Lipoprotein Subfractions Associated with Endothelial Function in Previously Healthy Subjects with Newly Diagnosed Sleep Apnea-A Pilot Study
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
PubMed
36836798
PubMed Central
PMC9962671
DOI
10.3390/life13020441
PII: life13020441
Knihovny.cz E-resources
- Keywords
- lipoprotein subfractions, obstructive sleep apnea, polysomnography,
- Publication type
- Journal Article MeSH
BACKGROUND: Obstructive sleep apnea (OSA) activates several pathophysiological mechanisms which can lead to the development of vascular diseases. Endothelial dysfunction (ED) is an initial step in the development of atherosclerosis. The association between ED and OSA has been described in several studies, even in previously healthy subjects. High-density lipoproteins (HDL) were generally considered to be atheroprotective, and low-density lipoprotein (LDL) to be an atherogenic component of lipoproteins. However, recent findings suggest a pro-atherogenic role of small HDL subfractions (8-10) and LDL subfractions (3-7). This study aimed to evaluate the relationship between endothelial function and lipid subfractions in previously healthy OSA subjects. MATERIAL AND METHODS: We prospectively enrolled 205 subjects with sleep monitoring. Plasma levels of triacylglycerols, total cholesterol, LDL, HDL, and their subfractions were assessed. Endothelial function was determined using peripheral arterial tonometry, and reperfusion hyperemia index (RHI) was assessed. RESULTS: Plasma levels of small and intermediate HDL subfractions have statistically significant pro-atherogenic correlations with endothelial function (p = 0.015 and p = 0.019). In other lipoprotein levels, no other significant correlation was found with RHI. In stepwise multiple linear regression analysis, small HDL (beta = -0.507, p = 0.032) was the only significant contributor in the model predicting RHI. CONCLUSIONS: In our studied sample, a pro-atherogenic role of small HDL subfractions in previously healthy subjects with moderate-to-severe OSA was proven.
Department of Neurology General Hospital 03123 Liptovsky Mikulas Slovakia
Department of Neurology University Hospital Bratislava 85107 Bratislava Slovakia
Department of Pediatric Otorhinolaryngology University Hospital Brno 61300 Brno Czech Republic
Faculty of Medicine Masaryk University 62500 Brno Czech Republic
Institute of Cancer and Genomic Sciences University of Birmingham Birmingham B15 2SQ UK
See more in PubMed
Hankey G.J., Wardlaw J.M., Gorelick P.B., Testai F.D. Hankey’s Clinical Neurology. 2nd ed. CRC Press; Boca Raton, FL, USA: 2014. Hankey’s Clinical Neurology preface; p. 9.
Gottlieb D.J., Punjabi N.M. Diagnosis and Management of Obstructive Sleep Apnea: A Review. JAMA. 2020;323:1389–1400. doi: 10.1001/jama.2020.3514. PubMed DOI
Dempsey J.A., Veasey S.C., Morgan B.J., O’Donnell C.P. Pathophysiology of sleep apnea. Physiol. Rev. 2010;90:47–112. doi: 10.1152/physrev.00043.2008. PubMed DOI PMC
Drager L.F., Polotsky V.Y., O’Donnell C.P., Cravo S.L., Lorenzi-Filho G., Machado B.H. Translational approaches to understanding metabolic dysfunction and cardiovascular consequences of obstructive sleep apnea. Am. J. Physiol. Heart Circ. Physiol. 2015;309:H1101–H1111. doi: 10.1152/ajpheart.00094.2015. PubMed DOI PMC
Liu A., Cardell J., Ariel D., Lamendola C., Abbasi F., Kim S.H., Holmes T.H., Tomasso V., Mojaddidi H., Grove K., et al. Abnormalities of lipoprotein concentrations in obstructive sleep apnea are related to insulin resistance. Sleep. 2015;38:793–799. doi: 10.5665/sleep.4678. PubMed DOI PMC
Hill J.M., Zalos G., Halcox J.P., Schenke W.H., Waclawiw M.A., Quyyumi A.A., Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N. Engl. J. Med. 2003;348:593–600. doi: 10.1056/NEJMoa022287. PubMed DOI
