-mediated dilation to ankle-brachial pressure index. Circulation 2003;108(17):2093-2098.
20. Bugiardini R, Manfrini O, Pizzi C, Fontana F, Morgagni G. Endothelial function predicts future development of coronary artery disease: a study of women with chest pain and normal coronary angiograms. Circulation 2004;109(21):2518-2523.
21. Ip MS, Tse HF, Lam B, Tsang KW, Lam WK. Endothelial function in obstructive sleep apnea and response to treatment. Am J Respir Crit Care Med 2004;169(3):348-353.
22. Grebe M, Eisele HJ, Weissmann N, Schaefer C, Tillmanns H, Seeger W, Schulz R. Antioxidant vitamin C improves endothelial function in obstructive sleep apnea. Am J Respir Crit Care Med 2006;173(8):897-901.
23. Phillips SA, Olson EB, Lombard JH, Morgan BJ. Chronic intermittent hypoxia alters NE reactivity and mechanics of skeletal muscle resistance arteries. J Appl Physiol 2006;100(4):1117-1123.
24. El Solh AA, Saliba R, Bosinski T, Grant BJ, Berbary E, Miller N. Allopurinol improves endothelial function in sleep apnoea: a randomised controlled study. Eur Respir J 2006;27:997-1002. (Pubitemid 44911115)
25. Pieper GM, Dembny K, Siebeneich W. Long-term treatment in vivo with NOX-101, a scavenger of nitric oxide, prevents diabetes-induced endothelial dysfunction. Diabetologia 1998;41:1220-1226.
26. Katayama Y, Shige H, Yamamoto A, Hirata F, Yasuda H. Oral vitamin C ameliorates smoking-induced arterial wall stiffness in healthy volunteers. J Atheroscler Thromb 2004;11:354-357.
27. 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.
28. Roy S, Patel D, Khanna S, Gordillo GM, Biswas S, Friedman A, Sen CK. Transcriptome-wide analysis of blood vessels laser captured from human skin and chronic wound-edge tissue. Proc Natl Acad Sci USA 2007;104:14472-14477.
29. Haddad D, Patt B, Yearsley K, Roy S, Sen C, Khayat R. Oxidative stress in an obstructive sleep apnea population. In: Association of professional sleep societies, vol. 32. Seattle: 2009; p. 1235.
30. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998;97:1837-1847.
31. Geny B, Rouyer O, Doutreleau S, Piquard F. Comments on Point-Counterpoint "Flow-mediated dilation does/does not reflect nitric oxide-mediated endothelial function." J Appl Physiol 2006;100:362.
32. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002;39:257-265.
33. Alguire PC, Mathes BM. Skin biopsy techniques for the internist. J Gen Intern Med 1998;13:46-54.
34. Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ. 8-Isoprostane, a marker of oxidative stress, is increased in exhaled breath condensate of patients with obstructive sleep apnea after night and is reduced by continuous positive airway pressure therapy. Chest 2003;124:1386-1392.
35. Lavie L, Vishnevsky A, Lavie P. Evidence for lipid peroxidation in obstructive sleep apnea. Sleep 2004;27:123-128. (Pubitemid 43906323)
36. Dyugovskaya L, Lavie P, Lavie L. Increased adhesion molecules expression and production of reactive oxygen species in leukocytes of sleep apnea patients. Am J Respir Crit Care Med 2002;165:934-939.
37. Schulz R, Mahmoudi S, Hattar K, Sibelius U, Olschewski H, Mayer K, Seeger W, Grimminger F. Enhanced release of superoxide from polymorphonuclear neutrophils in obstructive sleep apnea: impact of continuous positive airway pressure therapy. Am J Respir Crit Care Med 2000;162:566-570.
38. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000;86:494-501.
39. Mugge A, Elwell JH, Peterson TE, Hofmeyer TG, Heistad DD, Harrison DG. Chronic treatment with polyethylene-glycolated superoxide dismutase partially restores endothelium-dependent vascular relaxations in cholesterol-fed rabbits. Circ Res 1991;69:1293-1300.
40. Ito K, Akita H, Kanazawa K, Yamada S, Terashima M, Matsuda Y, Yokoyama M. Comparison of effects of ascorbic acid on endothelium-dependent vasodilation in patients with chronic congestive heart failure secondary to idiopathic dilated cardiomyopathy versus patients with effort angina pectoris secondary to coronary artery disease. Am J Cardiol 1998;82:762-767.
41. Bouloumie A, Bauersachs J, Linz W, Scholkens BA, Wiemer G, Fleming I, Busse R. Endothelial dysfunction coincides with an enhanced nitric oxide synthase expression and superoxide anion production. Hypertension 1997;30:934-941. (Pubitemid 27441125)
42. 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.
43. Cosentino F, Hishikawa K, Katusic ZS, Luscher TF. High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 1997;96:25-28.
44. Bauersachs J, Bouloumie A, Fraccarollo D, Hu K, Busse R, Ertl G. Endothelial dysfunction in chronic myocardial infarction despite increased vascular endothelial nitric oxide synthase and soluble guanylate cyclase expression: role of enhanced vascular superoxide production. Circulation 1999;100:292-298.
45. Ozaki M, Kawashima S, Yamashita T, Hirase T, Namiki M, Inoue N, Hirata K, Yasui H, Sakurai H, Yoshida Y, et al. Overexpression of endothelial nitric oxide synthase accelerates atherosclerotic lesion formation in apoE-deficient mice. J Clin Invest 2002;110:331-340.
46. Huie RE, Padmaja S. The reaction of no with superoxide. Free Radic Res Commun 1993;18:195-199.
47. Vasquez-Vivar J, Whitsett J, Martasek P, Hogg N, Kalyanaraman B. Reaction of tetrahydrobiopterin with superoxide: EPR-kinetic analysis and characterization of the pteridine radical. Free Radic Biol Med 2001;31:975-985. (Pubitemid 32939393)
48. Kuzkaya N, Weissmann N, Harrison DG, Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 2003;278:22546-22554.
49. Shi W, Wang X, Shih DM, Laubach VE, Navab M, Lusis AJ. Paradoxical reduction of fatty streak formation in mice lacking endothelial nitric oxide synthase. Circulation 2002;105:2078-2082.
50. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, Channon KM. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 2002;105:1656-1662.
51. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003;111:1201-1209.
52. Maier W, Cosentino F, Lutolf RB, Fleisch M, Seiler C, Hess OM, Meier B, Luscher TF. Tetrahydrobiopterin improves endothelial function in patients with coronary artery disease. J Cardiovasc Pharmacol 2000;35:173-178. (Pubitemid 30073806)
53. Agewall S, Henareh L, Kublickiene K. Endothelial function in conduit and resistance arteries in men with coronary disease. Atherosclerosis 2006;184:130-136.
54. Park JB, Charbonneau F, Schiffrin EL. Correlation of endothelial function in large and small arteries in human essential hypertension. J Hypertens 2001;19:415-420.