Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2017

Open Access 01-12-2017 | Original investigation

Association between obstructive sleep apnea severity and endothelial dysfunction in patients with type 2 diabetes

Authors: Vanessa Bironneau, François Goupil, Pierre Henri Ducluzeau, Marc Le Vaillant, Pierre Abraham, Samir Henni, Séverine Dubois, Audrey Paris, Pascaline Priou, Nicole Meslier, Claire Sanguin, Wojciech Trzépizur, Ramaroson Andriantsitohaina, Maria Carmen Martinez, Frédéric Gagnadoux

Published in: Cardiovascular Diabetology | Issue 1/2017

Login to get access

Abstract

Background

Obstructive sleep apnea (OSA) and type 2 diabetes (T2D) are associated with endothelial dysfunction a main predictor of late cardiovascular (CV) events. Despite the high prevalence of OSA in patients with T2D, the impact of OSA severity on endothelial function has not been clearly elucidated. The aim of this cross-sectional study was to determine whether increasing OSA severity is associated with poorer endothelial function in patients with T2D.

Methods

140 patients with T2D and no overt CV disease underwent polysomnography, peripheral arterial tonometry, clinic blood pressure (BP) measurement, biological assessment for CV risk factors, daytime sleepiness and health related quality of life (HRQL) questionnaires. The following commonly used cut-offs for apnea-hypopnea index (AHI) were used to define 3 categories of disease severity: AHI < 15 (no OSA or mild OSA), 15 ≤ AHI < 30 (moderate OSA), and AHI ≥ 30 (severe OSA). The primary outcome was the reactive hyperemia index (RHI), a validated assessment of endothelial function.

Results

21.4% of patients had moderate OSA and 47.6% had severe OSA. Increasing OSA severity and nocturnal hypoxemia were not associated with a significant decrease in RHI. Endothelial dysfunction (RHI < 1.67) was found in 47.1, 44.4 and 39.2% of patients with no OSA or mild OSA, moderate OSA and severe OSA, respectively (p = 0.76). After adjustment for confounders including body mass index, increasing OSA severity was associated with higher systolic BP (p = 0.03), lower circulating levels of adiponectin (p = 0.0009), higher levels of sP-selectin (p = 0.03), lower scores in 3 domains of HRQL including energy/vitality (p = 0.02), role functioning (p = 0.01), and social functioning (p = 0.04).

