Top

Sleep and Breathing

Published in:

11-07-2023 | Sleep Apnea | Sleep Breathing Physiology and Disorders • Original Article

The effects of disease severity and comorbidity on oxidative stress biomarkers in obstructive sleep apnea

Authors: Tuğba Raika Kıran, Önder Otlu, Mehmet Erdem, Ayşegül Altıntop Geçkil, Nurcan Kırıcı Berber, Erdal İn

Published in: Sleep and Breathing | Issue 1/2024

Abstract

Purpose

Ischemia-modified albumin (IMA), total oxidant status (TOS), and total antioxidant status (TAS) are biomarkers used to evaluate oxidative stress status in various diseases including obstructive sleep apnea (OSA). In this study, we investigated the effects of disease severity and comorbidity on IMA, TOS and TAS levels in OSA.

Methods

Patients with severe OSA (no-comorbidity, one comorbidity, and multiple comorbidities) and mild–moderate OSA (no-comorbidity, one and multiple comorbidities), and healthy controls were included in the study. Polysomnography was applied to all cases and blood samples were taken from each participant at the same time of day. ELISA was used to measure IMA levels in serum samples and colorimetric commercial kits were used to perform TOS and TAS analyses. In addition, routine biochemical analyses were performed on all serum samples.

Results

A total of 74 patients and 14 healthy controls were enrolled. There was no statistically significant difference between the disease groups according to gender, smoking status, age, body mass index (BMI), HDL, T3, T4, TSH, and B12 (p > 0.05). As the severity of OSA and comorbidities increased, IMA, TOS, apnea–hypopnea index (AHI), desaturation index (T90), cholesterol, LDL, triglyceride, AST, and CRP values increased significantly (p < 0.05). On the other hand, TAS, minimum desaturation, and mean desaturation values decreased significantly (p < 0.05).

Conclusions

We concluded that IMA, TOS, and TAS levels may indicate OSA–related oxidative stress, but as the severity of OSA increases and with the presence of comorbidity, IMA and TOS levels may increase and TAS levels decrease. These findings suggest that disease severity and presence/absence of comorbidity should be considered in studies on OSA.

Carberry JC, Jordan AS, White DP, Wellman A, Eckert DJ (2016) Upper airway collapsibility (Pcrit) and pharyngeal dilator muscle activity are sleep stage dependent. Sleep 39(3):511–521. https://doi.org/10.5665/sleep.5516CrossRefPubMedPubMedCentral

Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, Redline S, Strohl KP, Davidson Ward SL, Tangredi MM (2012) Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med 8(5):597–619. https://doi.org/10.5664/jcsm.2172CrossRefPubMedPubMedCentral

Sánchez-de-la-Torre M, Campos-Rodriguez F, Barbé F (2013) Obstructive sleep apnoea and cardiovascular disease. Lancet Respir Med 1(1):61–72. https://doi.org/10.1016/S2213-2600(12)70051-6CrossRefPubMed

Lévy P, Kohler M, McNicholas WT, Barbé F, McEvoy RD, Somers VK, Lavie L, Pépin JL (2015) Obstructive sleep apnoea syndrome. Nat Rev Dis Primers 1:15015. https://doi.org/10.1038/nrdp.2015.15CrossRefPubMed

McNicholas WT, Bonsigore MR (2007) Sleep apnoea as an independent risk factor for cardiovascular disease: current evidence, basic mechanisms and research priorities. Eur Respir J 29(1):156–178. https://doi.org/10.1183/09031936.00027406CrossRefPubMed

Ioachimescu OC, Janocko NJ, Ciavatta MM, Howard M, Warnock MV (2020) Obstructive lung disease and obstructive sleep apnea (OLDOSA) cohort study: 10–year assessment. J Clin Sleep Med 16(2):267–277. https://doi.org/10.5664/jcsm.8180CrossRefPubMedPubMedCentral

Pedrosa RP, Drager LF, Gonzaga CC, Sousa MG, de Paula LK, Amaro AC, Amodeo C, Bortolotto LA, Krieger EM, Bradley TD, Lorenzi-Filho G (2011) Obstructive sleep apnea: the most common secondary cause of hypertension associated with resistant hypertension. Hypertension 58(5):811–817. https://doi.org/10.1161/HYPERTENSIONAHA.111.179788CrossRefPubMed

Manin G, Pons A, Baltzinger P, Moreau F, Iamandi C, Wilhelm JM, Lenoble P, Kessler L, Kessler R (2015) Obstructive sleep apnoea in people with type 1 diabetes: prevalence and association with micro- and macrovascular complications. Diabet Med 32(1):90–96. https://doi.org/10.1111/dme.12582CrossRefPubMed

Aurora RN, Punjabi NM (2013) Obstructive sleep apnoea and type 2 diabetes mellitus: a bidirectional association. Lancet Respir Med 1(4):329–338. https://doi.org/10.1016/S2213-2600(13)70039-0CrossRefPubMed

10.

