Abstract
Purpose
Obstructive sleep apnea (OSA) and chronic obstructive pulmonary disease (COPD) have been known to be associated with atherosclerosis and hypoxia which was suggested to have an important role in this process by the way of increased oxidative stress. In the present study, we aimed to evaluate the effects of nocturnal hypoxia pattern (intermittent versus sustained) on serum lipid peroxidation and paraoxonase (PON) activity.
Methods
Blood collections were performed in 44 OSA, 11 non-apneic, nocturnal desaturated COPD, and 14 simple snorer patients after full-night polysomnographic recordings. Nocturnal sleep and respiratory parameters, oxygen desaturation indexes, serum malondialdehyde (MDA) levels by measuring with the help of the formation of thiobarbituric acid reactive substances (TBARS), and PON activity were assessed in all subjects.
Results
OSA and COPD patients showed nocturnal hypoxemia, with a minimum oxygen saturation (SaO2) in ranges of 53–92 % and 50–87 %, respectively. The mean levels of TBARS was 15.7 ± 3.6 nmol and 15.3 ± 3.4 nmol malondialdehyde (MDA)/ml in OSA and COPD patients, respectively, while the mean level of the control group was 4.1 ± 1.2 nmol MDA/ml. The mean PON activity was found to be 124.2 ± 35.5 U/l in OSA patients and 124.6 ± 28.4 U/l in COPD patients. The mean PON activity of the control group was 269.0 ± 135.8 U/l. The increase in TBARS levels and the decrease in PON1 levels were statistically significant in both OSA and COPD patients according to controls (p < 0.001 for TBARS as well as PON1).
Conclusion
The results of this study revealed that both OSA and non-apneic, nocturnal desaturated COPD patients showed increased levels of lipid peroxidation and decreased PON activity despite the differences in nocturnal hypoxia pattern.
Similar content being viewed by others
References
Peker Y, Kraiczi H, Hedner J, Loth S, Johansson A, Bende M (1999) An independent association between obstructive sleep apnoea and coronary artery disease. Eur Res J 14:179–184
Yaggi H, Mohsenin V (2003) Sleep-disordered breathing and stroke. Clin Chest Med 24:223–237
Camilli AG, Robbins DR, Lebowitz MD (1991) Death certificate reporting of confirmed airways obstructive disease. Am J Epidemiol 133:795–800
MacNee W, Maclay J, McAllister D (2008) Cardiovascular injury and repair in chronic obstructive pulmonary disease. Proc Am Thorac Soc 5:824–833
Kluchova Z, Perrasova P, Joppa DZ, Tkacova R (2007) The association between oxidative stress and obstructive lung impairment in patients with COPD. Physiol Res 56:51–56
Coulson JM, Rudd JHF, Duckers JM, Rees JLS, Shale DJ, Bolton CE, Cockcroft JR (2010) Excessive aortic inflammation in chronic obstructive pulmonary disease: an 18 F-FDG PET pilot study. J Nucl Med 51:1357–1360
Lavie P, Lavie L (2008) Cardiovascular morbidity and mortality in obstructive sleep apnea. Curr Pharmaceut Des 14:3466–3473
Fletcher EC, Miller J, Divine GW, Fletcher RN, Miller T (1987) Nocturnal oxyhemoglobin desaturation in COPD patients with arterial oxygen tension above 60 mmHg. Chest 92:604–608
Fletcher EC, Luckett RA, Goodnight-White S, Miller CC, Qian W, Costarangoz-Galarza C (1992) A double blind trial of nocturnal supplement oxygen for sleep desaturation in patient with chronic obstructive pulmonary disease and a daytime PaO2 >60 mmHg. Am Rev Respir Dis 145:1070–1076
