Top

Published in:

01-12-2018 | Original Article

The association of sleep-disordered breathing and white matter hyperintensities in heart failure patients

Authors: Chooza Moon, Barbara B. Bendlin, Kelsey E. Melah, Lisa C. Bratzke

Published in: Metabolic Brain Disease | Issue 6/2018

Abstract

Heart failure patients often manifest white matter hyperintensites on brain magnetic resonance imaging (MRI). White matter hyperintnsities have also been linked with cognitive problems in patients with heart failure. Sleep disordered breathing may contribute to structural brain changes in heart failure. The purpose of this study was to test the extent to which the apnea hypopnea index is associated with global and regional white matter hyperintensities, and is a moderating factor in the relationship between age and white matter hyperintensites. A total of 28 HF patients [mean age (SD) = 67.89 (5.8)] underwent T1-weighted and T2FLAIR MRI and a home sleep monitoring study. The apnea hypopnea index cut off of 10 was used to compare between higher and lower risks of sleep disordered breathing. Regression analysis was used to test the association between apnea hypopnea index and both global and regional white matter hyperintensities. The interaction term was entered to identify the moderation effect. Apnea hypopnea index was associated with higher regional white matter hyperintensities but not global white matter hyperintensities. There was a significant interaction between the apnea hypopnea index and age, such that older participants with the apnea hypopnea index ≥10 showed greater regional white matter hyperintensities than those with the apnea hypopnea index <10. The results of this preliminary study indicate that a higher apnea hypopnea index is associated with more white matter hyperintensities. The age-related white matter hyperintensities appear to be exacerbated by apnea hypopnea index in our individuals with heart failure. Future studies are needed to further investigate the underlying mechanisms.

Alosco ML, Brickman AM, Spitznagel MB, Garcia SL, Narkhede A, Griffith EY, Raz N, Cohen R, Sweet LH, Colbert LH, Josephson R, Hughes J, Rosneck J, Gunstad J (2013a) Cerebral perfusion is associated with white matter hyperintensities in older adults with heart failure. Congest Heart Fail Greenwich Conn 19(4):E29–E34. https://doi.org/10.1111/chf.12025 CrossRef

Alosco ML, Brickman AM, Spitznagel MB, Griffith EY, Narkhede A, Raz N, Cohen R, Sweet LH, Hughes J, Rosneck J, Gunstad J (2013b) Independent and interactive effects of blood pressure and cardiac function on brain volume and white matter hyperintensities in heart failure. J Am Soc Hypertens 7(5):336–343. https://doi.org/10.1016/j.jash.2013.04.011 CrossRefPubMedPubMedCentral

Avci AY, Avci S, Lakadamyali H, Can U (2017) Hypoxia and inflammation indicate significant differences in the severity of obstructive sleep apnea within similar apnea-hypopnea index groups. Sleep Breath 21(3):703–711. https://doi.org/10.1007/s11325-017-1486-5 CrossRefPubMed

Bauer L, Pozehl B (2011) Measurement of cognitive function in chronic heart failure: a feasibility study. Appl Nurs Res 24(4):223–228. https://doi.org/10.1016/j.apnr.2009.12.002 CrossRefPubMed

Bauer L, Johnson JK, Pozehl BJ (2011) Cognition in heart failure: an overview of the concepts and their measures. J Am Acad Nurse Pract 23(11):577–585. https://doi.org/10.1111/j.1745-7599.2011.00668.x CrossRefPubMedPubMedCentral

Bellesi M, de Vivo L, Chini M, Gilli F, Tononi G, Cirelli C (2017) Sleep loss promotes Astrocytic phagocytosis and microglial activation in mouse cerebral cortex. J Neurosci 37(21):5263–5273. https://doi.org/10.1523/JNEUROSCI.3981-16.2017 CrossRefPubMedPubMedCentral

Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, Isasi CR, Jiménez MC, Jordan LC, Judd SE, Lackland D, Lichtman JH, Lisabeth L, Liu S, Longenecker CT, Mackey RH, Matsushita K, Mozaffarian D, Mussolino ME, Nasir K, Neumar RW, Palaniappan L, Pandey DK, Thiagarajan RR, Reeves MJ, Ritchey M, Rodriguez CJ, Roth GA, Rosamond WD, Sasson C, Towfighi A, Tsao CW, Turner MB, Virani SS, Voeks JH, Willey JZ, Wilkins JT, Wu JHY, Alger HM, Wong SS, Muntner P (2017) Heart disease and stroke Statistics-2017 update: a report from the American Heart Association. Circulation 135(10):e146–e603. https://doi.org/10.1161/CIR.0000000000000485 CrossRefPubMedPubMedCentral

Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, Redline S, Strohl KP, Ward SLD, Tangredi MM (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 JCSM Off Publ Am Acad Sleep Med 8(5):597–619. https://doi.org/10.5664/jcsm.2172 CrossRef

Birdsill AC, Koscik RL, Jonaitis EM, Johnson SC, Okonkwo OC, Hermann BP, LaRue A, Sager MA, Bendlin BB (2014) Regional white matter hyperintensities: aging, Alzheimer’s disease risk, and cognitive function. Neurobiol Aging 35(4):769–776. https://doi.org/10.1016/j.neurobiolaging.2013.10.072 CrossRefPubMed

Bratzke-Bauer LC, Pozehl BJ, Paul SM, Johnson JK (2013) Neuropsychological patterns differ by type of left ventricle dysfunction in heart failure. Arch Clin Neuropsychol 28(2):114–124. https://doi.org/10.1093/arclin/acs101 CrossRefPubMed

Chen H, Lowe AA, Bai Y, Hamilton P, Fleetham JA, Almeida FR (2009) Evaluation of a portable recording device (ApneaLink) for case selection of obstructive sleep apnea. Sleep Breath Schlaf Atm 13(3):213–219. https://doi.org/10.1007/s11325-008-0232-4 CrossRef

Chen H-L, Lu C-H, Lin H-C, Chen PC, Chou KH, Lin WM, Tsai NW, Su YJ, Friedman M, Lin CP, Lin WC (2015) White matter damage and systemic inflammation in obstructive sleep apnea. Sleep 38(3):361–370. https://doi.org/10.5665/sleep.4490 CrossRefPubMedPubMedCentral

Collop NA, Anderson WM, Boehlecke B et al (2007) Clinical guidelines for the use of unattended portable monitors in the diagnosis of obstructive sleep apnea in adult patients. Portable monitoring task force of the American Academy of sleep medicine. J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med 3(7):737–747

De Groot JC, de Leeuw F-E, Oudkerk M et al Cerebral white matter lesions and cognitive function: The Rotterdam scan study. Ann Neurol 47(2):145–151. https://doi.org/10.1002/1531-8249(200002)47:2<145::AID-ANA3>3.0.CO;2-P

de Leeuw F-E, Richard F, de GJC et al (2004) Interaction between hypertension, apoE, and cerebral white matter lesions. Stroke 35(5):1057–1060. https://doi.org/10.1161/01.STR.0000125859.71051.83 CrossRefPubMed

Debette S, Markus HS (2010) The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ 341. https://doi.org/10.1136/bmj.c3666 CrossRefPubMedPubMedCentral

Ding N, Ni B-Q, Zhang X-L, Huang HP, Su M, Zhang SJ, Wang H (2013) Prevalence and risk factors of sleep disordered breathing in patients with rheumatic valvular heart disease. J Clin Sleep Med 9(8):781–787. https://doi.org/10.5664/jcsm.2920 CrossRefPubMedPubMedCentral

Garde E, Mortensen EL, Krabbe K, Rostrup E, Larsson HB (2000) Relation between age-related decline in intelligence and cerebral white-matter hyperintensities in healthy octogenarians: a longitudinal study. Lancet 356(9230):628–634. https://doi.org/10.1016/S0140-6736(00)02604-0 CrossRefPubMed

Hjelm C, Strömberg A, Arestedt K, Broström A (2013) Association between sleep-disordered breathing, sleep-wake pattern, and cognitive impairment among patients with chronic heart failure. Eur J Heart Fail 15(5):496–504. https://doi.org/10.1093/eurjhf/hft014 CrossRefPubMed