Salles C, Terse-Ramos R, Souza-Machado A, Cruz ÁA (2013) Obstructive sleep apnea and asthma. J Bras Pneumol 39(5):604–612. https://doi.org/10.1590/S1806-37132013000500011CrossRefPubMedPubMedCentral

11.

Zhang J, Song Y, Ji Y, Song Y, Cai S, Yu Y, Liu S, Zhang W (2018) Correlation between coronary artery disease and obstructive sleep apnea syndrome and analysis of risk factors. Exp Ther Med 15(6):4771–4776. https://doi.org/10.3892/etm.2018.6070CrossRefPubMedPubMedCentral

12.

Haddad L, Martinho Haddad FL, Bittencourt L, Gregório LC, Tufik S, Abrahão M (2014) Impact of thyroidectomy on the control of obstructive sleep apnea syndrome in patients with large goiters. Sleep Breath 18(4):825–828. https://doi.org/10.1007/s11325-014-0950-8CrossRefPubMed

13.

Lavie L (2003) Obstructive sleep apnoea syndrome-an oxidative stress disorder. Sleep Med Rev 7(1):35–51. https://doi.org/10.1053/smrv.2002.0261CrossRefPubMed

14.

Lavie L, Lavie P (2009) Molecular mechanisms of cardiovascular disease in OSAHS: the oxidative stress link. Eur Respir J 33(6):1467–1484. https://doi.org/10.1183/09031936.00086608CrossRefPubMed

15.

Lavie L (2012) Oxidative stress inflammation and endothelial dysfunction in obstructive sleep apnea. Front Biosci (Elite Ed) 4(4):1391–1403. https://doi.org/10.2741/e469MathSciNetCrossRefPubMed

16.

Lévy P, Pépin JL, Arnaud C, Baguet JP, Dematteis M, Mach F (2009) Obstructive sleep apnea and atherosclerosis. Prog Cardiovasc Dis 51(5):400–410. https://doi.org/10.1016/j.pcad.2008.03.001CrossRefPubMed

17.

Lavie L (2015) Oxidative stress in obstructive sleep apnea and intermittent hypoxia-revisited-the bad ugly and good: implications to the heart and brain. Sleep Med Rev 20:27–45. https://doi.org/10.1016/j.smrv.2014.07.003CrossRefPubMed

18.

Düger M, Seyhan EC, Günlüoğlu MZ, Bolatkale M, Özgül MA, Turan D, Uğur E, Ülfer G (2021) Does ischemia-modified albumin level predict severity of obstructive sleep apnea? Sleep Breath 25(1):65–73. https://doi.org/10.1007/s11325-020-02038-9CrossRefPubMed

19.

Ozben S, Huseyinoglu N, Hanikoglu F, Guvenc TS, Yildirim BZ, Cort A, Ozdem S, Ozben T (2014) Advanced oxidation protein products and ischaemia-modified albumin in obstructive sleep apnea. Eur J Clin Invest 44(11):1045–1052. https://doi.org/10.1111/eci.12338CrossRefPubMed

20.

Baysal E, Taysi S, Aksoy N, Uyar M, Celenk F, Karatas ZA, Tarakcioglu M, Bilinç H, Mumbuç S, Kanlikama M (2012) Serum paraoxonase, arylesterase activity and oxidative status in patients with obstructive sleep apnea syndrome (OSAS). Eur Rev Med Pharmacol Sci 16(6):770–774PubMed

21.

Yarcı Gursoy A, Caglar GS, Demirtas S (2017) Ischemia modified albumin in perinatology. Eur J Obstet Gynecol Reprod Biol 210:182–188. https://doi.org/10.1016/j.ejogrb.2016.12.022CrossRefPubMed

22.

Livaoğlu M, Kerimoğlu S, Karahan SC, Menteşe A, Sozen E, Karaçal N, Topbaş M (2009) Ischemia-modified albumin and flap viability. Eur Surg Res 42(2):87–90. https://doi.org/10.1159/000180115CrossRefPubMed

23.