Perticone F., Ceravolo R., Pujia A., Ventura G., Iacopino S., Scozzafava A., Ferraro A., Chello M., Mastroroberto P., Verdecchia P., et al. Prognostic significance of endothelial dysfunction in hypertensive patients. Circulation. 2001;104:191–196. doi: 10.1161/01.CIR.104.2.191. PubMed DOI
Victor V.M., Rocha M., Sola E., Banuls C., Garcia-Malpartida K., Hernandez-Mijares A. Oxidative stress, endothelial dysfunction and atherosclerosis. Curr. Pharm. Des. 2009;15:2988–3002. doi: 10.2174/138161209789058093. PubMed DOI
Flammer A.J., Anderson T., Celermajer D.S., Creager M.A., Deanfield J., Ganz P., Hamburg N.M., Lüscher T.F., Shechter M., Taddei S., et al. The assessment of endothelial function: From research into clinical practice. Circulation. 2012;126:753–767. doi: 10.1161/CIRCULATIONAHA.112.093245. PubMed DOI PMC
Rubinshtein R., Kuvin J.T., Soffler M., Lennon R.J., Lavi S., Nelson R.E., Pumper G.M., Lerman L.O., Lerman A. Assessment of endothelial function by non-invasive peripheral arterial tonometry predicts late cardiovascular adverse events. Eur. Heart J. 2010;31:1142–1148. doi: 10.1093/eurheartj/ehq010. PubMed DOI
Matsuzawa Y., Sugiyama S., Sugamura K., Nozaki T., Ohba K., Konishi M., Matsubara J., Sumida H., Kaikita K., Kojima S., et al. Digital assessment of endothelial function and ischemic heart disease in women. J. Am. Coll. Cardiol. 2010;55:1688–1696. doi: 10.1016/j.jacc.2009.10.073. PubMed DOI
Azuma M., Chihara Y., Yoshimura C., Murase K., Hamada S., Tachikawa R., Matsumoto T., Inouchi M., Tanizawa K., Handa T., et al. Association between endothelial function (assessed on reactive hyperemia peripheral arterial tonometry) and obstructive sleep apnea, visceral fat accumulation, and serum adiponectin. Circ. J. Off. J. Jpn. Circ. Soc. 2015;79:1381–1389. doi: 10.1253/circj.CJ-14-1303. PubMed DOI
Kheirandish-Gozal L., Etzioni T., Bhattacharjee R., Tan H.L., Samiei A., Molero Ramirez H., Abu Eta B., Pillar G. Obstructive sleep apnea in children is associated with severity-dependent deterioration in overnight endothelial function. Sleep Med. 2013;14:526–531. doi: 10.1016/j.sleep.2013.02.010. PubMed DOI
Siarnik P., Carnicka Z., Krizova L., Wagnerova H., Sutovsky S., Klobucnikova K., Kollar B., Turcani P., Sykora M. Predictors of impaired endothelial function in obstructive sleep apnea syndrome. Neuro Endocrinol. Lett. 2014;35:142–148. PubMed
Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation. 2002;106:3143–3421. doi: 10.1161/circ.106.25.3143. PubMed DOI
Gottlieb D.J. Sleep Apnea and Cardiovascular Disease. Curr. Diabetes Rep. 2021;21:64. doi: 10.1007/s11892-021-01426-z. PubMed DOI PMC
Juhász J. Dyslipidemia: Another brick in the wall. A feasible link in the OSA-cardiovascular disease axis. Sleep Breath. Schlaf. Atm. 2014;18:5–6. doi: 10.1007/s11325-013-0852-1. PubMed DOI
Šiarnik P., Klobučníková K., Mucska I., Černá K., Kollár B., Turčáni P. Obstructive sleep apnea and dyslipidemia. Vnitr. Lek. 2018;64:934–938. doi: 10.36290/vnl.2018.130. PubMed DOI
Drager L.F., Jun J., Polotsky V.Y. Obstructive sleep apnea and dyslipidemia: Implications for atherosclerosis. Curr. Opin. Endocrinol. Diabetes Obes. 2010;17:161–165. doi: 10.1097/MED.0b013e3283373624. PubMed DOI PMC
Oravec S., Dostal E., Dukát A., Gavorník P., Kucera M., Gruber K. HDL subfractions analysis: A new laboratory diagnostic assay for patients with cardiovascular diseases and dyslipoproteinemia. Neuro Endocrinol. Lett. 2011;32:502–509. PubMed
Kollar B., Siarnik P., Hluchanova A., Klobucnikova K., Mucska I., Turcani P., Paduchova Z., Katrencikova B., Janubova M., Konarikova K., et al. The impact of sleep apnea syndrome on the altered lipid metabolism and the redox balance. Lipids Health Dis. 2021;20:175. doi: 10.1186/s12944-021-01604-8. PubMed DOI PMC
Berry R.B., Brooks R., Gamaldo C.E., Harding S.M., Marcus C., Vaughn B.V. The AASM manual for the scoring of sleep and associated events. Rules Terminol. Tech. Specif. Darien Ill. Am. Acad. Sleep Med. 2012;176:2012.