Conclusions

Moderate to severe OSA is very common but has no impact on digital micro-vascular endothelial function in patients with T2D.
Literature
1.
go back to reference Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348(7):593–600.CrossRefPubMed Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348(7):593–600.CrossRefPubMed
2.
go back to reference 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(2):191–6.CrossRefPubMed 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(2):191–6.CrossRefPubMed
3.
go back to reference Flammer AJ, Anderson T, Celermajer DS, Creager MA, Deanfield J, Ganz P, Hamburg NM, Luscher TF, Shechter M, Taddei S, et al. The assessment of endothelial function: from research into clinical practice. Circulation. 2012;126(6):753–67.CrossRefPubMedPubMedCentral Flammer AJ, Anderson T, Celermajer DS, Creager MA, Deanfield J, Ganz P, Hamburg NM, Luscher TF, Shechter M, Taddei S, et al. The assessment of endothelial function: from research into clinical practice. Circulation. 2012;126(6):753–67.CrossRefPubMedPubMedCentral
4.
go back to reference Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Kuvin JT, Lerman A. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol. 2004;44(11):2137–41.CrossRefPubMed Bonetti PO, Pumper GM, Higano ST, Holmes DR Jr, Kuvin JT, Lerman A. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol. 2004;44(11):2137–41.CrossRefPubMed
5.
go back to reference Akiyama E, Sugiyama S, Matsuzawa Y, Konishi M, Suzuki H, Nozaki T, Ohba K, Matsubara J, Maeda H, Horibata Y, et al. Incremental prognostic significance of peripheral endothelial dysfunction in patients with heart failure with normal left ventricular ejection fraction. J Am Coll Cardiol. 2012;60(18):1778–86.CrossRefPubMed Akiyama E, Sugiyama S, Matsuzawa Y, Konishi M, Suzuki H, Nozaki T, Ohba K, Matsubara J, Maeda H, Horibata Y, et al. Incremental prognostic significance of peripheral endothelial dysfunction in patients with heart failure with normal left ventricular ejection fraction. J Am Coll Cardiol. 2012;60(18):1778–86.CrossRefPubMed
6.
go back to reference Rubinshtein R, Kuvin JT, Soffler M, Lennon RJ, Lavi S, Nelson RE, Pumper GM, Lerman LO, Lerman A. Assessment of endothelial function by non-invasive peripheral arterial tonometry predicts late cardiovascular adverse events. Eur Heart J. 2010;31(9):1142–8.CrossRefPubMed Rubinshtein R, Kuvin JT, Soffler M, Lennon RJ, Lavi S, Nelson RE, Pumper GM, Lerman LO, Lerman A. Assessment of endothelial function by non-invasive peripheral arterial tonometry predicts late cardiovascular adverse events. Eur Heart J. 2010;31(9):1142–8.CrossRefPubMed
7.
go back to reference 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(16):1688–96.CrossRefPubMed 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(16):1688–96.CrossRefPubMed
8.
go back to reference Tuttolomondo A, Casuccio A, Della Corte V, Maida C, Pecoraro R, Di Raimondo D, Vassallo V, Simonetta I, Arnao V, Pinto A. Endothelial function and arterial stiffness indexes in subjects with acute ischemic stroke: relationship with TOAST subtype. Atherosclerosis. 2017;256:94–9.CrossRefPubMed Tuttolomondo A, Casuccio A, Della Corte V, Maida C, Pecoraro R, Di Raimondo D, Vassallo V, Simonetta I, Arnao V, Pinto A. Endothelial function and arterial stiffness indexes in subjects with acute ischemic stroke: relationship with TOAST subtype. Atherosclerosis. 2017;256:94–9.CrossRefPubMed
9.
go back to reference Tuttolomondo A, Pecoraro R, Di Raimondo D, Di Sciacca R, Canino B, Arnao V, Butta C, Della Corte V, Maida C, Licata G, et al. Immune-inflammatory markers and arterial stiffness indexes in subjects with acute ischemic stroke with and without metabolic syndrome. Diabetol Metab Syndr. 2014;6(1):28.CrossRefPubMedPubMedCentral Tuttolomondo A, Pecoraro R, Di Raimondo D, Di Sciacca R, Canino B, Arnao V, Butta C, Della Corte V, Maida C, Licata G, et al. Immune-inflammatory markers and arterial stiffness indexes in subjects with acute ischemic stroke with and without metabolic syndrome. Diabetol Metab Syndr. 2014;6(1):28.CrossRefPubMedPubMedCentral
10.
go back to reference Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P. Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol. 2006;101(2):545–8.CrossRefPubMed Nohria A, Gerhard-Herman M, Creager MA, Hurley S, Mitra D, Ganz P. Role of nitric oxide in the regulation of digital pulse volume amplitude in humans. J Appl Physiol. 2006;101(2):545–8.CrossRefPubMed
11.
go back to reference Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, Karas RH, Udelson JE. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J. 2003;146(1):168–74.CrossRefPubMed Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, Karas RH, Udelson JE. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J. 2003;146(1):168–74.CrossRefPubMed
12.
