Skip to main content
Top
Published in: Sleep and Breathing 3/2011

01-09-2011 | Original Article

Obstructive sleep apnea causes oxidative damage to plasma lipids and proteins and decreases adiponectin levels

Authors: Ebru Vatansever, Esma Surmen-Gur, Ahmet Ursavas, Mehmet Karadag

Published in: Sleep and Breathing | Issue 3/2011

Login to get access

Abstract

Pupose

Obstructive sleep apnea (OSA) is associated with various metabolic disorders, and oxidative stress was suggested to play an important role. In the present study, we aimed to investigate serum adiponectin and oxidative stress markers, especially protein carbonyls, and to evaluate the correlation between these parameters and lipid, insulin and fasting glucose concentrations in OSA patients and controls.

Method

Blood was drawn from healthy male volunteers following full-night polysomnographic evaluation. Subjects were classified as controls (n = 24), mild OSA group (n = 9) and moderate-severe OSA group (n = 17) according to their apnea–hypopnea indices (AHIs). Serum lipids, fasting glucose, adiponectin, malondialdehyde (MDA), protein carbonyl concentrations, and paraoxonase activities were measured in all subjects.

Results

Results of this study indicated that serum adiponectin concentrations were significantly decreased and MDA and protein carbonyl concentrations were significantly elevated in OSA patients compared to the controls. Protein carbonyl and MDA concentrations were significantly and positively correlated with AHI, while a significant negative correlation was found between adiponectin concentrations and AHI. Adiponectin levels were negatively correlated with MDA levels.