Hoefner D.M., Hodel S.D., O’Brien J.F., Branum E.L., Sun D., Meissner I., McConnell J.P. Development of a rapid, quantitative method for LDL subfractionation with use of the Quantimetrix Lipoprint LDL System. Clin. Chem. 2001;47:266–274. doi: 10.1093/clinchem/47.2.266. PubMed DOI
Moerland M., Kales A.J., Schrier L., van Dongen M.G., Bradnock D., Burggraaf J. Evaluation of the EndoPAT as a Tool to Assess Endothelial Function. Int. J. Vasc. Med. 2012;2012:904141. doi: 10.1155/2012/904141. PubMed DOI PMC
Ott S.R., Korostovtseva L., Schmidt M., Horvath T., Brill A.K., Bassetti C.L. Sleep-disordered breathing: Clinical features, pathophysiology and diagnosis. Swiss. Med. Wkly. 2020;147:w14436 . doi: 10.4414/smw.2020.14436. PubMed DOI
Slouka D., Windrichova J., Rezackova H., Houfkova K., Kucera R., Cerna V., Kostlivy T., Topolcan O., Pesta M. The potential of miR-499 plasmatic level as a biomarker of obstructive sleep apnea syndrome. Biomark. Med. 2021;15:1011–1019. doi: 10.2217/bmm-2020-0826. PubMed DOI
Javaheri S., Barbe F., Campos-Rodriguez F., Dempsey J.A., Khayat R., Malhotra A., Martinez-Garcia M.A., Mehra R., Pack A.I., Polotsky V.Y., et al. Sleep Apnea: Types, Mechanisms, and Clinical Cardiovascular Consequences. J. Am. Coll. Cardiol. 2017;69:841–858. doi: 10.1016/j.jacc.2016.11.069. PubMed DOI PMC
Tuleta I., França C.N., Wenzel D., Fleischmann B., Nickenig G., Werner N., Skowasch D. Intermittent Hypoxia Impairs Endothelial Function in Early Preatherosclerosis. Adv. Exp. Med. Biol. 2015;858:1–7 . doi: 10.1007/5584_2015_1114. PubMed DOI
Shamsuzzaman A.S., Gersh B.J., Somers V.K. Obstructive sleep apnea: Implications for cardiac and vascular disease. JAMA. 2003;290:1906–1914. doi: 10.1001/jama.290.14.1906. PubMed DOI
Orrù G., Storari M., Scano A., Piras V., Taibi R., Viscuso D. Obstructive Sleep Apnea, oxidative stress, inflammation and endothelial dysfunction-An overview of predictive laboratory biomarkers. Eur. Rev. Med. Pharm. Sci. 2020;24:6939–6948. PubMed
Stanek A., Brożyna-Tkaczyk K., Myśliński W. Oxidative Stress Markers among Obstructive Sleep Apnea Patients. Oxid. Med. Cell Longev. 2021;2021:9681595 . doi: 10.1155/2021/9681595. PubMed DOI PMC
Trakada G., Lombardi C., Knechtle B. Editorial: The Complex Interaction Between Biological, Metabolic and Neurologic Dysregulation in Obstructive Sleep Apnea. Front. Psychiatry. 2021;12:770930 . doi: 10.3389/fpsyt.2021.770930. PubMed DOI PMC
Bhatt S.P., Guleria R., Kabra S.K. Metabolic alterations and systemic inflammation in overweight/obese children with obstructive sleep apnea. PLoS ONE. 2021;16:e0252353. doi: 10.1371/journal.pone.0252353. PubMed DOI PMC
Lévy P., Pépin J.-L., Arnaud C., Baguet J.-P., Dematteis M., Mach F. Obstructive sleep apnea and atherosclerosis. Prog. Cardiovasc. Dis. 2009;51:400–410. doi: 10.1016/j.pcad.2008.03.001. PubMed DOI