Kasai T, Bradley TD (2011) Obstructive sleep apnea and heart failure: Pathophysiologic and Therapeutic Implications. J Am Coll Cardiol 57(2):119–127. https://doi.org/10.1016/j.jacc.2010.08.627 CrossRefPubMed

Keihaninejad S, Heckemann RA, Fagiolo G, Symms MR, Hajnal JV, Hammers A (2010) A robust method to estimate the intracranial volume across MRI field strengths (1.5T and 3T). NeuroImage 50(4):1427–1437. https://doi.org/10.1016/j.neuroimage.2010.01.064 CrossRefPubMed

Kibble JD, Halsey CR. Cardiovascular physiology. In: Medical Physiology: The Big Picture. New York, NY: McGraw-hill education; 2015. Accessmedicine.mhmedical.com/content.aspx?aid=1106602247. Accessed September 27, 2017

Kiernan T-EJ, Capampangan DJ, Hickey MG, Pearce LA, Aguilar MI (2011) Sleep apnea and white matter disease in hypertensive patients: a case series. Neurologist 17(5):289–291. https://doi.org/10.1097/NRL.0b013e31821a25d6 CrossRefPubMed

Kim H, Yun C-H, Thomas R (2013) Joseph, et al. obstructive sleep apnea as a risk factor for cerebral white matter change in a middle-aged and older general population. Sleep 36(5):709–715. https://doi.org/10.5665/sleep.2632 CrossRefPubMedPubMedCentral

Kim LJ, Martinez D, Fiori CZ, Baronio D, Kretzmann NA, Barros HMT (2015) Hypomyelination, memory impairment, and blood–brain barrier permeability in a model of sleep apnea. Brain Res 1597(Supplement C):28–36. https://doi.org/10.1016/j.brainres.2014.11.052 CrossRefPubMed

Kryger MH, Roth T, Dement, WC. Principles and Practice of Sleep Medicine. 5 edition. Saunders; 2010

Kumar R, Woo MA, Macey PM, Fonarow GC, Hamilton MA, Harper RM (2011) Brain axonal and myelin evaluation in heart failure. J Neurol Sci 307(1–2):106–113. https://doi.org/10.1016/j.jns.2011.04.028 CrossRefPubMedPubMedCentral

Launer LJ (2004) Epidemiology of white matter lesions. Top Magn Reson Imaging TMRI 15(6):365–367CrossRefPubMed

Lutsey PL, Norby FL, Gottesman RF, Mosley T, MacLehose RF, Punjabi NM, Shahar E, Jack CR, Alonso A (2016) Sleep apnea, sleep duration and brain MRI markers of cerebral vascular disease and Alzheimer’s disease: the atherosclerosis risk in communities study (ARIC). PLoS One 11(7). https://doi.org/10.1371/journal.pone.0158758 CrossRefPubMedPubMedCentral

Macey PM, Kumar R, Woo MA, Valladares EM, Yan-Go FL, Harper RM (2008) Brain structural changes in obstructive sleep apnea. Sleep 31(7):967–977PubMedPubMedCentral

Melah K, Moon C, Johnson SC, Bratzke LC (2015) Abstract 18696: regional distribution of cerebral white matter Hyperintensities in HFrEF and HFpEF. Circulation 132(Suppl 3):A18696–A18696

Melah KE, Jankowski B, Moon C, Rivera LA, Wieben O, Johnson SC, Bratzke LC (2016) Reduced middle cerebral artery blood flow is associated with decrements in executive function, attention, and verbal learning and memory in aging individuals with heart failure: a 4D flow MRI study. Alzheimers Dement 12(7, Supplement):P950–P952. https://doi.org/10.1016/j.jalz.2016.06.1954 CrossRef

Minoguchi K, Yokoe T, Tazaki T, Minoguchi H, Oda N, Tanaka A, Yamamoto M, Ohta S, O'Donnell CP, Adachi M (2007) Silent brain infarction and platelet activation in obstructive sleep apnea. Am J Respir Crit Care Med 175(6):612–617. https://doi.org/10.1164/rccm.200608-1141OC CrossRefPubMed