go back to reference Dhindsa M, Sommerlad SM, DeVan AE, Barnes JN, Sugawara J, Ley O, Tanaka H. Interrelationships among noninvasive measures of postischemic macro- and microvascular reactivity. J Appl Physiol. 2008;105(2):427–32.CrossRefPubMedPubMedCentral Dhindsa M, Sommerlad SM, DeVan AE, Barnes JN, Sugawara J, Ley O, Tanaka H. Interrelationships among noninvasive measures of postischemic macro- and microvascular reactivity. J Appl Physiol. 2008;105(2):427–32.CrossRefPubMedPubMedCentral
13.
go back to reference Hamburg NM, Palmisano J, Larson MG, Sullivan LM, Lehman BT, Vasan RS, Levy D, Mitchell GF, Vita JA, Benjamin EJ. Relation of brachial and digital measures of vascular function in the community: the Framingham heart study. Hypertension. 2011;57(3):390–6.CrossRefPubMedPubMedCentral Hamburg NM, Palmisano J, Larson MG, Sullivan LM, Lehman BT, Vasan RS, Levy D, Mitchell GF, Vita JA, Benjamin EJ. Relation of brachial and digital measures of vascular function in the community: the Framingham heart study. Hypertension. 2011;57(3):390–6.CrossRefPubMedPubMedCentral
14.
go back to reference Gall MA, Rossing P, Skott P, Damsbo P, Vaag A, Bech K, Dejgaard A, Lauritzen M, Lauritzen E, Hougaard P, et al. Prevalence of micro- and macroalbuminuria, arterial hypertension, retinopathy and large vessel disease in European type 2 (non-insulin-dependent) diabetic patients. Diabetologia. 1991;34(9):655–61.CrossRefPubMed Gall MA, Rossing P, Skott P, Damsbo P, Vaag A, Bech K, Dejgaard A, Lauritzen M, Lauritzen E, Hougaard P, et al. Prevalence of micro- and macroalbuminuria, arterial hypertension, retinopathy and large vessel disease in European type 2 (non-insulin-dependent) diabetic patients. Diabetologia. 1991;34(9):655–61.CrossRefPubMed
15.
go back to reference Rafnsson A, Bohm F, Settergren M, Gonon A, Brismar K, Pernow J. The endothelin receptor antagonist bosentan improves peripheral endothelial function in patients with type 2 diabetes mellitus and microalbuminuria: a randomised trial. Diabetologia. 2012;55(3):600–7.CrossRefPubMed Rafnsson A, Bohm F, Settergren M, Gonon A, Brismar K, Pernow J. The endothelin receptor antagonist bosentan improves peripheral endothelial function in patients with type 2 diabetes mellitus and microalbuminuria: a randomised trial. Diabetologia. 2012;55(3):600–7.CrossRefPubMed
16.
go back to reference Creager MA, Luscher TF, Cosentino F, Beckman JA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Circulation. 2003;108(12):1527–32.CrossRefPubMed Creager MA, Luscher TF, Cosentino F, Beckman JA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Circulation. 2003;108(12):1527–32.CrossRefPubMed
17.
go back to reference Tooke JE, Hannemann MM. Adverse endothelial function and the insulin resistance syndrome. J Intern Med. 2000;247(4):425–31.CrossRefPubMed Tooke JE, Hannemann MM. Adverse endothelial function and the insulin resistance syndrome. J Intern Med. 2000;247(4):425–31.CrossRefPubMed
18.
go back to reference Gargiulo P, Marciano C, Savarese G, D’Amore C, Paolillo S, Esposito G, Santomauro M, Marsico F, Ruggiero D, Scala O, et al. Endothelial dysfunction in type 2 diabetic patients with normal coronary arteries: a digital reactive hyperemia study. Int J Cardiol. 2013;165(1):67–71.CrossRefPubMed Gargiulo P, Marciano C, Savarese G, D’Amore C, Paolillo S, Esposito G, Santomauro M, Marsico F, Ruggiero D, Scala O, et al. Endothelial dysfunction in type 2 diabetic patients with normal coronary arteries: a digital reactive hyperemia study. Int J Cardiol. 2013;165(1):67–71.CrossRefPubMed
19.
go back to reference Jenkins DJ, Kendall CW, Vuksan V, Faulkner D, Augustin LS, Mitchell S, Ireland C, Srichaikul K, Mirrahimi A, Chiavaroli L, et al. Effect of lowering the glycemic load with canola oil on glycemic control and cardiovascular risk factors: a randomized controlled trial. Diabetes Care. 2014;37(7):1806–14.CrossRefPubMed Jenkins DJ, Kendall CW, Vuksan V, Faulkner D, Augustin LS, Mitchell S, Ireland C, Srichaikul K, Mirrahimi A, Chiavaroli L, et al. Effect of lowering the glycemic load with canola oil on glycemic control and cardiovascular risk factors: a randomized controlled trial. Diabetes Care. 2014;37(7):1806–14.CrossRefPubMed
20.
go back to reference Kwak JH, Paik JK, Kim HI, Kim OY, Shin DY, Kim HJ, Lee JH, Lee JH. Dietary treatment with rice containing resistant starch improves markers of endothelial function with reduction of postprandial blood glucose and oxidative stress in patients with prediabetes or newly diagnosed type 2 diabetes. Atherosclerosis. 2012;224(2):457–64.CrossRefPubMed Kwak JH, Paik JK, Kim HI, Kim OY, Shin DY, Kim HJ, Lee JH, Lee JH. Dietary treatment with rice containing resistant starch improves markers of endothelial function with reduction of postprandial blood glucose and oxidative stress in patients with prediabetes or newly diagnosed type 2 diabetes. Atherosclerosis. 2012;224(2):457–64.CrossRefPubMed
21.
go back to reference Sagara M, Suzuki K, Aoki C, Tanaka S, Taguchi I, Inoue T, Aso Y. Impact of teneligliptin on oxidative stress and endothelial function in type 2 diabetes patients with chronic kidney disease: a case-control study. Cardiovasc Diabetol. 2016;15:76.CrossRefPubMedPubMedCentral Sagara M, Suzuki K, Aoki C, Tanaka S, Taguchi I, Inoue T, Aso Y. Impact of teneligliptin on oxidative stress and endothelial function in type 2 diabetes patients with chronic kidney disease: a case-control study. Cardiovasc Diabetol. 2016;15:76.CrossRefPubMedPubMedCentral