Seiler A., Camilo M., Korostovtseva L., Haynes A.G., Brill A.K., Horvath T., Egger M., Bassetti C.L. Prevalence of sleep-disordered breathing after stroke and TIA: A meta-analysis. Neurology. 2019;92:e648–e654. doi: 10.1212/WNL.0000000000006904. PubMed DOI
Bonetti P.O., Lerman L.O., Lerman A. Endothelial dysfunction: A marker of atherosclerotic risk. Arterioscler. Thromb. Vasc. Biol. 2003;23:168–175. doi: 10.1161/01.ATV.0000051384.43104.FC. PubMed DOI
Gimbrone M.A., Jr., García-Cardeña G. Endothelial Cell Dysfunction and the Pathobiology of Atherosclerosis. Circ. Res. 2016;118:620–636. doi: 10.1161/CIRCRESAHA.115.306301. PubMed DOI PMC
Ip M.S., Tse H.-F., Lam B., Tsang K.W., Lam W.-K. Endothelial function in obstructive sleep apnea and response to treatment. Am. J. Respir. Crit. Care Med. 2004;169:348–353. doi: 10.1164/rccm.200306-767OC. PubMed DOI
Helkin A., Stein J.J., Lin S., Siddiqui S., Maier K.G., Gahtan V. Dyslipidemia Part 1--Review of Lipid Metabolism and Vascular Cell Physiology. Vasc Endovasc. Surg. 2016;50:107–118. doi: 10.1177/1538574416628654. PubMed DOI
Oravec S., Dukat A., Gavornik P., Caprnda M., Kucera M., Ocadlik I. Contribution of the atherogenic lipoprotein profile to the development of arterial hypertension. Bratisl. Lek. Listy. 2011;112:4–7. PubMed
Oravec S., Krivosikova Z., Krivosik M., Gruber K., Gruber M., Dukát A., Gavorník P. Lipoprotein profile in patients who survive a stroke. Neuro Endocrinol. Lett. 2011;32:496–501. PubMed
Oravec S., Gruber K., Dostal E., Mikl J. Hyper-betalipoproteinemia LDL 1,2: A newly identified nonatherogenic hypercholesterolemia in a group of hypercholesterolemic subjects. Neuro Endocrinol. Lett. 2011;32:322–327. PubMed
Šiarnik P., Čarnická Z., Krivošíková Z., Klobučníková K., Žitňanová I., Kollár B., Sýkora M., Turčáni P. Association of lipoprotein subfractions with endothelial function and arterial stiffness in acute ischemic stroke. Scand. J. Clin. Lab. Invest. 2017;77:36–39. doi: 10.1080/00365513.2016.1243257. PubMed DOI
Sopkova Z., Berneis K., Rizzo M., Spinas G.A., Dorkova Z., Tisko R., Tkacova R. Size and subclasses of low-density lipoproteins in patients with obstructive sleep apnea. Angiology. 2012;63:617–621. doi: 10.1177/0003319711433811. PubMed DOI
Meszaros M., Bikov A. Obstructive Sleep Apnoea and Lipid Metabolism: The Summary of Evidence and Future Perspectives in the Pathophysiology of OSA-Associated Dyslipidaemia. Biomedicines. 2022;10:2754. doi: 10.3390/biomedicines10112754. PubMed DOI PMC
Rizk S.M., Sabri N.A. Evaluation of clinical activity and safety of Daflon 500 mg in type 2 diabetic female patients. Saudi Pharm. J. SPJ Off. Publ. Saudi Pharm. Soc. 2009;17:199–207. doi: 10.1016/j.jsps.2009.08.008. PubMed DOI PMC