Nair D, Dayyat EA, Zhang SX, Wang Y, Gozal D (2011) Intermittent hypoxia-induced cognitive deficits are mediated by NADPH oxidase activity in a murine model of sleep apnea. PLoS One 6(5):e19847. https://doi.org/10.1371/journal.pone.0019847 CrossRefPubMedPubMedCentral

Nishibayashi M, Miyamoto M, Miyamoto T, Suzuki K, Hirata K (2008) Correlation between severity of obstructive sleep apnea and prevalence of silent cerebrovascular lesions. J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med 4(3):242–247

Oktay B, Rice TB, Atwood CW Jr et al (2011) Evaluation of a single-channel portable monitor for the diagnosis of obstructive sleep apnea. J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med 7(4):384–390. https://doi.org/10.5664/JCSM.1196 CrossRef

Pae E-K, Chien P, Harper RM (2005) Intermittent hypoxia damages cerebellar cortex and deep nuclei. Neurosci Lett 375(2):123–128. https://doi.org/10.1016/j.neulet.2004.10.091 CrossRefPubMed

Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9(7):689–701. https://doi.org/10.1016/S1474-4422(10)70104-6 CrossRefPubMed

Patel SK, Hanly PJ, Smith EE, Chan W, Coutts SB (2015) Nocturnal Hypoxemia is Associated with white matter Hyperintensities in patients with a minor stroke or transient ischemic attack. J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med 11(12):1417–1424. https://doi.org/10.5664/jcsm.5278 CrossRef

Polotsky VY, Rubin AE, Balbir A et al (2006) Intermittent hypoxia causes REM sleep deficits and decreases EEG delta power in NREM sleep in the C57BL/6J mouse. Sleep Med 7(1):7–16. https://doi.org/10.1016/j.sleep.2005.06.006 CrossRefPubMed

Pressler SJD (2008) Cognitive functioning and chronic heart failure: a review of the literature (2002-July 2007). J Cardiovasc Nurs May 23(3):239–249. https://doi.org/10.1097/01.JCN.0000305096.09710.ec CrossRef

Pressler SJ, Subramanian U, Kareken D, Perkins SM, Gradus-Pizlo I, Sauvé MJ, Ding Y, Kim JS, Sloan R, Jaynes H, Shaw RM (2010) Cognitive deficits in chronic heart failure. Nurs Res 59(2):127–139. https://doi.org/10.1097/NNR.0b013e3181d1a747 CrossRefPubMedPubMedCentral

Ragette R, Wang Y, Weinreich G, Teschler H (2010) Diagnostic performance of single airflow channel recording (ApneaLink) in home diagnosis of sleep apnea. Sleep Breath Schlaf Atm 14(2):109–114. https://doi.org/10.1007/s11325-009-0290-2 CrossRef

Rivera-Rivera LA, Schubert T, Turski P, Johnson KM, Berman SE, Rowley HA, Carlsson CM, Johnson SC, Wieben O (2016) Changes in intracranial venous blood flow and pulsatility in Alzheimer’s disease: a 4D flow MRI study. In: J Cereb blood flow Metab off J Int Soc Cereb blood flow Metab, vol 37, pp 2149–2158. https://doi.org/10.1177/0271678X16661340 CrossRef

Sapin E, Peyron C, Roche F, Gay N, Carcenac C, Savasta M, Levy P, Dematteis M (2015) Chronic intermittent hypoxia induces chronic low-grade Neuroinflammation in the dorsal Hippocampus of mice. Sleep 38(10):1537–1546. https://doi.org/10.5665/sleep.5042 CrossRefPubMedPubMedCentral

Schmidt P, Gaser C, Arsic M, Buck D, Förschler A, Berthele A, Hoshi M, Ilg R, Schmid VJ, Zimmer C, Hemmer B, Mühlau M (2012) An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. NeuroImage 59(4):3774–3783. https://doi.org/10.1016/j.neuroimage.2011.11.032 CrossRefPubMed