22.
go back to reference Matsubara J, Sugiyama S, Akiyama E, Iwashita S, Kurokawa H, Ohba K, Maeda H, Fujisue K, Yamamoto E, Kaikita K, et al. Dipeptidyl peptidase-4 inhibitor, sitagliptin, improves endothelial dysfunction in association with its anti-inflammatory effects in patients with coronary artery disease and uncontrolled diabetes. Circ J. 2013;77(5):1337–44.CrossRefPubMed Matsubara J, Sugiyama S, Akiyama E, Iwashita S, Kurokawa H, Ohba K, Maeda H, Fujisue K, Yamamoto E, Kaikita K, et al. Dipeptidyl peptidase-4 inhibitor, sitagliptin, improves endothelial dysfunction in association with its anti-inflammatory effects in patients with coronary artery disease and uncontrolled diabetes. Circ J. 2013;77(5):1337–44.CrossRefPubMed
23.
go back to reference Tuttolomondo A, Casuccio A, Guercio G, Maida C, Del Cuore A, Di Raimondo D, Simonetta I, Di Bona D, Pecoraro R, Della Corte V, et al. Arterial stiffness, endothelial and cognitive function in subjects with type 2 diabetes in accordance with absence or presence of diabetic foot syndrome. Cardiovasc Diabetol. 2017;16(1):2.CrossRefPubMedPubMedCentral Tuttolomondo A, Casuccio A, Guercio G, Maida C, Del Cuore A, Di Raimondo D, Simonetta I, Di Bona D, Pecoraro R, Della Corte V, et al. Arterial stiffness, endothelial and cognitive function in subjects with type 2 diabetes in accordance with absence or presence of diabetic foot syndrome. Cardiovasc Diabetol. 2017;16(1):2.CrossRefPubMedPubMedCentral
24.
go back to reference Jelic S, Lederer DJ, Adams T, Padeletti M, Colombo PC, Factor PH, Le Jemtel TH. Vascular inflammation in obesity and sleep apnea. Circulation. 2010;121(8):1014–21.CrossRefPubMedPubMedCentral Jelic S, Lederer DJ, Adams T, Padeletti M, Colombo PC, Factor PH, Le Jemtel TH. Vascular inflammation in obesity and sleep apnea. Circulation. 2010;121(8):1014–21.CrossRefPubMedPubMedCentral
25.
go back to reference Toraldo DM, De Benedetto M, Scoditti E, De Nuccio F. Obstructive sleep apnea syndrome: coagulation anomalies and treatment with continuous positive airway pressure. Sleep Breath. 2016;20(2):457–65.CrossRefPubMed Toraldo DM, De Benedetto M, Scoditti E, De Nuccio F. Obstructive sleep apnea syndrome: coagulation anomalies and treatment with continuous positive airway pressure. Sleep Breath. 2016;20(2):457–65.CrossRefPubMed
26.
go back to reference Arias MA, Garcia-Rio F, Alonso-Fernandez A, Hernanz A, Hidalgo R, Martinez-Mateo V, Bartolome S, Rodriguez-Padial L. CPAP decreases plasma levels of soluble tumour necrosis factor-alpha receptor 1 in obstructive sleep apnoea. Eur Respir J. 2008;32(4):1009–15.CrossRefPubMed Arias MA, Garcia-Rio F, Alonso-Fernandez A, Hernanz A, Hidalgo R, Martinez-Mateo V, Bartolome S, Rodriguez-Padial L. CPAP decreases plasma levels of soluble tumour necrosis factor-alpha receptor 1 in obstructive sleep apnoea. Eur Respir J. 2008;32(4):1009–15.CrossRefPubMed
27.
go back to reference Alonso-Fernandez A, Garcia-Rio F, Arias MA, Hernanz A, de la Pena M, Pierola J, Barcelo A, Lopez-Collazo E, Agusti A. Effects of CPAP on oxidative stress and nitrate efficiency in sleep apnoea: a randomised trial. Thorax. 2009;64(7):581–6.CrossRefPubMed Alonso-Fernandez A, Garcia-Rio F, Arias MA, Hernanz A, de la Pena M, Pierola J, Barcelo A, Lopez-Collazo E, Agusti A. Effects of CPAP on oxidative stress and nitrate efficiency in sleep apnoea: a randomised trial. Thorax. 2009;64(7):581–6.CrossRefPubMed
28.
go back to reference Sanchez-de-la-Torre M, Campos-Rodriguez F, Barbe F. Obstructive sleep apnoea and cardiovascular disease. Lancet Respir Med. 2013;1(1):61–72.CrossRefPubMed Sanchez-de-la-Torre M, Campos-Rodriguez F, Barbe F. Obstructive sleep apnoea and cardiovascular disease. Lancet Respir Med. 2013;1(1):61–72.CrossRefPubMed
29.
go back to reference 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. 2015;79(6):1381–9.CrossRefPubMed 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. 2015;79(6):1381–9.CrossRefPubMed
30.
go back to reference Itzhaki S, Lavie L, Pillar G, Tal G, Lavie P. Endothelial dysfunction in obstructive sleep apnea measured by peripheral arterial tone response in the finger to reactive hyperemia. Sleep. 2005;28(5):594–600.PubMed Itzhaki S, Lavie L, Pillar G, Tal G, Lavie P. Endothelial dysfunction in obstructive sleep apnea measured by peripheral arterial tone response in the finger to reactive hyperemia. Sleep. 2005;28(5):594–600.PubMed
31.
go back to reference Kheirandish-Gozal L, Etzioni T, Bhattacharjee R, Tan HL, 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(6):526–31.CrossRefPubMed Kheirandish-Gozal L, Etzioni T, Bhattacharjee R, Tan HL, 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(6):526–31.CrossRefPubMed
32.
