Skip to main content
SpringerLink
Log in

Is obstructive sleep apnea associated with the presence of intracranial cerebral atherosclerosis?

  • Sleep Breathing Physiology and Disorders • Original Article
  • Published:
Sleep and Breathing Aims and scope Submit manuscript

Abstract

Purpose

Intracranial cerebral atherosclerosis (ICAS) is one of critical atherosclerosis which closely related with stroke. Obstructive sleep apnea (OSA) is associated with systemic atherosclerosis, but it is unclear whether OSA is related with the presence of ICAS. We aimed to investigate the association between the presence of ICAS and severity of OSA in patients with suspected OSA.

Methods

This retrospective, cross-sectional study included 283 patients who suspected OSA (presence of one or more OSA-related symptom and high-risk category in Berlin questionnaire) and underwent polysomnography and brain magnetic resonance angiography (MRA). The ICAS was defined as ≥50% decrease of luminal diameter in MRA. The severity of OSA was defined by apnea-hypopnea index (AHI).

Results

The mean age was 60.7 ± 13.5 years, and 55.8% (158/283) were male in all included patients. The 53 (18.7%) patients had ICAS and 117 (41.3%) patients had moderate to severe OSA (AHI ≥ 15). Higher AHI was noted in patients with ICAS compared to those without ICAS (31.7 ± 25.8 versus 15.2 ± 17.4, p = 0.001). In multivariable logistic analyses, after adjusting for age, sex, and variables with p < 0.1 in univariable analyses (hypertension, diabetes mellitus, atrial fibrillation, previous stroke history, body mass index, lipid-lowing agents, arousal index, and minimum oxygen saturation), moderate to severe OSA were independently related with the presence of ICAS (odds ratio 4.17, 95% confidence interval 1.40–12.40, p = 0.010).

Conclusions

Our findings suggest that moderate to severe OSA is associated with the presence of ICAS in patients with suspected OSA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bang OY (2014) Intracranial atherosclerosis: current understanding and perspectives. J Stroke 16(1):27–35. doi:10.5853/jos.2014.16.1.27

    Article  PubMed  PubMed Central  Google Scholar 

  2. Arenillas JF, Molina CA, Chacon P, Rovira A, Montaner J, Coscojuela P, Sanchez E, Quintana M, Alvarez-Sabin J (2004) High lipoprotein (a), diabetes, and the extent of symptomatic intracranial atherosclerosis. Neurology 63(1):27–32

    Article  CAS  PubMed  Google Scholar 

  3. Park KY, Chung CS, Lee KH, Kim GM, Kim YB, Oh K (2006) Prevalence and risk factors of intracranial atherosclerosis in an asymptomatic Korean population. J Clin Neurol 2(1):29–33. doi:10.3988/jcn.2006.2.1.29

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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. doi:10.1056/NEJMoa043104

    Article  CAS  PubMed  Google Scholar 

  5. Song TJ, Park JH, Chang Y, Moon J, Kim JH, Heo JH, Kim YJ, Lee HW (2017) Moderate-to-severe obstructive sleep apnea is associated with cerebral small vessel disease. Sleep Med 30(2):36–42. http://dx.doi.org/10.1016/j.sleep.2016.03.006

  6. Gonzaga C, Bertolami A, Bertolami M, Amodeo C, Calhoun D (2015) Obstructive sleep apnea, hypertension and cardiovascular diseases. J Hum Hypertens 29(12):705–712. doi:10.1038/jhh.2015.15

    Article  CAS  PubMed  Google Scholar 

  7. Ali SS, Oni ET, Warraich HJ, Blaha MJ, Blumenthal RS, Karim A, Shaharyar S, Jamal O, Fialkow J, Cury R, Budoff MJ, Agatston AS, Nasir K (2014) Systematic review on noninvasive assessment of subclinical cardiovascular disease in obstructive sleep apnea: new kid on the block! Sleep Med Rev 18(5):379–391. doi:10.1016/j.smrv.2014.01.004

    Article  PubMed  Google Scholar 

  8. Dziewas R, Ritter M, Usta N, Boentert M, Hor H, Dittrich R, Schabitz WR, Ringelstein EB, Young P (2007) Atherosclerosis and obstructive sleep apnea in patients with ischemic stroke. Cerebrovasc Dis 24(1):122–126. doi:10.1159/000103611