Conclusion

Results of this study, which is the first human study investigating and describing serum protein carbonyl concentrations in OSA patients, reveal that OSA causes increments in oxidative damage and decreases adiponectin levels. The recurrent hypoxia-reoxygenation attacks in OSA patients may activate oxidative stress, elevating sympathetic activity and leading to low levels of adiponectin.
Literature
1.
go back to reference Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ (2003) 8-Isoprostane, a marker of oxidative stress, is increased in exhaled breath condensate of patients with obstructive sleep apnea after night is reduced by continious positive air way pressure therapy. Chest 124:1386–1392PubMedCrossRef Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ (2003) 8-Isoprostane, a marker of oxidative stress, is increased in exhaled breath condensate of patients with obstructive sleep apnea after night is reduced by continious positive air way pressure therapy. Chest 124:1386–1392PubMedCrossRef
2.
go back to reference Christou K, Markoulis N, Moulas AN, Pastaka C, Gourgoulianis KI (2003) Reactive oxygen metabolites (ROMs) as an index of oxidative stress in obstructive sleep apnea patients. Sleep Breath 7:105–110PubMedCrossRef Christou K, Markoulis N, Moulas AN, Pastaka C, Gourgoulianis KI (2003) Reactive oxygen metabolites (ROMs) as an index of oxidative stress in obstructive sleep apnea patients. Sleep Breath 7:105–110PubMedCrossRef
3.
go back to reference Saarelainen S, Lehtimaki T, Jaak-Kola O, Poussa T, Nikkila M, Solakivi T, Nieminen MM (1996) Autoantibodies against oxidised low-density lipoprotein in patients with obstructive sleep apneoea. Clin Chem Lab Med 37:517–520CrossRef Saarelainen S, Lehtimaki T, Jaak-Kola O, Poussa T, Nikkila M, Solakivi T, Nieminen MM (1996) Autoantibodies against oxidised low-density lipoprotein in patients with obstructive sleep apneoea. Clin Chem Lab Med 37:517–520CrossRef
4.
go back to reference Jordan W, Berger C, Cohrs S, Rodenbeck A, Mayer G, Niedmann PD, vanAhsen N, Rüther E, Kornhuber J, Bleich S (2004) CPAP-therapy efficiently lowers serum homocysteine in obstructive sleep apnea syndrome. J Neural Transm 111:683–689PubMedCrossRef Jordan W, Berger C, Cohrs S, Rodenbeck A, Mayer G, Niedmann PD, vanAhsen N, Rüther E, Kornhuber J, Bleich S (2004) CPAP-therapy efficiently lowers serum homocysteine in obstructive sleep apnea syndrome. J Neural Transm 111:683–689PubMedCrossRef
5.
go back to reference Lavie L (2003) Obstructive sleep apnoea syndrome—an oxidative stress disorder. Sleep Med Rev 7:35–51PubMedCrossRef Lavie L (2003) Obstructive sleep apnoea syndrome—an oxidative stress disorder. Sleep Med Rev 7:35–51PubMedCrossRef
6.
7.
go back to reference Ip MS, Lam B, Ng MM, Lam WK, Tsang KW, Lam KS (2002) Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med 165:670–676PubMed Ip MS, Lam B, Ng MM, Lam WK, Tsang KW, Lam KS (2002) Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med 165:670–676PubMed
8.
go back to reference Punjabi NM, Sorkin JD, Katzel LI, Goldberg AP, Schwartz AR, Smith PL (2002) Sleepdisordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 165:677–682PubMed Punjabi NM, Sorkin JD, Katzel LI, Goldberg AP, Schwartz AR, Smith PL (2002) Sleepdisordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 165:677–682PubMed
9.
go back to reference Meslier N, Gagnadoux F, Giraud P, Person C, Ouksel H, Urban T, Racineux J-L (2003) Impaired glucose-insulin metabolism in males with obstructive sleep apnoea syndrome. Eur Respir J 22:156–160PubMedCrossRef Meslier N, Gagnadoux F, Giraud P, Person C, Ouksel H, Urban T, Racineux J-L (2003) Impaired glucose-insulin metabolism in males with obstructive sleep apnoea syndrome. Eur Respir J 22:156–160PubMedCrossRef
10.
go back to reference Newman AB, Nieto FJ, Guidry U, Lind BK, Redline S, Shahar E, Pickering TG, Quan SF (2001) Sleep Heart Health Study Research Group. Relation of sleepdisordered breathing to cardiovascular disease risk factors: the Sleep Heart Health Study. Am J Epidemiol 154:50–59PubMedCrossRef Newman AB, Nieto FJ, Guidry U, Lind BK, Redline S, Shahar E, Pickering TG, Quan SF (2001) Sleep Heart Health Study Research Group. Relation of sleepdisordered breathing to cardiovascular disease risk factors: the Sleep Heart Health Study. Am J Epidemiol 154:50–59PubMedCrossRef
