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Published in: European Archives of Oto-Rhino-Laryngology 4/2014

01-04-2014 | Miscellaneous

Obstructive sleep apnea syndrome is associated with metabolic syndrome and inflammation

Authors: Qi-Chang Lin, Li-Da Chen, Yao-Hua Yu, Kai-Xiong Liu, Shao-Yong Gao

Published in: European Archives of Oto-Rhino-Laryngology | Issue 4/2014

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Abstract

Obstructive sleep apnea (OSA) is an independent risk factor for cardiovascular morbidity and mortality. However, the underlying mechanism is unclear. In this cross-sectional study, we investigated the influence of OSA on metabolic syndrome (MetS) and inflammation, which were considered as cardiovascular risks. A total of 144 consecutive male patients who underwent standard polysomnography were enrolled. Fasting blood samples were obtained from all patients for glucose, high-sensitivity C-reactive protein (hs-CRP) and lipids measurement. A metabolic score was established as the total number of the positive diagnostic criteria of metabolic syndrome for each patient. Systolic blood pressure, diastolic blood pressure, fasting glucose, hs-CRP and metabolic score significantly increased with the aggravation of OSA severity. Metabolic score increased from 1.74 ± 1.20 to 2.89 ± 0.99 with OSA severity (p = 0.000). hs-CRP increased from 0.68 (0.43–1.10) to 1.44 (0.62–4.02) mg/L with OSA severity (p = 0.002). After adjustment for confounders, apnea–hypopnea index and body mass index (BMI) were the major contributing factors for metabolic score (β = 0.257, p = 0.003 and β = 0.344, p = 0.000, respectively), lowest O2 saturation and BMI were the independent predictors of hs-CRP (β = −0.255, p = 0.003 and β = 0.295, p = 0.001, respectively). OSA is independently associated with sum of metabolic components and hs-CRP.
Literature
1.
go back to reference Young T, Peppard PE, Gottlieb DJ (2002) Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med 165:1217–1239PubMedCrossRef Young T, Peppard PE, Gottlieb DJ (2002) Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med 165:1217–1239PubMedCrossRef
2.
go back to reference Shahar E, Whitney CW, Redline S, Lee ET, Newman AB, Nieto FJ, O’Connor GT, Boland LL, Schwartz JE, Samet JM (2001) Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the sleep heart health study. Am J Respir Crit Care Med 163:19–25PubMedCrossRef Shahar E, Whitney CW, Redline S, Lee ET, Newman AB, Nieto FJ, O’Connor GT, Boland LL, Schwartz JE, Samet JM (2001) Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the sleep heart health study. Am J Respir Crit Care Med 163:19–25PubMedCrossRef
3.
go back to reference Chami HA, Resnick HE, Quan SF, Gottlieb DJ (2011) Association of incident cardiovascular disease with progression of sleep-disordered breathing. Circulation 123:1280–1286PubMedCentralPubMedCrossRef Chami HA, Resnick HE, Quan SF, Gottlieb DJ (2011) Association of incident cardiovascular disease with progression of sleep-disordered breathing. Circulation 123:1280–1286PubMedCentralPubMedCrossRef
4.
go back to reference Redline S, Yenokyan G, Gottlieb DJ, Shahar E, O’Connor GT, Resnick HE, Diener-West M, Sanders MH, Wolf PA, Geraghty EM, Ali T, Lebowitz M, Punjabi NM (2010) Obstructive sleep apnea–hypopnea and incident stroke: the sleep heart health study. Am J Respir Crit Care Med 182:269–277PubMedCentralPubMedCrossRef Redline S, Yenokyan G, Gottlieb DJ, Shahar E, O’Connor GT, Resnick HE, Diener-West M, Sanders MH, Wolf PA, Geraghty EM, Ali T, Lebowitz M, Punjabi NM (2010) Obstructive sleep apnea–hypopnea and incident stroke: the sleep heart health study. Am J Respir Crit Care Med 182:269–277PubMedCentralPubMedCrossRef
5.
go back to reference Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American heart association/national heart, lung, and blood institute scientific statement. Circulation 112:2735–2752PubMedCrossRef Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American heart association/national heart, lung, and blood institute scientific statement. Circulation 112:2735–2752PubMedCrossRef
6.