go back to reference Randby A, Namtvedt SK, Hrubos-Strom H, Einvik G, Somers VK, Omland T. Sex-dependent impact of OSA on digital vascular function. Chest. 2013;144(3):915–22.CrossRefPubMed Randby A, Namtvedt SK, Hrubos-Strom H, Einvik G, Somers VK, Omland T. Sex-dependent impact of OSA on digital vascular function. Chest. 2013;144(3):915–22.CrossRefPubMed
33.
go back to reference Seif F, Patel SR, Walia H, Rueschman M, Bhatt DL, Gottlieb DJ, Lewis EF, Patil SP, Punjabi NM, Babineau DC, et al. Association between obstructive sleep apnea severity and endothelial dysfunction in an increased background of cardiovascular burden. J Sleep Res. 2013;22(4):443–51.CrossRefPubMedPubMedCentral Seif F, Patel SR, Walia H, Rueschman M, Bhatt DL, Gottlieb DJ, Lewis EF, Patil SP, Punjabi NM, Babineau DC, et al. Association between obstructive sleep apnea severity and endothelial dysfunction in an increased background of cardiovascular burden. J Sleep Res. 2013;22(4):443–51.CrossRefPubMedPubMedCentral
34.
go back to reference Olafiranye O, Kip KE, Rhinehart Z, Mulukutla SR, Aiyer A, Strollo PJ, Reis SE. Impact of race and obesity on arterial endothelial dysfunction associated with sleep apnea: results from the Heart SCORE study. Int J Cardiol. 2015;201:476–8.CrossRefPubMed Olafiranye O, Kip KE, Rhinehart Z, Mulukutla SR, Aiyer A, Strollo PJ, Reis SE. Impact of race and obesity on arterial endothelial dysfunction associated with sleep apnea: results from the Heart SCORE study. Int J Cardiol. 2015;201:476–8.CrossRefPubMed
35.
go back to reference Trzepizur W, Martinez MC, Priou P, Andriantsitohaina R, Gagnadoux F. Microparticles and vascular dysfunction in obstructive sleep apnoea. Eur Respir J. 2014;44(1):207–16.CrossRefPubMed Trzepizur W, Martinez MC, Priou P, Andriantsitohaina R, Gagnadoux F. Microparticles and vascular dysfunction in obstructive sleep apnoea. Eur Respir J. 2014;44(1):207–16.CrossRefPubMed
36.
go back to reference Agouni A, Andriantsitohaina R, Martinez MC. Microparticles as biomarkers of vascular dysfunction in metabolic syndrome and its individual components. Curr Vasc Pharmacol. 2014;12(3):483–92.CrossRefPubMed Agouni A, Andriantsitohaina R, Martinez MC. Microparticles as biomarkers of vascular dysfunction in metabolic syndrome and its individual components. Curr Vasc Pharmacol. 2014;12(3):483–92.CrossRefPubMed
37.
go back to reference Torres G, Sanchez-de-la-Torre M, Barbe F. Relationship between OSA and hypertension. Chest. 2015;148(3):824–32.CrossRefPubMed Torres G, Sanchez-de-la-Torre M, Barbe F. Relationship between OSA and hypertension. Chest. 2015;148(3):824–32.CrossRefPubMed
38.
go back to reference 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. 2010;181(5):507–13.CrossRefPubMed 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. 2010;181(5):507–13.CrossRefPubMed
39.
go back to reference Foster GD, Sanders MH, Millman R, Zammit G, Borradaile KE, Newman AB, Wadden TA, Kelley D, Wing RR, Sunyer FX, et al. Obstructive sleep apnea among obese patients with type 2 diabetes. Diabetes Care. 2009;32(6):1017–9.CrossRefPubMedPubMedCentral Foster GD, Sanders MH, Millman R, Zammit G, Borradaile KE, Newman AB, Wadden TA, Kelley D, Wing RR, Sunyer FX, et al. Obstructive sleep apnea among obese patients with type 2 diabetes. Diabetes Care. 2009;32(6):1017–9.CrossRefPubMedPubMedCentral
40.
go back to reference Drager LF, Bortolotto LA, Maki-Nunes C, Trombetta IC, Alves MJ, Fraga RF, Negrao CE, Krieger EM, Lorenzi-Filho G. The incremental role of obstructive sleep apnoea on markers of atherosclerosis in patients with metabolic syndrome. Atherosclerosis. 2010;208(2):490–5.CrossRefPubMed Drager LF, Bortolotto LA, Maki-Nunes C, Trombetta IC, Alves MJ, Fraga RF, Negrao CE, Krieger EM, Lorenzi-Filho G. The incremental role of obstructive sleep apnoea on markers of atherosclerosis in patients with metabolic syndrome. Atherosclerosis. 2010;208(2):490–5.CrossRefPubMed
41.
go back to reference Drager LF, Bortolotto LA, Krieger EM, Lorenzi-Filho G. Additive effects of obstructive sleep apnea and hypertension on early markers of carotid atherosclerosis. Hypertension. 2009;53(1):64–9.CrossRefPubMed Drager LF, Bortolotto LA, Krieger EM, Lorenzi-Filho G. Additive effects of obstructive sleep apnea and hypertension on early markers of carotid atherosclerosis. Hypertension. 2009;53(1):64–9.CrossRefPubMed
42.
go back to reference Banerjee D, Leong WB, Arora T, Nolen M, Punamiya V, Grunstein R, Taheri S. The potential association between obstructive sleep apnea and diabetic retinopathy in severe obesity-the role of hypoxemia. PLoS ONE. 2013;8(11):e79521.CrossRefPubMedPubMedCentral Banerjee D, Leong WB, Arora T, Nolen M, Punamiya V, Grunstein R, Taheri S. The potential association between obstructive sleep apnea and diabetic retinopathy in severe obesity-the role of hypoxemia. PLoS ONE. 2013;8(11):e79521.CrossRefPubMedPubMedCentral
43.
go back to reference Tahrani AA, Ali A, Raymond NT, Begum S, Dubb K, Altaf QA, Piya MK, Barnett AH, Stevens MJ. Obstructive sleep apnea and diabetic nephropathy: a cohort study. Diabetes Care. 2013;36(11):3718–25.CrossRefPubMedPubMedCentral Tahrani AA, Ali A, Raymond NT, Begum S, Dubb K, Altaf QA, Piya MK, Barnett AH, Stevens MJ. Obstructive sleep apnea and diabetic nephropathy: a cohort study. Diabetes Care. 2013;36(11):3718–25.CrossRefPubMedPubMedCentral