11.
go back to reference McArdle N, Hillman D, Beilin L, Watts G (2007) Metabolic risk factors for vascular disease in obstructive sleep apnea: a matched controlled study. Am J Respir Crit Care Med 175:190–195PubMedCrossRef McArdle N, Hillman D, Beilin L, Watts G (2007) Metabolic risk factors for vascular disease in obstructive sleep apnea: a matched controlled study. Am J Respir Crit Care Med 175:190–195PubMedCrossRef
12.
go back to reference Tan KC, Chowa W-S, Lama JC, Lama B, Wong W-K, Tamb S, Ipl MS (2006) HDL dysfunction in obstructive sleep apnea. Atherosclerosis 184:377–382PubMedCrossRef Tan KC, Chowa W-S, Lama JC, Lama B, Wong W-K, Tamb S, Ipl MS (2006) HDL dysfunction in obstructive sleep apnea. Atherosclerosis 184:377–382PubMedCrossRef
13.
go back to reference Sharma SK, Kumpawat S, Goel A, Banga A, Ramakrishnan L, Chaturvedi P (2007) Obesity and not obstructive sleep apnea is responsible for metabolic abnormalities in a cohort with sleep disordered breathing. Sleep Medicine 8:12–17PubMedCrossRef Sharma SK, Kumpawat S, Goel A, Banga A, Ramakrishnan L, Chaturvedi P (2007) Obesity and not obstructive sleep apnea is responsible for metabolic abnormalities in a cohort with sleep disordered breathing. Sleep Medicine 8:12–17PubMedCrossRef
14.
go back to reference Ciftci TU, Kokturk O, Bukan N, Bilgihan A (2005) Leptin and ghrelin levels in patients with obstructive sleep apnea syndrome. Respiration 72:395–401CrossRef Ciftci TU, Kokturk O, Bukan N, Bilgihan A (2005) Leptin and ghrelin levels in patients with obstructive sleep apnea syndrome. Respiration 72:395–401CrossRef
15.
go back to reference Punjabi NM, Sorkin JD, Katzel LI, Goldberg AP, Schwartz AR, Smith PL (2002) Sleep-disordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 165:677–682PubMed Punjabi NM, Sorkin JD, Katzel LI, Goldberg AP, Schwartz AR, Smith PL (2002) Sleep-disordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 165:677–682PubMed
16.
go back to reference Punjabi NM, Shahar E, Redline S, Gottlieb DJ, Givelber R, Resnick HE (2004) Sleep Heart Health Study Investigators. Sleepdisordered breathing, glucose intolerance, and insulin resistance: the sleep heart health Study. Am J Epidemiol 160:521–530PubMedCrossRef Punjabi NM, Shahar E, Redline S, Gottlieb DJ, Givelber R, Resnick HE (2004) Sleep Heart Health Study Investigators. Sleepdisordered breathing, glucose intolerance, and insulin resistance: the sleep heart health Study. Am J Epidemiol 160:521–530PubMedCrossRef
17.
go back to reference Lihn AS, Pedersen SB, Richelsen B (2005) Adiponectin: action, regulation and association to insulin sensitivity. Obes Rev 6:13–21PubMedCrossRef Lihn AS, Pedersen SB, Richelsen B (2005) Adiponectin: action, regulation and association to insulin sensitivity. Obes Rev 6:13–21PubMedCrossRef
18.
go back to reference Fantuzzi G (2005) Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 115:911–919PubMedCrossRef Fantuzzi G (2005) Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 115:911–919PubMedCrossRef
19.
go back to reference Masserini B, Morpurgo PS, Donadio F, Baldessari C, Bossi R, Beck-Peccoz P, Orsi E (2006) Reduced levels of adiponectin in sleep apnea syndrome. J Endocrinol Invest 29:700–705PubMed Masserini B, Morpurgo PS, Donadio F, Baldessari C, Bossi R, Beck-Peccoz P, Orsi E (2006) Reduced levels of adiponectin in sleep apnea syndrome. J Endocrinol Invest 29:700–705PubMed
20.
go back to reference Harsch IA, Schahin SP, Radespiel-Tröger M, Weintz O, Jahreiss H, Fuchs FS, Wiest GH, Hahn EG, Lohmann T, Konturek PC, Ficker JH (2004) Continious positive airway pressure tratment rapidly improves insulin sensitivity in patients with obstructive sleep apnea syndrome. Am J Respir Crit Care Med 169:156–162PubMedCrossRef Harsch IA, Schahin SP, Radespiel-Tröger M, Weintz O, Jahreiss H, Fuchs FS, Wiest GH, Hahn EG, Lohmann T, Konturek PC, Ficker JH (2004) Continious positive airway pressure tratment rapidly improves insulin sensitivity in patients with obstructive sleep apnea syndrome. Am J Respir Crit Care Med 169:156–162PubMedCrossRef