go back to reference Reaven GM (1988) Banting lecture 1988: role of insulin resistance in human disease. Diabetes 37:1595–1607PubMedCrossRef Reaven GM (1988) Banting lecture 1988: role of insulin resistance in human disease. Diabetes 37:1595–1607PubMedCrossRef
7.
go back to reference Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT (2002) The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA 288:2709–2716PubMedCrossRef Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT (2002) The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA 288:2709–2716PubMedCrossRef
8.
go back to reference Ho JS, Cannaday JJ, Barlow CE, Mitchell TL, Cooper KH, FitzGerald SJ (2008) Relation of the number of metabolic syndrome risk factors with all-cause and cardiovascular mortality. Am J Cardiol 102:689–692PubMedCrossRef Ho JS, Cannaday JJ, Barlow CE, Mitchell TL, Cooper KH, FitzGerald SJ (2008) Relation of the number of metabolic syndrome risk factors with all-cause and cardiovascular mortality. Am J Cardiol 102:689–692PubMedCrossRef
9.
go back to reference Thomas GN, Phillips AC, Carroll D, Gale CR, Batty GD (2010) The metabolic syndrome adds utility to the prediction of mortality over its components: the Vietnam experience study. Atherosclerosis 210:256–261PubMedCrossRef Thomas GN, Phillips AC, Carroll D, Gale CR, Batty GD (2010) The metabolic syndrome adds utility to the prediction of mortality over its components: the Vietnam experience study. Atherosclerosis 210:256–261PubMedCrossRef
10.
go back to reference Corrado E, Rizzo M, Coppola G, Fattouch K, Novo G, Marturana I, Ferrara F, Novo S (2010) An update on the role of markers of inflammation in atherosclerosis. J Atheroscler Thromb 17:1–11PubMedCrossRef Corrado E, Rizzo M, Coppola G, Fattouch K, Novo G, Marturana I, Ferrara F, Novo S (2010) An update on the role of markers of inflammation in atherosclerosis. J Atheroscler Thromb 17:1–11PubMedCrossRef
11.
go back to reference Ikonomidis I, Stamatelopoulos K, Lekakis J, Vamvakou GD, Kremastinos DT (2008) Inflammatory and non-invasive vascular markers: the multimarker approach for risk stratification in coronary artery disease. Atherosclerosis 199:3–11PubMedCrossRef Ikonomidis I, Stamatelopoulos K, Lekakis J, Vamvakou GD, Kremastinos DT (2008) Inflammatory and non-invasive vascular markers: the multimarker approach for risk stratification in coronary artery disease. Atherosclerosis 199:3–11PubMedCrossRef
14.
go back to reference Rifai N, Tracy RP, Ridker PM (1999) Clinical efficacy of an automated high-sensitivity C-reactive protein assay. Clin Chem 45:2136–2141PubMed Rifai N, Tracy RP, Ridker PM (1999) Clinical efficacy of an automated high-sensitivity C-reactive protein assay. Clin Chem 45:2136–2141PubMed
15.
go back to reference Kono M, Tatsumi K, Saibara T, Nakamura A, Tanabe N, Takiguchi Y, Kuriyama T (2007) Obstructive sleep apnea syndrome is associated with some components of metabolic syndrome. Chest 131:1387–1392PubMedCrossRef Kono M, Tatsumi K, Saibara T, Nakamura A, Tanabe N, Takiguchi Y, Kuriyama T (2007) Obstructive sleep apnea syndrome is associated with some components of metabolic syndrome. Chest 131:1387–1392PubMedCrossRef
16.
go back to reference Lam JC, Lam B, Lam CL, Fong D, Wang JK, Tse HF, Lam KS, Ip MS (2006) Obstructive sleep apnea and the metabolic syndrome in community-based Chinese adults in Hong Kong. Respir Med 100:980–987PubMedCrossRef Lam JC, Lam B, Lam CL, Fong D, Wang JK, Tse HF, Lam KS, Ip MS (2006) Obstructive sleep apnea and the metabolic syndrome in community-based Chinese adults in Hong Kong. Respir Med 100:980–987PubMedCrossRef
17.