Schünemann HJ, Dorn J, Grant BJ, Winkelstein W Jr, Trevisan M (2000) Pulmonary function is a long-term predictor of mortality in the general population: 29-year follow-up of the Buffalo Health Study. Chest 118:656–664
Hole DJ, Watt GC, Davey-Smith G, Hart CL, Gillis CR, Hawthorne VM (1996) Impaired lung function and mortality risk in men and women: findings from the Renfrew and Paisley prospective population study. BMJ 313:711–715
Mackness MI, Durrington PN, Mackness B (2004) The role of paraoxonase 1 activity in cardiovascular disease. Am J Cardiovasc Drugs 4(4):211–217
Lavie L, Vishnevsky A, Lavie P (2004) Evidence for lipid peroxidation in obstructive sleep apnea. Sleep 27:123–128
Yamauchi M, Nakano H, Maekawa J, Okamoto Y, Ohnishi Y, Suzuki T, Kimura H (2005) Oxidative stress in obstructive sleep apnea. Chest 127:1674–1679
Minoguchi K, Yokoe T, Tanaka A, Ohta S, Hirano T, Yoshino G, Q’Donnell CP, Adachi M (2006) Association between lipid peroxidation and inflammation in obstructive sleep apnoea. Eur Respir J 28:378–385
MacNee W (2000) Oxidants/antioxidants and COPD. Chest 117:303–317
Chess PR, O'Reilly MA, Sachs F, Finkelstein JN (2005) Reactive oxidant and p42/44MAP kinase signaling is necessary for mechanical strain-induced proliferation in pulmonary epithelial cells. J Appl Physiol 99(3):1226–1232
Papaiahgari S, Yerrapureddy A, Hassoun PM, Garcia JG, Birukov KG, Reddy SP (2007) EGFR-activated signaling and actin remodeling regulate cyclic stretch-induced NRF2-ARE activation. Am Respir Cell Mol Biol 36(3):304–312
McQuaid KE, Smyth EM, Keenan AK (1996) Evidence for modulation of hydrogen peroxide induced endothelial barrier dysfunction by nitric oxide in vitro. Eur J Pharmacol 307(2):233–241
McCord JM (1985) Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312:159–63
Schünemann HJ, Dorn J, Grant BJ, Winkelstein W Jr, Trevisan M (2000) Pulmonary function is a long-term predictor of mortality in the general population: 29-year follow-up of the Buffalo Health Study. Chest 118:656–664
Friedman GD, Klatsky AL (1976) Siegelaub AB. Lung function and risk of myocardial infarction and sudden cardiac death. N Engl J Med 294:1071–1075
Johns MW (1992) Reliability and factor analysis of the Epworth Sleepiness Scale. Sleep 15(4):376–381
Pauwels RA, Buıst AS, Calverley PMA (2001) Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global initiative for chronic obstructive lung disease (GOLD) workshop summary. Am J Respir Crit Care Med 163:1256–1276
Iber K, Ancoli-Israel S, Chesson AL, Quan SF (2007) The AASM manual for the scoring of sleep and associated events. American Academy of Sleep Medicine, Westchester
Mackness MI, Harty D, Bhatnagar D, Winocour PH, Arrol S, Ishola M, Durrington PN (1991) Serum paraoxonase activity in familial hypercholesterolaemia and insulin-dependent diabetes mellitus. Atherosclerosis 86:193–199
Yagi K (1984) Assay for blood plasma or serum. Methods Enzymol 105:328–31
Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57:715–725
Alzoghaibi MA, BaHammam AS (2011) The effect of night of continuous positive airway pressure therapy on oxidative stress and antioxidant defense in hypertensive patients with severe obstructive sleep apnea. Sleep Breath;doi 10.1007/s11325-011-0531-z.