Sharma S, Mather PJ, Chowdhury A, Gupta S, Mukhtar U, Willes L, Whellan DJ, Malhotra A, Quan SF (2017) Sleep overnight monitoring for apnea in patients hospitalized with heart failure (SOMA-HF study). J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med 13(10):1185–1190. https://doi.org/10.5664/jcsm.6768 CrossRef

Veasey SC, Lear J, Zhu Y, Grinspan JB, Hare DJ, Wang SH, Bunch D, Doble PA, Robinson SR (2013) Long-term intermittent hypoxia elevates cobalt levels in the brain and injures white matter in adult mice. Sleep 36(10):1471–1481. https://doi.org/10.5665/sleep.3038 CrossRefPubMedPubMedCentral

Vogels RLC, Oosterman JM, van Harten B, Gouw AA, Schroeder-Tanka JM, Scheltens P, van der Flier WM, Weinstein HC (2007) Neuroimaging and correlates of cognitive function among patients with heart failure. Dement Geriatr Cogn Disord 24(6):418–423. https://doi.org/10.1159/000109811 CrossRefPubMed

Woo MA, Macey PM, Fonarow GC, Hamilton MA, Harper RM (2003) Regional brain gray matter loss in heart failure. J Appl Physiol Bethesda Md 1985 95(2):677–684. https://doi.org/10.1152/japplphysiol.00101.2003 CrossRef

Woo MA, Kumar R, Macey PM, Fonarow GC, Harper RM (2009) Brain injury in autonomic, emotional, and cognitive regulatory areas in patients with heart failure. J Card Fail 15(3):214–223. https://doi.org/10.1016/j.cardfail.2008.10.020 CrossRefPubMed

Xu W, Chi L, Row BW, Xu R, Ke Y, Xu B, Luo C, Kheirandish L, Gozal D, Liu R (2004) Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea. Neuroscience 126(2):313–323. https://doi.org/10.1016/j.neuroscience.2004.03.055 CrossRefPubMed

Ylikoski A, Erkinjuntti T, Raininko R, Sarna S, Sulkava R, Tilvis R (1995) White matter hyperintensities on MRI in the neurologically nondiseased elderly. Analysis of cohorts of consecutive subjects aged 55 to 85 years living at home. Stroke J Cereb Circ 26(7):1171–1177CrossRef

Yuan L, Wu J, Liu J, Li G, Liang D (2015) Intermittent hypoxia-induced Parvalbumin-Immunoreactive interneurons loss and neurobehavioral impairment is mediated by NADPH-Oxidase-2. Neurochem Res 40(6):1232–1242. https://doi.org/10.1007/s11064-015-1586-1 CrossRefPubMed

Zuccalà G, Pedone C, Cesari M, onder G, Pahor M, Marzetti E, Lo Monaco MR, Cocchi A, Carbonin P, Bernabei R (2003) The effects of cognitive impairment on mortality among hospitalized patients with heart failure. Am J Med 115(2):97–103CrossRefPubMed

Title: The association of sleep-disordered breathing and white matter hyperintensities in heart failure patients
Authors: Chooza Moon
Barbara B. Bendlin
Kelsey E. Melah
Lisa C. Bratzke
Publication date: 01-12-2018
Publisher: Springer US
Published in: Metabolic Brain Disease / Issue 6/2018
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-018-0309-0

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The association of sleep-disordered breathing and white matter hyperintensities in heart failure patients

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2018

L-3-n-Butylphthalide reduces ischemic stroke injury and increases M2 microglial polarization

Contemporary scope of inborn errors of metabolism involving epilepsy or seizures

Gradual common carotid artery occlusion as a novel model for cerebrovascular Hypoperfusion

Correction to: Therapeutic effects of probiotics on neurotoxicity induced by clindamycin and propionic acid in juvenile hamsters

Correlation of PICALM polymorphism rs3851179 with Alzheimer’s disease among Caucasian and Chinese populations: a meta-analysis and systematic review

Mitochondrial alterations accompanied by oxidative stress conditions in skin fibroblasts of Huntington’s disease patients