go back to reference Punjabi NM, Beamer BA (2007) C-reactive protein is associated with sleep disordered breathing independent of adiposity. Sleep 30:29–34PubMed Punjabi NM, Beamer BA (2007) C-reactive protein is associated with sleep disordered breathing independent of adiposity. Sleep 30:29–34PubMed
18.
go back to reference Lui MM, Lam JC, Mak HK, Xu A, Ooi C, Lam DC, Mak JC, Khong PL, Ip MS (2009) C-reactive protein is associated with obstructive sleep apnea independent of visceral obesity. Chest 135:950–956PubMedCrossRef Lui MM, Lam JC, Mak HK, Xu A, Ooi C, Lam DC, Mak JC, Khong PL, Ip MS (2009) C-reactive protein is associated with obstructive sleep apnea independent of visceral obesity. Chest 135:950–956PubMedCrossRef
19.
go back to reference Peled N, Kassirer M, Shitrit D, Kogan Y, Shlomi D, Berliner AS, Kramer MR (2007) The association of OSA with insulin resistance, inflammation and metabolic syndrome. Respir Med 101:1696–1701PubMedCrossRef Peled N, Kassirer M, Shitrit D, Kogan Y, Shlomi D, Berliner AS, Kramer MR (2007) The association of OSA with insulin resistance, inflammation and metabolic syndrome. Respir Med 101:1696–1701PubMedCrossRef
20.
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 Med 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 Med 8:12–17PubMedCrossRef
21.
go back to reference Barcelo A, Barbe F, Llompart E, Mayoralas LR, Ladaria A, Bosch M, Agusti AG (2004) Effects of obesity on C-reactive protein level and metabolic disturbances in male patients with obstructive sleep apnea. Am J Med 117:118–121PubMedCrossRef Barcelo A, Barbe F, Llompart E, Mayoralas LR, Ladaria A, Bosch M, Agusti AG (2004) Effects of obesity on C-reactive protein level and metabolic disturbances in male patients with obstructive sleep apnea. Am J Med 117:118–121PubMedCrossRef
22.
go back to reference Taheri S, Austin D, Lin L, Nieto FJ, Young T, Mignot E (2007) Correlates of serum C-reactive protein (CRP)—no association with sleep duration or sleep disordered breathing. Sleep 30:991–996PubMedCentralPubMed Taheri S, Austin D, Lin L, Nieto FJ, Young T, Mignot E (2007) Correlates of serum C-reactive protein (CRP)—no association with sleep duration or sleep disordered breathing. Sleep 30:991–996PubMedCentralPubMed
23.
go back to reference Guilleminault C, Kirisoglu C, Ohayon MM (2004) C-reactive protein and sleep-disordered breathing. Sleep 27:1507–1511PubMed Guilleminault C, Kirisoglu C, Ohayon MM (2004) C-reactive protein and sleep-disordered breathing. Sleep 27:1507–1511PubMed
24.
go back to reference Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee (1995). World Health Organ Tech Rep Ser 854:1-452 Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee (1995). World Health Organ Tech Rep Ser 854:1-452
25.
go back to reference Schulz H (2007) Phasic or transient? Comment on the terminology of the AASM manual for the scoring of sleep and associated events. J Clin Sleep Med 3:752PubMedCentralPubMed Schulz H (2007) Phasic or transient? Comment on the terminology of the AASM manual for the scoring of sleep and associated events. J Clin Sleep Med 3:752PubMedCentralPubMed
26.
go back to reference Lam DC, Xu A, Lam KS, Lam B, Lam JC, Lui MM, Ip MS (2009) Serum adipocyte-fatty acid binding protein level is elevated in severe OSA and correlates with insulin resistance. Eur Respir J 33:346–351PubMedCrossRef Lam DC, Xu A, Lam KS, Lam B, Lam JC, Lui MM, Ip MS (2009) Serum adipocyte-fatty acid binding protein level is elevated in severe OSA and correlates with insulin resistance. Eur Respir J 33:346–351PubMedCrossRef
27.