44.
go back to reference Tahrani AA, Ali A, Raymond NT, Begum S, Dubb K, Mughal S, Jose B, Piya MK, Barnett AH, Stevens MJ. Obstructive sleep apnea and diabetic neuropathy: a novel association in patients with type 2 diabetes. Am J Respir Crit Care Med. 2012;186(5):434–41.CrossRefPubMedPubMedCentral Tahrani AA, Ali A, Raymond NT, Begum S, Dubb K, Mughal S, Jose B, Piya MK, Barnett AH, Stevens MJ. Obstructive sleep apnea and diabetic neuropathy: a novel association in patients with type 2 diabetes. Am J Respir Crit Care Med. 2012;186(5):434–41.CrossRefPubMedPubMedCentral
45.
go back to reference Greco C, Spallone V. Obstructive sleep apnoea syndrome and diabetes. Fortuitous Association or Interaction? Curr Diabetes Rev. 2015;12(2):129–55.CrossRefPubMed Greco C, Spallone V. Obstructive sleep apnoea syndrome and diabetes. Fortuitous Association or Interaction? Curr Diabetes Rev. 2015;12(2):129–55.CrossRefPubMed
46.
go back to reference Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, et al. 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. 2012;8(5):597–619.PubMedPubMedCentral Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, et al. 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. 2012;8(5):597–619.PubMedPubMedCentral
47.
go back to reference Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14(6):540–5.CrossRefPubMed Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14(6):540–5.CrossRefPubMed
48.
go back to reference Perneger TV, Leplege A, Etter JF, Rougemont A. Validation of a French-language version of the MOS 36-Item Short Form Health Survey (SF-36) in young healthy adults. J Clin Epidemiol. 1995;48(8):1051–60.CrossRefPubMed Perneger TV, Leplege A, Etter JF, Rougemont A. Validation of a French-language version of the MOS 36-Item Short Form Health Survey (SF-36) in young healthy adults. J Clin Epidemiol. 1995;48(8):1051–60.CrossRefPubMed
49.
go back to reference McNicholas WT, Bonsignore MR, Levy P, Ryan S. Mild obstructive sleep apnoea: clinical relevance and approaches to management. Lancet Respir Med. 2016;4(10):826–34.CrossRefPubMed McNicholas WT, Bonsignore MR, Levy P, Ryan S. Mild obstructive sleep apnoea: clinical relevance and approaches to management. Lancet Respir Med. 2016;4(10):826–34.CrossRefPubMed
50.
go back to reference Sawatari H, Chishaki A, Nishizaka M, Tokunou T, Adachi S, Yoshimura C, Ohkusa T, Ando S. Cumulative hypoxemia during sleep predicts vascular endothelial dysfunction in patients with sleep-disordered breathing. Am J Hypertens. 2016;29(4):458–63.CrossRefPubMed Sawatari H, Chishaki A, Nishizaka M, Tokunou T, Adachi S, Yoshimura C, Ohkusa T, Ando S. Cumulative hypoxemia during sleep predicts vascular endothelial dysfunction in patients with sleep-disordered breathing. Am J Hypertens. 2016;29(4):458–63.CrossRefPubMed
51.
go back to reference Duce B, Milosavljevic J, Hukins C. The 2012 AASM respiratory event criteria increase the incidence of hypopneas in an adult sleep Center population. J Clin Sleep Med. 2015;11(12):1425–31.CrossRefPubMedPubMedCentral Duce B, Milosavljevic J, Hukins C. The 2012 AASM respiratory event criteria increase the incidence of hypopneas in an adult sleep Center population. J Clin Sleep Med. 2015;11(12):1425–31.CrossRefPubMedPubMedCentral
52.
go back to reference Escourrou P, Grote L, Penzel T, McNicholas WT, Verbraecken J, Tkacova R, Riha RL, Hedner J, Group ES. The diagnostic method has a strong influence on classification of obstructive sleep apnea. J Sleep Res. 2015;24(6):730–8.CrossRefPubMed Escourrou P, Grote L, Penzel T, McNicholas WT, Verbraecken J, Tkacova R, Riha RL, Hedner J, Group ES. The diagnostic method has a strong influence on classification of obstructive sleep apnea. J Sleep Res. 2015;24(6):730–8.CrossRefPubMed
53.
go back to reference Yim-Yeh S, Rahangdale S, Nguyen AT, Stevenson KE, Novack V, Veves A, Malhotra A. Vascular dysfunction in obstructive sleep apnea and type 2 diabetes mellitus. Obesity (Silver Spring). 2011;19(1):17–22.CrossRef Yim-Yeh S, Rahangdale S, Nguyen AT, Stevenson KE, Novack V, Veves A, Malhotra A. Vascular dysfunction in obstructive sleep apnea and type 2 diabetes mellitus. Obesity (Silver Spring). 2011;19(1):17–22.CrossRef
54.
go back to reference Gagnadoux F, Pepin JL, Vielle B, Bironneau V, Chouet-Girard F, Launois S, Meslier N, Meurice JC, Nguyen XL, Paris A, et al. Impact of mandibular advancement therapy on endothelial function in severe obstructive sleep apnea. Am J Respir Crit Care Med. 2017. doi:10.1164/rccm.201609-1817OC.PubMed Gagnadoux F, Pepin JL, Vielle B, Bironneau V, Chouet-Girard F, Launois S, Meslier N, Meurice JC, Nguyen XL, Paris A, et al. Impact of mandibular advancement therapy on endothelial function in severe obstructive sleep apnea. Am J Respir Crit Care Med. 2017. doi:10.​1164/​rccm.​201609-1817OC.PubMed
55.