    Article  PubMed  Google Scholar 

  9. Bang OY, Lee PH, Yoon SR, Lee MA, Joo IS, Huh K (2005) Inflammatory markers, rather than conventional risk factors, are different between carotid and MCA atherosclerosis. J Neurol Neurosurg Psychiatry 76(8):1128–1134. doi:10.1136/jnnp.2004.054403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Epstein LJ, Kristo D, Strollo PJ Jr, Friedman N, Malhotra A, Patil SP, Ramar K, Rogers R, Schwab RJ, Weaver EM, Weinstein MD, Adult Obstructive Sleep Apnea Task Force of the American Academy of Sleep M (2009) Clinical guideline for the evaluation, management and long-term care of obstructive sleep apnea in adults. J Clin Sleep Med 5(3):263–276

    PubMed  Google Scholar 

  11. Netzer NC, Stoohs RA, Netzer CM, Clark K, Strohl KP (1999) Using the Berlin questionnaire to identify patients at risk for the sleep apnea syndrome. Ann Intern Med 131(7):485–491

    Article  CAS  PubMed  Google Scholar 

  12. Samuels OB, Joseph GJ, Lynn MJ, Smith HA, Chimowitz MI (2000) A standardized method for measuring intracranial arterial stenosis. AJNR Am J Neuroradiol 21(4):643–646

    CAS  PubMed  Google Scholar 

  13. Kim J, Cha MJ, Lee DH, Lee HS, Nam CM, Nam HS, Kim YD, Heo JH (2011) The association between cerebral atherosclerosis and arterial stiffness in acute ischemic stroke. Atherosclerosis 219(2):887–891. doi:10.1016/j.atherosclerosis.2011.09.013

    Article  CAS  PubMed  Google Scholar 

  14. North American Symptomatic Carotid Endarterectomy Trial C (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325(7):445–453. doi:10.1056/NEJM199108153250701

    Article  Google Scholar 

  15. 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, American Academy of Sleep M (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. doi:10.5664/jcsm.2172

    PubMed  PubMed Central  Google Scholar 

  16. Sateia MJ (2014) International classification of sleep disorders-third edition: highlights and modifications. Chest 146(5):1387–1394. doi:10.1378/chest.14-0970

    Article  PubMed  Google Scholar 

  17. Song TJ, Kim J, Lee HS, Nam CM, Nam HS, Kim YD, Heo JH (2014) Distribution of cerebral microbleeds determines their association with impaired kidney function. J Clin Neurol 10(3):222–228. doi:10.3988/jcn.2014.10.3.222

    Article  PubMed  PubMed Central  Google Scholar 

  18. Schaefer CA, Adam L, Weisser-Thomas J, Pingel S, Vogel G, Klarmann-Schulz U, Nickenig G, Pizarro C, Skowasch D (2015) High prevalence of peripheral arterial disease in patients with obstructive sleep apnoea. Clin Res Cardiol 104(9):719–726. doi:10.1007/s00392-015-0834-3

    Article  CAS  PubMed  Google Scholar 

  19. Gunnarsson SI, Peppard PE, Korcarz CE, Barnet JH, Aeschlimann SE, Hagen EW, Young T, Hla KM, Stein JH (2014) Obstructive sleep apnea is associated with future subclinical carotid artery disease: thirteen-year follow-up from the Wisconsin sleep cohort. Arterioscler Thromb Vasc Biol 34(10):2338–2342. doi:10.1161/ATVBAHA.114.303965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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. doi:10.1161/JAHA.114.001241

    Article  PubMed  PubMed Central  Google Scholar 

  21. Elmasry A, Lindberg E, Berne C, Janson C, Gislason T, Awad Tageldin M, Boman G (2001) Sleep-disordered breathing and glucose metabolism in hypertensive men: a population-based study. J Intern Med 249(2):153–161

    Article  CAS  PubMed  Google Scholar 

  22. Ip MS, Tse HF, Lam B, Tsang KW, Lam WK (2004) Endothelial function in obstructive sleep apnea and response to treatment. Am J Respir Crit Care Med 169(3):348–353. doi:10.1164/rccm.200306-767OC