Dorkova Z, Petrasova D, Molcanyiova A, Popovnakova M, Tkacova R (2008) Effects of continuous positive airway pressure on cardiovascular risk profile in patients whit severe obstructive sleep apnea and metabolic syndrome. Chest 134:686–692
Vatansever E, Surmen-Gur E, Ursavaş A, Karadağ M (2011) Obstructive sleep apnea causes oxidative damage to plasma lipids and proteins and decreases adiponectin levels. Sleep Breath 15:275–282
Rahman I, Skwarska E, MacNee W (1997) Attenuation of oxidant/antioxidant imbalance during treatment of exacerbation of chronic obstructive pulmonary disease. Thorax 52:565–568
Stanojkovic I, Kotur-Stevuljevic J, Milenkovic B, Spasic S, Vujic T, Stefanovic A, Ilic A, Ivanisevic J (2011) Pulmonary function, oxidative stress and inflammatory markers in severe COPD exacerbation. Respir Med 105:31–37
Aviram M (1996) Interaction of oxidized low density lipoprotein with macrophages in atherosclerosis and the antiatherogenicity of antioxidant. Eur J Clin Chem Clin Biochem 34:599–608
Steinberg DS, Parthasarathy TE, Carew JC Khoo, Witztum JL (1989) Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 320:915–924
Aviram M (1993) Modified forms of low density lipoprotein and atherosclerosis. Atherosclerosis 98:1–9
Mitchinson MJ, Ball RY, Carpenter KL, Enright JH (1990) Macrophages and ceroid in human atherosclerosis. Eur Heart J 11:116–121
Aviram M, Rosenblat M, Bisgaier CL, Newton RS, Primo-Parmo SL, La Du BN (1998) Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. J Clin Invest 101(8):1581–1590
Leuenberger UA, Hogeman CS, Quraishi S, Linton-Frazier L, Gray KS (2007) Short-term intermittent hypoxia enhances sympathetic responses to continuous hypoxia in humans. J Appl Physiol 103:835–842
Gilmartin GS, Lynch M, Tamisier R, Weiss JW (2010) Chronic intermittent hypoxia in humans during 28 nights results in blood pressure elevation and increased muscle sympathetic nerve activity. Am J Physiol Heart Circ Physiol 299:925–931
Tamisier R, Gilmartin GS, Launois SH, Pepin JL, Nespoulet H, Thomas R, Levy P, Weiss JW (2009) A new model of chronic intermittent hypoxia in humans: effect on ventilation, sleep, and blood pressure. J Appl Physiol 107:17–24
Rajagopalan S, Kurz S, Münzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG (1996) Angiotensin II mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation: contribution to alterations of vasomotor tone. J Clin Invest 97:1916–1923
Inoue N, Kawashima S, Hirata KI, Rikitake Y, Takeshita S, Yamochi W, Akita H, Yokoyama M (1998) Stretch force on vascular smooth muscle cells enhances oxidation of LDL via superoxide production. Am J Physiol 274:1928–1932
Urakawa H, Katsuki A, Sumida Y, Gabazza EC, Murashima S, Morioka K, Maruyama N, Kitagawa N, Tanaka T, Hori Y, Nakatani K, Yano Y, Adachi Y (2003) Oxidative stress is associated with adiposity and insulin resistance in men. J Clin Endocrinol Metab 88:4673–4676
Suzuki K, Ito Y, Ochiai J, Kusuhara Y, Hashimoto S, Tokudome S, Kojima M, Wakai K, Toyoshima H, Tamakoshi K, Watanabe Y, Hayakawa N, Maruta M, Watanabe M, Kato K, Ohta Y, Tamakoshi A (2003) JACC Study Group. Relationship between obesity and serum markers of oxidative stress and inflammation in Japanese. Asian Pac J Cancer Prev 4:259–266
Harman SM, Liang L, Tsitouras PD, Gucciardo F, Heward CB, Reaven PD, Ping W, Ahmed A, Cutler RG (2003) Urinary excretion of three nucleic acid oxidation adducts and isoprostane F(2) measured by liquid chromatography–mass spectrometry in smokers, ex-smokers, and nonsmokers. Free Radic Biol Med 35:1301–1309
Kirkham PA, Spooner G, Ffoulkes-Jones C, Calvez R (2003) Cigarette smoke triggers macrophage adhesion and activation: role of lipid peroxidation products and scavenger receptor. Free Radic Biol Med 35:697–710
Ohara Y, Peterson TE, Harrison DG (1993) Hypercholesterolemia increases endothelial superoxide anion production. J Clin Invest 91:2546–2551
Cosentino F, Hishikawa K, Katusic ZS, Lüscher TF (1997) High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96:25–28
Kashiwagi A, Shinozaki K, Nishio Y, Maegawa H, Maeno Y, Kanazawa A, Kojima H, Haneda M, Hikada H, Yasuda H, Kikkawa R (1999) Endothelium-specific activation of NAD(P)H oxidase in aortas of exogenously hyperinsulinemic rats. Am J Physiol 277:976–983
Tekes S, Isik B, Yildiz T, Simsek S, Isik MR, Budak T (2010) Chronic obstructive pulmonary disease and paraoxonase 1 192 and 55 gene polymorphisms. Biotechnology & Biotechnological Equipment 24(1):1644–1647
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Okur, H.K., Pelin, Z., Yuksel, M. et al. Lipid peroxidation and paraoxonase activity in nocturnal cyclic and sustained intermittent hypoxia. Sleep Breath 17, 365–371 (2013). https://doi.org/10.1007/s11325-012-0703-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11325-012-0703-5