21.
go back to reference Makino S, Handa H, Suzukawa K, Fujiwara M, Nakamura M, Muraoka S, Takasago I, Tanaka Y, Hashimato K, Sugimoto T (2006) Obstructive sleep apnoea syndrome, plasma adiponectin levels, and insulin resistance. Clin Endocrinol 64:12–19CrossRef Makino S, Handa H, Suzukawa K, Fujiwara M, Nakamura M, Muraoka S, Takasago I, Tanaka Y, Hashimato K, Sugimoto T (2006) Obstructive sleep apnoea syndrome, plasma adiponectin levels, and insulin resistance. Clin Endocrinol 64:12–19CrossRef
22.
go back to reference Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S (1993) The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 328:1230–1235PubMedCrossRef Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S (1993) The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 328:1230–1235PubMedCrossRef
23.
go back to reference Banno K, Walld R, Kryger MH (2005) Increasing obesity trends in patients with sleep breathing disorders referred to a sleep disorders centre. J Clin Sleep Med 1:364–366PubMed Banno K, Walld R, Kryger MH (2005) Increasing obesity trends in patients with sleep breathing disorders referred to a sleep disorders centre. J Clin Sleep Med 1:364–366PubMed
24.
go back to reference Vgontzas AN, Papanicolaou DA, Bixler EO, Kales A, Tyson K, Chrousos GP (1997) Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab 82:1313–1316PubMedCrossRef Vgontzas AN, Papanicolaou DA, Bixler EO, Kales A, Tyson K, Chrousos GP (1997) Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab 82:1313–1316PubMedCrossRef
25.
go back to reference Soares AF, Guichardant M, Cozzone D, Bernoud-Hubac N, Bouzaïdi-Tiali N, Lagarde M, Géloën A (2005) Effects of oxidative stress on adiponectin secretion and lactate production in 3T3-L1 adipocytes. Free Radic Biol Med 38:882–889PubMedCrossRef Soares AF, Guichardant M, Cozzone D, Bernoud-Hubac N, Bouzaïdi-Tiali N, Lagarde M, Géloën A (2005) Effects of oxidative stress on adiponectin secretion and lactate production in 3T3-L1 adipocytes. Free Radic Biol Med 38:882–889PubMedCrossRef
26.
go back to reference Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419PubMedCrossRef Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419PubMedCrossRef
27.
go back to reference Young IS, Trimble ER (1991) Measurement of malondialdehyde in plasma by high performance liquid chromatography with fluorimetric detection. Ann Clin Biochem 28:504–508PubMed Young IS, Trimble ER (1991) Measurement of malondialdehyde in plasma by high performance liquid chromatography with fluorimetric detection. Ann Clin Biochem 28:504–508PubMed
28.
go back to reference Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363PubMedCrossRef Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363PubMedCrossRef
29.
go back to reference Eckerson HW, Wyte CM, La Du BN (1983) The human serum paraoxonase/arylesterase polymorphism. Am J Hum Genet 35:1126–1138PubMed Eckerson HW, Wyte CM, La Du BN (1983) The human serum paraoxonase/arylesterase polymorphism. Am J Hum Genet 35:1126–1138PubMed
30.
go back to reference Lavie L, Vishnevsky A, Lavie P (2004) Evidence for lipid peroxidation in obstructive sleep apnea. Sleep 27:123–128PubMed Lavie L, Vishnevsky A, Lavie P (2004) Evidence for lipid peroxidation in obstructive sleep apnea. Sleep 27:123–128PubMed
31.
go back to reference Barcelo A, Miralles C, Barbe F, Vila M, Pons S, Agusti AG (2000) Abnormal lipid peroxidation in patients with sleep apnoea. Eur Respir J 16:644–647PubMedCrossRef Barcelo A, Miralles C, Barbe F, Vila M, Pons S, Agusti AG (2000) Abnormal lipid peroxidation in patients with sleep apnoea. Eur Respir J 16:644–647PubMedCrossRef
32.
go back to reference Itzhaki S, Dorchin H, Clark G, Lavie L, Lavie P, Pillar G (2007) The effects of 1-year treatment with a herbst mandibular advancement splint on obstructive sleep apnea, oxidative stress, and endothelial function. Chest 131:740–749PubMedCrossRef Itzhaki S, Dorchin H, Clark G, Lavie L, Lavie P, Pillar G (2007) The effects of 1-year treatment with a herbst mandibular advancement splint on obstructive sleep apnea, oxidative stress, and endothelial function. Chest 131:740–749PubMedCrossRef
