Obstructive sleep apnea (OSA) is an independent risk factor for stroke. Furthermore, intracranial carotid artery calcification (ICAC) is a marker for subclinical atherosclerosis and future cardiovascular events. We investigated the association between the high risk for OSA and ICAC in patients with acute ischemic stroke.
We retrospectively investigated 73 patients who were admitted to the hospital with acute ischemic stroke in the internal carotid artery (ICA) territory due to large-artery atherosclerosis. The risk for OSA was assessed using the Berlin Questionnaire, and patients were classified into low-risk (LR-OSA) and high-risk groups (HR-OSA). We compared the burden of ICAC between the two groups. Univariable and multivariable analyses were conducted to investigate the association of high risk for OSA with the presence of calcium in intracranial ICA.
The HR-OSA group of 35 patients (48%) was significantly older and had a higher rate of hypertension and diabetes mellitus than the LR-OSA group. The HR-OSA group had more frequent ICAC (92% vs. 63%, p < 0.001), higher Agatston score (162.0 vs. 8.5, p < 0.001), and greater total volume of ICAC (261.2 mm3 vs. 20.1 mm3, p < 0.001) in the intracranial ICA. Presence of calcium in symptomatic intracranial ICA was positively correlated with age (odds ratio, OR, 1.432; 95% confidence interval, CI, 1.098–1.868) and HR-OSA (OR, 18.272; 95% CI, 0.500–668.401) in multivariable logistic regression analysis.
This study showed that the presence of calcium in symptomatic intracranial ICA was related to high risk for OSA in patients with acute ischemic stroke.
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Bradley TD, Floras JS (2009) Obstructive sleep apnoea and its cardiovascular consequences. Lancet 373(9657):82–93. https://doi.org/10.1016/S0140-6736(08)61622-0
Song TJ, Park JH, Choi KH, Chang Y, Moon J, Kim JH, Choi Y, Kim YJ, Lee HW (2017) Moderate-to-severe obstructive sleep apnea is associated with cerebral small vessel disease. Sleep Med 30:36–42. https://doi.org/10.1016/j.sleep.2016.03.006
Song TJ, Park JH, Choi KH, Kim JH, Choi Y, Chang Y, Kim HJ, Moon J, Kim YJ, Lee HW (2017) Is obstructive sleep apnea associated with the presence of intracranial cerebral atherosclerosis? Sleep Breath 21(3):639–646. https://doi.org/10.1007/s11325-016-1450-9
Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM, Mohsenin V (2005) Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med 353(19):2034–2041. https://doi.org/10.1056/NEJMoa043104
Lipford MC, Flemming KD, Calvin AD, Mandrekar J, Brown RD Jr, Somers VK, Caples SM (2015) Associations between cardioembolic stroke and obstructive sleep apnea. Sleep 38(11):1699–1705. https://doi.org/10.5665/sleep.5146
Disler P, Hansford A, Skelton J, Wright P, Kerr J, O'Reilly J, Hepworth J, Middleton S, Sullivan C (2002) Diagnosis and treatment of obstructive sleep apnea in a stroke rehabilitation unit: a feasibility study. Am J Phys Med Rehabil 81(8):622–625
Johnson KG, Johnson DC (2010) Frequency of sleep apnea in stroke and TIA patients: a meta-analysis. J Clin Sleep Med 6(2):131–137
Senaratna CV, Perret JL, Lodge CJ, Lowe AJ, Campbell BE, Matheson MC, Hamilton GS, Dharmage SC (2017) Prevalence of obstructive sleep apnea in the general population: a systematic review. Sleep Med Rev 34:70–81. https://doi.org/10.1016/j.smrv.2016.07.002
Kim J, In K, Kim J, You S, Kang K, Shim J, Lee S, Lee J, Lee S, Park C, Shin C (2004) Prevalence of sleep-disordered breathing in middle-aged Korean men and women. Am J Respir Crit Care Med 170(10):1108–1113. https://doi.org/10.1164/rccm.200404-519OC