go back to reference Araujo Lda S, Fernandes JF, Klein MR, Sanjuliani AF. Obstructive sleep apnea is independently associated with inflammation and insulin resistance, but not with blood pressure, plasma catecholamines, and endothelial function in obese subjects. Nutrition. 2015;31(11–12):1351–7.CrossRefPubMed Araujo Lda S, Fernandes JF, Klein MR, Sanjuliani AF. Obstructive sleep apnea is independently associated with inflammation and insulin resistance, but not with blood pressure, plasma catecholamines, and endothelial function in obese subjects. Nutrition. 2015;31(11–12):1351–7.CrossRefPubMed
56.
go back to reference Hanis CL, Redline S, Cade BE, Bell GI, Cox NJ, Below JE, Brown EL, Aguilar D. Beyond type 2 diabetes, obesity and hypertension: an axis including sleep apnea, left ventricular hypertrophy, endothelial dysfunction, and aortic stiffness among Mexican Americans in Starr County, Texas. Cardiovasc Diabetol. 2016;15:86.CrossRefPubMedPubMedCentral Hanis CL, Redline S, Cade BE, Bell GI, Cox NJ, Below JE, Brown EL, Aguilar D. Beyond type 2 diabetes, obesity and hypertension: an axis including sleep apnea, left ventricular hypertrophy, endothelial dysfunction, and aortic stiffness among Mexican Americans in Starr County, Texas. Cardiovasc Diabetol. 2016;15:86.CrossRefPubMedPubMedCentral
57.
go back to reference Rodriguez CJ, Miyake Y, Grahame-Clarke C, Di Tullio MR, Sciacca RR, Boden-Albala B, Sacco RL, Homma S. Relation of plasma glucose and endothelial function in a population-based multiethnic sample of subjects without diabetes mellitus. Am J Cardiol. 2005;96(9):1273–7.CrossRefPubMed Rodriguez CJ, Miyake Y, Grahame-Clarke C, Di Tullio MR, Sciacca RR, Boden-Albala B, Sacco RL, Homma S. Relation of plasma glucose and endothelial function in a population-based multiethnic sample of subjects without diabetes mellitus. Am J Cardiol. 2005;96(9):1273–7.CrossRefPubMed
58.
go back to reference Shaw JE, Punjabi NM, Naughton MT, Willes L, Bergenstal RM, Cistulli PA, Fulcher GR, Richards GN, Zimmet PZ. the effect of treatment of obstructive sleep apnea on glycemic control in type 2 diabetes. Am J Respir Crit Care Med. 2016;194(4):486–92.CrossRefPubMed Shaw JE, Punjabi NM, Naughton MT, Willes L, Bergenstal RM, Cistulli PA, Fulcher GR, Richards GN, Zimmet PZ. the effect of treatment of obstructive sleep apnea on glycemic control in type 2 diabetes. Am J Respir Crit Care Med. 2016;194(4):486–92.CrossRefPubMed
59.
go back to reference McEvoy RD, Antic NA, Heeley E, Luo Y, Ou Q, Zhang X, Mediano O, Chen R, Drager LF, Liu Z, et al. CPAP for prevention of cardiovascular events in obstructive sleep apnea. N Engl J Med. 2016;375(10):919–31.CrossRefPubMed McEvoy RD, Antic NA, Heeley E, Luo Y, Ou Q, Zhang X, Mediano O, Chen R, Drager LF, Liu Z, et al. CPAP for prevention of cardiovascular events in obstructive sleep apnea. N Engl J Med. 2016;375(10):919–31.CrossRefPubMed
60.
go back to reference Lavie L. Oxidative stress in obstructive sleep apnea and intermittent hypoxia–revisited–the bad ugly and good: implications to the heart and brain. Sleep Med Rev. 2015;20:27–45.CrossRefPubMed Lavie L. Oxidative stress in obstructive sleep apnea and intermittent hypoxia–revisited–the bad ugly and good: implications to the heart and brain. Sleep Med Rev. 2015;20:27–45.CrossRefPubMed
61.
go back to reference Kayama Y, Raaz U, Jagger A, Adam M, Schellinger IN, Sakamoto M, Suzuki H, Toyama K, Spin JM, Tsao PS. Diabetic cardiovascular disease induced by oxidative stress. Int J Mol Sci. 2015;16(10):25234–63.CrossRefPubMedPubMedCentral Kayama Y, Raaz U, Jagger A, Adam M, Schellinger IN, Sakamoto M, Suzuki H, Toyama K, Spin JM, Tsao PS. Diabetic cardiovascular disease induced by oxidative stress. Int J Mol Sci. 2015;16(10):25234–63.CrossRefPubMedPubMedCentral
62.
go back to reference Stradling JR, Schwarz EI, Schlatzer C, Manuel AR, Lee R, Antoniades C, Kohler M. Biomarkers of oxidative stress following continuous positive airway pressure withdrawal: data from two randomised trials. Eur Respir J. 2015;46(4):1065–71.CrossRefPubMedPubMedCentral Stradling JR, Schwarz EI, Schlatzer C, Manuel AR, Lee R, Antoniades C, Kohler M. Biomarkers of oxidative stress following continuous positive airway pressure withdrawal: data from two randomised trials. Eur Respir J. 2015;46(4):1065–71.CrossRefPubMedPubMedCentral
63.
go back to reference Chen LD, Liu JN, Lin L, Wu Z, Li H, Ye YM, Xu QZ, Lin QC. Effect of continuous positive airway pressure on adiponectin in patients with obstructive sleep apnea: a meta-analysis. PLoS ONE. 2015;10(9):e0136837.CrossRefPubMedPubMedCentral Chen LD, Liu JN, Lin L, Wu Z, Li H, Ye YM, Xu QZ, Lin QC. Effect of continuous positive airway pressure on adiponectin in patients with obstructive sleep apnea: a meta-analysis. PLoS ONE. 2015;10(9):e0136837.CrossRefPubMedPubMedCentral
64.
go back to reference Wagner DD. The Weibel-Palade body: the storage granule for von Willebrand factor and P-selectin. Thromb Haemost. 1993;70(1):105–10.PubMed Wagner DD. The Weibel-Palade body: the storage granule for von Willebrand factor and P-selectin. Thromb Haemost. 1993;70(1):105–10.PubMed