33.
go back to reference Lavie L (2005) Sleep-disordered breathing and cerebrovascular disease: a mechanistic approach. Neurol Clin 23:1059–1075PubMedCrossRef Lavie L (2005) Sleep-disordered breathing and cerebrovascular disease: a mechanistic approach. Neurol Clin 23:1059–1075PubMedCrossRef
34.
go back to reference Suzuki YJ, Jain V, Park AM, Day RM (2006) Oxidative stress and oxidant signaling in obstructive sleep apnea and associated cardiovascular diseases. Free Radic Biol Med 40:1683–1692PubMedCrossRef Suzuki YJ, Jain V, Park AM, Day RM (2006) Oxidative stress and oxidant signaling in obstructive sleep apnea and associated cardiovascular diseases. Free Radic Biol Med 40:1683–1692PubMedCrossRef
35.
go back to reference Arnardottir ES, Mackiewicz M, Gislason T, Teff KL, Pack AI (2009) Molecular sigantures of obstructive sleep apnea in adults: a riview and perspective. Sleep 32:447–470PubMed Arnardottir ES, Mackiewicz M, Gislason T, Teff KL, Pack AI (2009) Molecular sigantures of obstructive sleep apnea in adults: a riview and perspective. Sleep 32:447–470PubMed
36.
go back to reference Sonka K, Fialová L, Volná J, Jiroutek P, Vávrová J, Kemlink D, Pretl M, Kalousová M (2008) Advanced oxidation protein products in obstructive sleep apnea. Prague Med Rep 109:159–165PubMed Sonka K, Fialová L, Volná J, Jiroutek P, Vávrová J, Kemlink D, Pretl M, Kalousová M (2008) Advanced oxidation protein products in obstructive sleep apnea. Prague Med Rep 109:159–165PubMed
37.
go back to reference Tanriverdi H, Evrengul H, Kuru O, Tanriverdi S, Seleci D, Enli Y, Kaftan HA, Kilic M (2006) Cigarette smoking induced oxidative stress may impair endothelial function and coronary blood flow in angiographically normal coronary arteries. Circ J 70(5):593–599PubMedCrossRef Tanriverdi H, Evrengul H, Kuru O, Tanriverdi S, Seleci D, Enli Y, Kaftan HA, Kilic M (2006) Cigarette smoking induced oxidative stress may impair endothelial function and coronary blood flow in angiographically normal coronary arteries. Circ J 70(5):593–599PubMedCrossRef
38.
go back to reference Lavie P (2004) Evidence for lipid peroxidation in obstructive sleep apnea. Sleep 27(1):123–8PubMed Lavie P (2004) Evidence for lipid peroxidation in obstructive sleep apnea. Sleep 27(1):123–8PubMed
39.
go back to reference Trujillo ME, Scherer PE (2005) Adiponectin—journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med 257:167–175PubMedCrossRef Trujillo ME, Scherer PE (2005) Adiponectin—journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med 257:167–175PubMedCrossRef
40.
go back to reference Buckley TM, Schatzberg AF (2005) On the interactions of the hypothalamic–pituitary–adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rythm, exemplary sleep disorders. J Clin Endocrinol Metab 90:3106–3114PubMedCrossRef Buckley TM, Schatzberg AF (2005) On the interactions of the hypothalamic–pituitary–adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rythm, exemplary sleep disorders. J Clin Endocrinol Metab 90:3106–3114PubMedCrossRef
41.
go back to reference Bruun JM, Lihn AS, Verdich C, Pedersen SB, Toubro S, Astrup A, Richelsen B (2003) Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans. Am J Physiol Endocrinol Metab 285:527–533 Bruun JM, Lihn AS, Verdich C, Pedersen SB, Toubro S, Astrup A, Richelsen B (2003) Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans. Am J Physiol Endocrinol Metab 285:527–533
Metadata
Title
Obstructive sleep apnea causes oxidative damage to plasma lipids and proteins and decreases adiponectin levels
Authors
Ebru Vatansever
Esma Surmen-Gur
Ahmet Ursavas
Mehmet Karadag
Publication date
01-09-2011
Publisher
Springer-Verlag
Published in
Sleep and Breathing / Issue 3/2011
Print ISSN: 1520-9512
Electronic ISSN: 1522-1709
DOI
https://doi.org/10.1007/s11325-010-0378-8

Other articles of this Issue 3/2011

Sleep and Breathing 3/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.