Sunwoo JS, Hwangbo Y, Kim WJ, Chu MK, Yun CH, Yang KI (2018) Prevalence, sleep characteristics, and comorbidities in a population at high risk for obstructive sleep apnea: a nationwide questionnaire study in South Korea. PLoS One 13(2):e0193549. https://doi.org/10.1371/journal.pone.0193549
Kwon Y, Duprez DA, Jacobs DR, Nagayoshi M, McClelland RL, Shahar E, Budoff M, Redline S, Shea S, Carr JJ, Lutsey PL (2014) Obstructive sleep apnea and progression of coronary artery calcium: the multi-ethnic study of atherosclerosis study. J Am Heart Assoc 3(5):e001241. https://doi.org/10.1161/JAHA.114.001241
Peters SA, den Ruijter HM, Bots ML, Moons KG (2012) Improvements in risk stratification for the occurrence of cardiovascular disease by imaging subclinical atherosclerosis: a systematic review. Heart 98(3):177–184. https://doi.org/10.1136/heartjnl-2011-300747
Mauriello A, Servadei F, Zoccai GB, Giacobbi E, Anemona L, Bonanno E, Casella S (2013) Coronary calcification identifies the vulnerable patient rather than the vulnerable plaque. Atherosclerosis 229(1):124–129. https://doi.org/10.1016/j.atherosclerosis.2013.03.010
Cho KH, Lee DH, Kim KM, Choi YH, Nam HS, Heo JH, Heo K, Kim YD (2019) Relationship between sleep apnea and coronary artery calcium in patients with ischemic stroke. Front Neurol 10:819. https://doi.org/10.3389/fneur.2019.00819
Alexopoulos N, Raggi P (2009) Calcification in atherosclerosis. Nat Rev Cardiol 6(11):681–688. https://doi.org/10.1038/nrcardio.2009.165
Bugnicourt JM, Leclercq C, Chillon JM, Diouf M, Deramond H, Canaple S, Lamy C, Massy ZA, Godefroy O (2011) Presence of intracranial artery calcification is associated with mortality and vascular events in patients with ischemic stroke after hospital discharge: a cohort study. Stroke 42(12):3447–3453. https://doi.org/10.1161/STROKEAHA.111.618652
Bos D, Portegies ML, van der Lugt A, Bos MJ, Koudstaal PJ, Hofman A, Krestin GP, Franco OH, Vernooij MW, Ikram MA (2014) Intracranial carotid artery atherosclerosis and the risk of stroke in whites: the Rotterdam study. JAMA Neurol 71(4):405–411. https://doi.org/10.1001/jamaneurol.2013.6223
Kim JM, Park KY, Bae JH, Han SH, Jeong HB, Jeong D (2019) Intracranial arterial calcifications can reflect cerebral atherosclerosis burden. J Clin Neurol 15(1):38–45. https://doi.org/10.3988/jcn.2019.15.1.38
Kang K, Park KS, Kim JE, Kim SW, Kim YT, Kim JS, Lee HW (2013) Usefulness of the Berlin questionnaire to identify patients at high risk for obstructive sleep apnea: a population-based door-to-door study. Sleep Breath 17(2):803–810. https://doi.org/10.1007/s11325-012-0767-2
Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15(4):827–832
Tachikawa R, Koyasu S, Matsumoto T, Hamada S, Azuma M, Murase K, Tanizawa K, Inouchi M, Oga T, Mishima M, Togashi K, Chin K (2015) Obstructive sleep apnea and abdominal aortic calcification: is there an association independent of comorbid risk factors? Atherosclerosis 241(1):6–11. https://doi.org/10.1016/j.atherosclerosis.2015.04.801
Lutsey PL, McClelland RL, Duprez D, Shea S, Shahar E, Nagayoshi M, Budoff M, Kaufman JD, Redline S (2015) Objectively measured sleep characteristics and prevalence of coronary artery calcification: the multi-ethnic study of atherosclerosis sleep study. Thorax 70(9):880–887. https://doi.org/10.1136/thoraxjnl-2015-206871
van Dijk AC, Fonville S, Zadi T, van Hattem AM, Saiedie G, Koudstaal PJ, van der Lugt A (2014) Association between arterial calcifications and nonlacunar and lacunar ischemic strokes. Stroke 45(3):728–733. https://doi.org/10.1161/STROKEAHA.113.003197