Serinkan Cinemre FB, Cinemre H, Bahtiyar N, Kahyaoğlu B, Ağaç MT, Shundo H, Sevinç L, Aydemir B (2021) Apelin, Omentin–1, and Vaspin in patients with essential hypertension: association of adipokines with trace elements, inflammatory cytokines, and oxidative damage markers. Ir J Med Sci 190(1):97–106. https://doi.org/10.1007/s11845-020-02272-wCrossRefPubMed

24.

Erem C, Suleyman AK, Civan N, Mentese A, Nuhoglu İ, Uzun A, Ersoz HO, Deger O (2015) Ischemia-modified albümin and malondialdehyde levels in patients with overt and subclinical hyperthyroidism: effects of treatment on oxidative stress. Endocr J 62(6):493–501. https://doi.org/10.1507/endocrj.EJ14-0542CrossRefPubMed

25.

Sbarouni E, Georgiadou P, Voudris V (2011) Ischemia modified albumin changes - review and clinical implications. Clin Chem Lab Med 49(2):177–184. https://doi.org/10.1515/CCLM.2011.037CrossRefPubMed

26.

Ekin S, Yildiz H, Alp HH (2021) NOX4, MDA, IMA and oxidative DNA damage: can these parameters be used to estimate the presence and severity of OSA? Sleep Breath 25(1):529–536. https://doi.org/10.1007/s11325-020-02093-2CrossRefPubMed

27.

Üstündağ Y, Demirci H, Balık R, Erel O, Özaydın F, Kücük B, Ertaş D, Ustunyurt E (2019) Thiol/disulfide homeostasis in pregnant women with obstructive sleep apnea syndrome. J Matern Fetal Neonatal Med 32(7):1136–1141. https://doi.org/10.1080/14767058.2017.1401995CrossRefPubMed

28.

Sunnetcioglu A, Asker S, Alp HH, Gunbatar H (2016) Increased asymmetric dimethylarginine and ischemia-modified albumin levels in obstructive sleep apnea. Respir Care 61(8):1038–1043. https://doi.org/10.4187/respcare.04472CrossRefPubMed

29.

Uygur F, Tanriverdi H, Can M, Ornek T, Erboy F, Altinsoy B, Atalay F, Damar M, Kokturk F, Tor M (2016) The impact of obstructive sleep apnoea and nasal continuous positive airway pressure on circulating ischaemia-modified albumin concentrations. Mediators Inflamm 2016:8907314. https://doi.org/10.1155/2016/8907314CrossRefPubMedPubMedCentral

30.

Sengoren Dikis O, Acat M, Casim H, Haskul I, Neselioglu S, Simsek A, Erel O (2020) The relationship of thiol/disulfide homeostasis in the etiology of patients with obstructive sleep apnea: a case-control study. Aging Male 23(5):679–686. https://doi.org/10.1080/13685538.2019.1573890CrossRefPubMed

31.

Yang LX, Ma SG, Liu H, Xu W (2013) Influence of obstructive sleep apnea on serum butyrylcholinesterase activity and ischemia-modified albumin levels. Clinics (Sao Paulo) 68(7):968–973. https://doi.org/10.6061/clinics/2013(07)13CrossRefPubMed

32.

Dogan D, Ocal N, Aydogan M, Tasci C, Arslan Y, Tapan S, Yetkin S, Bilgic H (2016) Assessment of the role of serum ischemia-modified albumin in obstructive sleep apnea in comparison with interleukin–6. Postgrad Med 128(6):603–608. https://doi.org/10.1080/00325481.2016.1203237CrossRefPubMed

33.

Karamanli H, Kiyici A, Arik B, Efe D, Akgedik R (2016) Influence of obstructive sleep apnea on ischemia-modified albumin levels and carotid intima–media thickness. J Investig Med 64(5):1035–1041. https://doi.org/10.1136/jim-2016-000063CrossRefPubMed

34.

He Y, Chen R, Wang J, Pan W, Sun Y, Han F, Wang Q, Liu C (2016) Neurocognitive impairment is correlated with oxidative stress in patients with moderate-to-severe obstructive sleep apnea hypopnea syndrome. Respir Med 120:25–30. https://doi.org/10.1016/j.rmed.2016.09.009CrossRefPubMed

35.

Xu Q, Du J, Ling X, Lu Y (2017) Evaluation of MIh scoring system in diagnosis of obstructive sleep apnea syndrome. Med Sci Monit 23:4715–4722. https://doi.org/10.12659/msm.904087CrossRefPubMedPubMedCentral

36.