    Article  PubMed  Google Scholar 

  23. Bang OY, Chung JW, Ryoo S, Moon GJ, Kim GM, Chung CS, Lee KH (2016) Brain microangiopathy and macroangiopathy share common risk factors and biomarkers. Atherosclerosis 246:71–77. doi:10.1016/j.atherosclerosis.2015.12.040

    Article  CAS  PubMed  Google Scholar 

  24. Hayashi K, Handa H, Nagasawa S, Okumura A, Moritake K (1980) Stiffness and elastic behavior of human intracranial and extracranial arteries. J Biomech 13(2):175–184

    Article  CAS  PubMed  Google Scholar 

  25. Merei FT, Gallyas F, Horvath Z (1980) Elastic elements in the media and adventitia of human intracranial extracerebral arteries. Stroke 11(4):329–336

    Article  CAS  PubMed  Google Scholar 

  26. Minoguchi K, Yokoe T, Tazaki T, Minoguchi H, Tanaka A, Oda N, Okada S, Ohta S, Naito H, Adachi M (2005) Increased carotid intima-media thickness and serum inflammatory markers in obstructive sleep apnea. Am J Respir Crit Care Med 172(5):625–630. doi:10.1164/rccm.200412-1652OC

    Article  PubMed  Google Scholar 

  27. Ovbiagele B, Lynn MJ, Saver JL, Chimowitz MI, Group WS (2007) Leukocyte count and vascular risk in symptomatic intracranial atherosclerosis. Cerebrovasc Dis 24(2–3):283–288. doi:10.1159/000105681

    Article  PubMed  Google Scholar 

  28. 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. doi:10.1016/j.smrv.2014.07.003

    Article  PubMed  Google Scholar 

  29. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95. doi:10.1152/physrev.00018.2001

    Article  CAS  PubMed  Google Scholar 

  30. Walters AS, Rye DB (2009) Review of the relationship of restless legs syndrome and periodic limb movements in sleep to hypertension, heart disease, and stroke. Sleep 32(5):589–597

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurology, Ewha Womans University School of Medicine, 1071 Anyangcheon-ro, Yangcheon-gu, Seoul, 07985, South Korea

    Tae-Jin Song, Jung-Hyun Park, Yoonkyung Chang, Hyeon Jin Kim, Jangsup Moon, Yong-Jae Kim & Hyang Woon Lee

  2. Department of Medical Science, Ewha Womans University School of Medicine, Seoul, South Korea

    Tae-Jin Song, Kang Hyun Choi, Ju-Hee Kim, Yunseo Choi, Jangsup Moon, Yong-Jae Kim & Hyang Woon Lee

  3. Ewha Medical Research Institute, Seoul, South Korea

    Kang Hyun Choi, Ju-Hee Kim, Yunseo Choi, Hyeon Jin Kim, Jangsup Moon & Hyang Woon Lee

Authors
  1. Tae-Jin Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jung-Hyun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kang Hyun Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ju-Hee Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yunseo Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoonkyung Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hyeon Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jangsup Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yong-Jae Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hyang Woon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hyang Woon Lee.

Ethics declarations

Funding

Tae-Jin Song provided financial support in the form of Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (2015R1D1A1A01057934) and grants of the Korean Society of Neurosonology and the Korean Neurological Associaiton. Kang Hyun Choi was supported by the Research Grant 2014 from Ewha Womans University. Hyang Woon Lee provided financial support in the form of Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (2014-R1A2A1A11052103) and Ministry of Education the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health and Welfare (HI14C1989).

The sponsor had no role in the design or conduct of this research.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Our study was approved by the Institutional Review Board of our hospital and observed strictly with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was waived due to the retrospective nature of study.

Electronic supplementary material

ESM 1

(DOCX 20 kb)

ESM 2

(DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, TJ., Park, JH., Choi, K.H. et al. Is obstructive sleep apnea associated with the presence of intracranial cerebral atherosclerosis?. Sleep Breath 21, 639–646 (2017). https://doi.org/10.1007/s11325-016-1450-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11325-016-1450-9

Keywords

Search

Navigation