Berliner JA, Navab M, Fogelman AM, Frank JS, Demer LL, Edwards PA, Watson AD, Lusis AJ (1995) Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation 91(9):2488–2496
Kapur VK, Auckley DH, Chowdhuri S, Kuhlmann DC, Mehra R, Ramar K, Harrod CG (2017) Clinical practice guideline for diagnostic testing for adult obstructive sleep apnea: an American Academy of sleep medicine clinical practice guideline. J Clin Sleep Med 13(3):479–504. https://doi.org/10.5664/jcsm.6506
Kepplinger J, Barlinn K, Albright KC, Schrempf W, Boehme AK, Pallesen LP, Schwanebeck U, Graehlert X, Storch A, Reichmann H, Alexandrov AV, Bodechtel U (2013) Early sleep apnea screening on a stroke unit is feasible in patients with acute cerebral ischemia. J Neurol 260(5):1343–1350. https://doi.org/10.1007/s00415-012-6803-0
ElKholy SH, Amer HA, Nada MM, Nada MA, Labib A (2012) Sleep-related breathing disorders in cerebrovascular stroke and transient ischemic attacks: a comparative study. J Clin Neurophysiol 29(2):194–198. https://doi.org/10.1097/WNP.0b013e31824d96b0
Wu XH, Chen XY, Wang LJ, Wong KS (2016) Intracranial artery calcification and its clinical significance. J Clin Neurol 12(3):253–261. https://doi.org/10.3988/jcn.2016.12.3.253
Drager LF, Polotsky VY, Lorenzi-Filho G (2011) Obstructive sleep apnea: an emerging risk factor for atherosclerosis. Chest 140(2):534–542. https://doi.org/10.1378/chest.10-2223
Lee SA, Amis TC, Byth K, Larcos G, Kairaitis K, Robinson TD, Wheatley JR (2008) Heavy snoring as a cause of carotid artery atherosclerosis. Sleep 31(9):1207–1213
Amatoury J, Howitt L, Wheatley JR, Avolio AP, Amis TC (2006) Snoring-related energy transmission to the carotid artery in rabbits. J Appl Physiol (1985) 100(5):1547–1553. https://doi.org/10.1152/japplphysiol.01439.2005
Savransky V, Jun J, Li J, Nanayakkara A, Fonti S, Moser AB, Steele KE, Schweitzer MA, Patil SP, Bhanot S, Schwartz AR, Polotsky VY (2008) Dyslipidemia and atherosclerosis induced by chronic intermittent hypoxia are attenuated by deficiency of stearoyl coenzyme A desaturase. Circ Res 103(10):1173–1180. https://doi.org/10.1161/CIRCRESAHA.108.178533
A AT (2015) Obstructive sleep apnoea and vascular disease in patients with type 2 diabetes. Eur Endocrinol 11(2):81–89. https://doi.org/10.17925/EE.2015.11.02.81
Arzt M, Young T, Finn L, Skatrud JB, Bradley TD (2005) Association of sleep-disordered breathing and the occurrence of stroke. Am J Respir Crit Care Med 172(11):1447–1451. https://doi.org/10.1164/rccm.200505-702OC
Availability of data and material
We deposited the raw data. However, out data cannot be used without approval of Institutional Review Board of our hospital for ethical or legal reasons.
This work was supported by the Soonchunhyang University Research Fund.
Conflict of interest
The authors declare that they have no competing interests.
The institutional review board of Soonchunhyang University Cheonan Hospital (SCHCA 2018-07-027-001) approved this retrospective study.
The institutional review board approved this retrospective study, and the requirement for informed consent was waived.
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Woo, H.G., Song, T., Jung, J.S. et al. Association between the high risk for obstructive sleep apnea and intracranial carotid artery calcification in patients with acute ischemic stroke. Sleep Breath (2020). https://doi.org/10.1007/s11325-020-02117-x
- Obstructive sleep apnea
- Intracranial carotid artery calcification
- Berlin questionnaire