go back to reference Tan CE, Ma S, Wai D, Chew SK, Tai ES (2004) Can we apply the national cholesterol education program adult treatment panel definition of the metabolic syndrome to Asians? Diabetes Care 27:1182–1186PubMedCrossRef Tan CE, Ma S, Wai D, Chew SK, Tai ES (2004) Can we apply the national cholesterol education program adult treatment panel definition of the metabolic syndrome to Asians? Diabetes Care 27:1182–1186PubMedCrossRef
28.
go back to reference Oktay B, Akbal E, Firat H, Ardic S, Kizilgun M (2009) CPAP treatment in the coexistence of obstructive sleep apnea syndrome and metabolic syndrome, results of one year follow up. Acta Clin Belg 64:329–334PubMed Oktay B, Akbal E, Firat H, Ardic S, Kizilgun M (2009) CPAP treatment in the coexistence of obstructive sleep apnea syndrome and metabolic syndrome, results of one year follow up. Acta Clin Belg 64:329–334PubMed
29.
go back to reference Mota PC, Drummond M, Winck JC, Santos AC, Almeida J, Marques JA (2011) APAP impact on metabolic syndrome in obstructive sleep apnea patients. Sleep Breath 15:665–672PubMedCrossRef Mota PC, Drummond M, Winck JC, Santos AC, Almeida J, Marques JA (2011) APAP impact on metabolic syndrome in obstructive sleep apnea patients. Sleep Breath 15:665–672PubMedCrossRef
30.
go back to reference Coughlin SR, Mawdsley L, Mugarza JA, Wilding JP, Calverley PM (2007) Cardiovascular and metabolic effects of CPAP in obese males with OSA. Eur Respir J 29:720–727PubMedCrossRef Coughlin SR, Mawdsley L, Mugarza JA, Wilding JP, Calverley PM (2007) Cardiovascular and metabolic effects of CPAP in obese males with OSA. Eur Respir J 29:720–727PubMedCrossRef
31.
go back to reference Shamsuzzaman AS, Winnicki M, Lanfranchi P, Wolk R, Kara T, Accurso V, Somers VK (2002) Elevated C-reactive protein in patients with obstructive sleep apnea. Circulation 105:2462–2464PubMedCrossRef Shamsuzzaman AS, Winnicki M, Lanfranchi P, Wolk R, Kara T, Accurso V, Somers VK (2002) Elevated C-reactive protein in patients with obstructive sleep apnea. Circulation 105:2462–2464PubMedCrossRef
32.
go back to reference Zouaoui Boudjeltia K, Van Meerhaeghe A, Doumit S, Guillaume M, Cauchie P, Brohee D, Vanhaeverbeek M, Kerkhofs M (2006) Sleep apnoea–hypopnoea index is an independent predictor of high-sensitivity C-reactive protein elevation. Respiration 73:243–246PubMedCrossRef Zouaoui Boudjeltia K, Van Meerhaeghe A, Doumit S, Guillaume M, Cauchie P, Brohee D, Vanhaeverbeek M, Kerkhofs M (2006) Sleep apnoea–hypopnoea index is an independent predictor of high-sensitivity C-reactive protein elevation. Respiration 73:243–246PubMedCrossRef
33.
go back to reference Kapsimalis F, Varouchakis G, Manousaki A, Daskas S, Nikita D, Kryger M, Gourgoulianis K (2008) Association of sleep apnea severity and obesity with insulin resistance, C-reactive protein, and leptin levels in male patients with obstructive sleep apnea. Lung 186:209–217PubMedCrossRef Kapsimalis F, Varouchakis G, Manousaki A, Daskas S, Nikita D, Kryger M, Gourgoulianis K (2008) Association of sleep apnea severity and obesity with insulin resistance, C-reactive protein, and leptin levels in male patients with obstructive sleep apnea. Lung 186:209–217PubMedCrossRef
34.
go back to reference Su MC, Chen YC, Huang KT, Wang CC, Lin MC, Lin HC (2013) Association of metabolic factors with high-sensitivity C-reactive protein in patients with sleep-disordered breathing. Eur Arch Otorhinolaryngol 270:749–754PubMedCrossRef Su MC, Chen YC, Huang KT, Wang CC, Lin MC, Lin HC (2013) Association of metabolic factors with high-sensitivity C-reactive protein in patients with sleep-disordered breathing. Eur Arch Otorhinolaryngol 270:749–754PubMedCrossRef
35.