Ateya A.M., Sabri N.A., El Hakim I., Shaheen S.M. Effect of Omega-3 Fatty Acids on Serum Lipid Profile and Oxidative Stress in Pediatric Patients on Regular Hemodialysis: A Randomized Placebo-Controlled Study. J. Ren. Nutr. Off. J. Counc. Ren. Nutr. Natl. Kidney Found. 2017;27:169–174. doi: 10.1053/j.jrn.2016.11.005. PubMed DOI
Ateya A.M., El Hakim I., Shahin S.M., El Borolossy R., Kreutz R., Sabri N.A. Effects of Ramipril on Biomarkers of Endothelial Dysfunction and Inflammation in Hypertensive Children on Maintenance Hemodialysis: The SEARCH Randomized Placebo-Controlled Trial. Hypertension. 2022;79:1856–1865. doi: 10.1161/HYPERTENSIONAHA.122.19312. PubMed DOI
Alshahawey M., Shaheen S.M., Elsaid T., Sabri N.A. Effect of febuxostat on oxidative stress in hemodialysis patients with endothelial dysfunction: A randomized, placebo-controlled, double-blinded study. Int. Urol. Nephrol. 2019;51:1649–1657. doi: 10.1007/s11255-019-02243-w. PubMed DOI
Alshahawey M., Shahin S.M., Elsaid T.W., Sabri N.A. Effect of Febuxostat on the Endothelial Dysfunction in Hemodialysis Patients: A Randomized, Placebo-Controlled, Double-Blinded Study. Am. J. Nephrol. 2017;45:452–459. doi: 10.1159/000471893. PubMed DOI
Alshahawey M., El Borolossy R., El Wakeel L., Elsaid T., Sabri N.A. The impact of cholecalciferol on markers of vascular calcification in hemodialysis patients: A randomized placebo controlled study. Nutr. Metab. Cardiovasc. Dis. NMCD. 2021;31:626–633. doi: 10.1016/j.numecd.2020.09.014. PubMed DOI
Dutheil F., Walther G., Chapier R., Mnatzaganian G., Lesourd B., Naughton G., Verney J., Fogli A., Sapin V., Duclos M., et al. Atherogenic subfractions of lipoproteins in the treatment of metabolic syndrome by physical activity and diet-the RESOLVE trial. Lipids Health Dis. 2014;13:112. doi: 10.1186/1476-511X-13-112. PubMed DOI PMC
Bajer B., Rádiková Ž., Havranová A., Žitňanová I., Vlček M., Imrich R., Sabaka P., Bendžala M., Penesová A. Effect of 8-weeks intensive lifestyle intervention on LDL and HDL subfractions. Obes. Res. Clin. Pract. 2019;13:586–593. doi: 10.1016/j.orcp.2019.10.010. PubMed DOI
Habanova M., Holovicova M., Scepankova H., Lorkova M., Gazo J., Gazarova M., Pinto C.A., Saraiva J.A., Estevinho L.M. Modulation of Lipid Profile and Lipoprotein Subfractions in Overweight/Obese Women at Risk of Cardiovascular Diseases through the Consumption of Apple/Berry Juice. Antioxidants. 2022;11:2239. doi: 10.3390/antiox11112239. PubMed DOI PMC
Xu H., Yi H., Guan J., Yin S. Effect of continuous positive airway pressure on lipid profile in patients with obstructive sleep apnea syndrome: A meta-analysis of randomized controlled trials. Atherosclerosis. 2014;234:446–453. doi: 10.1016/j.atherosclerosis.2014.03.034. PubMed DOI