65.
go back to reference Dong ZM, Brown AA, Wagner DD. Prominent role of P-selectin in the development of advanced atherosclerosis in ApoE-deficient mice. Circulation. 2000;101(19):2290–5.CrossRefPubMed Dong ZM, Brown AA, Wagner DD. Prominent role of P-selectin in the development of advanced atherosclerosis in ApoE-deficient mice. Circulation. 2000;101(19):2290–5.CrossRefPubMed
66.
go back to reference Minoguchi K, Yokoe T, Tazaki T, Minoguchi H, Oda N, Tanaka A, Yamamoto M, Ohta S, O’Donnell CP, Adachi M. Silent brain infarction and platelet activation in obstructive sleep apnea. Am J Respir Crit Care Med. 2007;175(6):612–7.CrossRefPubMed Minoguchi K, Yokoe T, Tazaki T, Minoguchi H, Oda N, Tanaka A, Yamamoto M, Ohta S, O’Donnell CP, Adachi M. Silent brain infarction and platelet activation in obstructive sleep apnea. Am J Respir Crit Care Med. 2007;175(6):612–7.CrossRefPubMed
67.
go back to reference Schiffrin EL. Remodeling of resistance arteries in essential hypertension and effects of antihypertensive treatment. Am J Hypertens. 2004;17(12 Pt 1):1192–200.CrossRefPubMed Schiffrin EL. Remodeling of resistance arteries in essential hypertension and effects of antihypertensive treatment. Am J Hypertens. 2004;17(12 Pt 1):1192–200.CrossRefPubMed
68.
go back to reference Simpson PJ, Hoyos CM, Celermajer D, Liu PY, Ng MK. Effects of continuous positive airway pressure on endothelial function and circulating progenitor cells in obstructive sleep apnoea: a randomised sham-controlled study. Int J Cardiol. 2013;168(3):2042–8.CrossRefPubMed Simpson PJ, Hoyos CM, Celermajer D, Liu PY, Ng MK. Effects of continuous positive airway pressure on endothelial function and circulating progenitor cells in obstructive sleep apnoea: a randomised sham-controlled study. Int J Cardiol. 2013;168(3):2042–8.CrossRefPubMed
69.
go back to reference Lian BQ, Keaney JF Jr. Predicting ischemic heart disease in women: the value of endothelial function. J Am Coll Cardiol. 2010;55(16):1697–9.CrossRefPubMed Lian BQ, Keaney JF Jr. Predicting ischemic heart disease in women: the value of endothelial function. J Am Coll Cardiol. 2010;55(16):1697–9.CrossRefPubMed
70.
go back to reference Parati G, Lombardi C, Hedner J, Bonsignore MR, Grote L, Tkacova R, Levy P, Riha R, Bassetti C, Narkiewicz K, et al. Recommendations for the management of patients with obstructive sleep apnoea and hypertension. Eur Respir J. 2013;41(3):523–38.CrossRefPubMed Parati G, Lombardi C, Hedner J, Bonsignore MR, Grote L, Tkacova R, Levy P, Riha R, Bassetti C, Narkiewicz K, et al. Recommendations for the management of patients with obstructive sleep apnoea and hypertension. Eur Respir J. 2013;41(3):523–38.CrossRefPubMed
71.
go back to reference Fontes-Guerra PC, Cardoso CR, Muxfeldt ES, Salles GF. Nitroglycerin-mediated, but not flow-mediated vasodilation, is associated with blunted nocturnal blood pressure fall in patients with resistant hypertension. J Hypertens. 2015;33(8):1666–75.CrossRefPubMed Fontes-Guerra PC, Cardoso CR, Muxfeldt ES, Salles GF. Nitroglycerin-mediated, but not flow-mediated vasodilation, is associated with blunted nocturnal blood pressure fall in patients with resistant hypertension. J Hypertens. 2015;33(8):1666–75.CrossRefPubMed
72.
go back to reference 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(2):257–65.CrossRefPubMed 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(2):257–65.CrossRefPubMed
73.
go back to reference Torimoto K, Okada Y, Mori H, Tanaka Y. Relationship between fluctuations in glucose levels measured by continuous glucose monitoring and vascular endothelial dysfunction in type 2 diabetes mellitus. Cardiovasc Diabetol. 2013;12:1.CrossRefPubMedPubMedCentral Torimoto K, Okada Y, Mori H, Tanaka Y. Relationship between fluctuations in glucose levels measured by continuous glucose monitoring and vascular endothelial dysfunction in type 2 diabetes mellitus. Cardiovasc Diabetol. 2013;12:1.CrossRefPubMedPubMedCentral
74.
go back to reference Fendri S, Rose D, Myambu S, Jeanne S, Lalau JD. Nocturnal hyperglycaemia in type 2 diabetes with sleep apnoea syndrome. Diabetes Res Clin Pract. 2011;91(1):e21–3.CrossRefPubMed Fendri S, Rose D, Myambu S, Jeanne S, Lalau JD. Nocturnal hyperglycaemia in type 2 diabetes with sleep apnoea syndrome. Diabetes Res Clin Pract. 2011;91(1):e21–3.CrossRefPubMed
Metadata
Title
Association between obstructive sleep apnea severity and endothelial dysfunction in patients with type 2 diabetes
Authors
Vanessa Bironneau
François Goupil
Pierre Henri Ducluzeau
Marc Le Vaillant
Pierre Abraham
Samir Henni
Séverine Dubois
Audrey Paris
Pascaline Priou
Nicole Meslier
Claire Sanguin
Wojciech Trzépizur
Ramaroson Andriantsitohaina
Maria Carmen Martinez
Frédéric Gagnadoux
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2017
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-017-0521-y

Other articles of this Issue 1/2017

Cardiovascular Diabetology 1/2017 Go to the issue
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.