go back to reference Sharma SK, Mishra HK, Sharma H, Goel A, Sreenivas V, Gulati V, Tahir M (2008) Obesity, and not obstructive sleep apnea, is responsible for increased serum hs-CRP levels in patients with sleep-disordered breathing in Delhi. Sleep Med 9:149–156PubMedCrossRef Sharma SK, Mishra HK, Sharma H, Goel A, Sreenivas V, Gulati V, Tahir M (2008) Obesity, and not obstructive sleep apnea, is responsible for increased serum hs-CRP levels in patients with sleep-disordered breathing in Delhi. Sleep Med 9:149–156PubMedCrossRef
36.
go back to reference Ryan S, Nolan GM, Hannigan E, Cunningham S, Taylor C, McNicholas WT (2007) Cardiovascular risk markers in obstructive sleep apnoea syndrome and correlation with obesity. Thorax 62:509–514PubMedCentralPubMedCrossRef Ryan S, Nolan GM, Hannigan E, Cunningham S, Taylor C, McNicholas WT (2007) Cardiovascular risk markers in obstructive sleep apnoea syndrome and correlation with obesity. Thorax 62:509–514PubMedCentralPubMedCrossRef
37.
go back to reference Schiza SE, Mermigkis C, Panagiotis P, Bouloukaki I, Kallergis E, Tzanakis N, Tzortzaki E, Vlachaki E, Siafakas NM (2010) C-reactive protein evolution in obstructive sleep apnoea patients under CPAP therapy. Eur J Clin Invest 40:968–975PubMedCrossRef Schiza SE, Mermigkis C, Panagiotis P, Bouloukaki I, Kallergis E, Tzanakis N, Tzortzaki E, Vlachaki E, Siafakas NM (2010) C-reactive protein evolution in obstructive sleep apnoea patients under CPAP therapy. Eur J Clin Invest 40:968–975PubMedCrossRef
38.
go back to reference Ishida K, Kato M, Kato Y, Yanagihara K, Kinugasa Y, Kotani K, Igawa O, Hisatome I, Shigemasa C, Somers VK (2009) Appropriate use of nasal continuous positive airway pressure decreases elevated C-reactive protein in patients with obstructive sleep apnea. Chest 136:125–129PubMedCentralPubMedCrossRef Ishida K, Kato M, Kato Y, Yanagihara K, Kinugasa Y, Kotani K, Igawa O, Hisatome I, Shigemasa C, Somers VK (2009) Appropriate use of nasal continuous positive airway pressure decreases elevated C-reactive protein in patients with obstructive sleep apnea. Chest 136:125–129PubMedCentralPubMedCrossRef
39.
go back to reference Kohler M, Ayers L, Pepperell JC, Packwood KL, Ferry B, Crosthwaite N, Craig S, Siccoli MM, Davies RJ, Stradling JR (2009) Effects of continuous positive airway pressure on systemic inflammation in patients with moderate to severe obstructive sleep apnoea: a randomised controlled trial. Thorax 64:67–73PubMedCrossRef Kohler M, Ayers L, Pepperell JC, Packwood KL, Ferry B, Crosthwaite N, Craig S, Siccoli MM, Davies RJ, Stradling JR (2009) Effects of continuous positive airway pressure on systemic inflammation in patients with moderate to severe obstructive sleep apnoea: a randomised controlled trial. Thorax 64:67–73PubMedCrossRef
Metadata
Title
Obstructive sleep apnea syndrome is associated with metabolic syndrome and inflammation
Authors
Qi-Chang Lin
Li-Da Chen
Yao-Hua Yu
Kai-Xiong Liu
Shao-Yong Gao
Publication date
01-04-2014
Publisher
Springer Berlin Heidelberg
Published in
European Archives of Oto-Rhino-Laryngology / Issue 4/2014
Print ISSN: 0937-4477
Electronic ISSN: 1434-4726
DOI
https://doi.org/10.1007/s00405-013-2669-8

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