Arısoy A, Ekin S, Sertogullarindan B, Gunbatar H, Sunnetcioglu A, Aksoy N, Sezen H, Asker S, Turan M, Yildiz H (2016) The relationship among oxidative and anti–oxidative parameters and myeloperoxidase in subjects with obstructive sleep apnea syndrome. Respir Care 61(2):200–204. https://doi.org/10.4187/respcare.04277CrossRefPubMed

37.

Bozkurt H, Neyal A, Geyik S, Taysi S, Anarat R, Bulut M, Neyal AM (2015) Investigation of the plasma nitrite levels and oxidant-antioxidant status in obstructive sleep apnea syndrome. Noro Psikiyatr Ars 52(3):221–225. https://doi.org/10.5152/npa.2015.7607CrossRefPubMedPubMedCentral

38.

Monneret D, Tamisier R, Ducros V, Faure P, Halimi S, Baguet JP, Lévy P, Pépin JL, Borel AL (2016) Glucose tolerance and cardiovascular risk biomarkers in non–diabetic non–obese obstructive sleep apnea patients: effects of long-term continuous positive airway pressure. Respir Med 112:119–125. https://doi.org/10.1016/j.rmed.2016.01.015CrossRefPubMed

39.

Katsoulis K, Kontakiotis T, Spanogiannis D, Vlachogiannis E, Kougioulis M, Gerou S, Daskalopoulou E (2011) Total antioxidant status in patients with obstructive sleep apnea without comorbidities: the role of the severity of the disease. Sleep Breath 15(4):861–866. https://doi.org/10.1007/s11325-010-0456-yCrossRefPubMed

40.

Berry RB, Brooks R, Gamaldo C, Harding SM, Lloyd RM, Quan SF, Troester MT, Vaughn BV (2017) AASM scoring manual updates for 2017 (Version 2.4). J Clin Sleep Med 13(5):665–666. https://doi.org/10.5664/jcsm.6576CrossRefPubMedPubMedCentral

41.

Geçkil AA, Kıran TR, Berber NK, Otlu Ö, Erdem M, İn E (2022) Carbonic anhydrase IX as a marker of disease severity in obstructive sleep apnea. Medicina (Kaunas) 58(11):1643. https://doi.org/10.3390/medicina58111643CrossRefPubMed

42.

Erdem M, Karahan SC, Menteşe A, ÖzerYaman S, Demir S (2021) The assessment of oxidative stress biomarkers in different serum and plasma specimens. Erciyes Med J 43(6):541–547. https://doi.org/10.14744/etd.2021.75983CrossRef

43.

West SD, Turnbull C (2018) Obstructive sleep apnoea. Eye (Lond) 32(5):889–903. https://doi.org/10.1038/s41433-017-0006-yCrossRefPubMed

44.

Lee SD, Ju G, Choi JA, Kim JW, Yoon IY (2012) The association of oxidative stress with central obesity in obstructive sleep apnea. Sleep Breath 16(2):511–517. https://doi.org/10.1007/s11325-011-0536-7CrossRefPubMed

45.

Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38(12):1103–1111. https://doi.org/10.1016/j.clinbiochem.2005.08.008CrossRefPubMed

46.

Erel O (2004) A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 37(2):112–119. https://doi.org/10.1016/j.clinbiochem.2003.10.014CrossRefPubMed

Title: The effects of disease severity and comorbidity on oxidative stress biomarkers in obstructive sleep apnea
Authors: Tuğba Raika Kıran
Önder Otlu
Mehmet Erdem
Ayşegül Altıntop Geçkil
Nurcan Kırıcı Berber
Erdal İn
Publication date: 11-07-2023
Publisher: Springer International Publishing
Keywords: Sleep Apnea
Polysomnography
Biomarkers
Published in: Sleep and Breathing / Issue 1/2024
Print ISSN: 1520-9512
Electronic ISSN: 1522-1709
DOI: https://doi.org/10.1007/s11325-023-02870-9

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

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

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2024

Intermittent hypoxia induces myofibroblast differentiation and extracellular matrix production of MRC5s via HIF-1α-TGF-β/Smad pathway

The relationship between sleep problems and sexual dysfunction among pregnant women in Turkey

Poor sleep quality and its associated neurocognitive function in children with obesity with or without obstructive sleep apnea

Longitudinal patterns of patient-reported sleep disturbances after surgery for lung cancer

Evaluation of the relationship between the Mediterranean diet adherence and sleep quality in adults

Effect of mandibular advancement splint therapy on cardiac autonomic function in obstructive sleep apnoea

Keynote webinar | Spotlight on medication adherence

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

At a glance: The STEP trials