Cerebral blood flow, sympathetic nerve activity and stroke risk in obstructive sleep apnoea. Is there a direct link?

Blood Pressure

Volumn 22, Issue 1, 2013, Pages 27-33

  Winklewski, Pawel J ^a   Frydrychowski, Andrzej F ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

Cerebral blood flow; Cerebral venous blood volume; Obstructive sleep apnoea; Pial artery; Stroke; Sympathetic nerve activity

Indexed keywords

ARTICLE; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; CEREBROVASCULAR ACCIDENT; HEMODYNAMICS; HUMAN; NERVE CONDUCTION; PATHOGENESIS; PRIORITY JOURNAL; SLEEP DISORDERED BREATHING; SYMPATHETIC NERVE;

BLOOD PRESSURE; BRAIN; CEREBRAL ARTERIES; CEREBROVASCULAR CIRCULATION; HEMODYNAMICS; HUMANS; RISK FACTORS; SLEEP APNEA, OBSTRUCTIVE; SLEEP, REM; STROKE; SYMPATHETIC NERVOUS SYSTEM;

EID: 84872240102     PISSN: 08037051     EISSN: 16511999     Source Type: Journal    
DOI: 10.3109/08037051.2012.701407     Document Type: Article

References (75)

1. Kernan WN, Lichtman JH, Brass LM, Mohsenin V. Obstructive sleep apnea as a risk factor for stroke and death . N Engl J Med. 2005; 353 : 2034 - 2041 .
2. Munoz R, D uran-Cantolla J, M art í nez-Vila E, G allego J, Rubio R, Aizpuru F, et al . Severe sleep apnea and risk of ischemic stroke in the elderly . Stroke. 2006; 37 : 2317 - 2321 .
3. Redline S, Y enokyan G, G ottlieb D J, Shahar E, O ' C onnor GT, Resnick HE, et al . Obstructive sleep apnea - hypopnea and incident stroke: The sleep heart health study . Am J Respir Crit Care Med. 2010; 182 : 269 - 277 .
4. Urbano F, Roux F, Schindler J, Mohsenin V. Impaired cerebral autoregulation in obstructive sleep apnea . J Appl Physiol. 2008; 105 : 1852 - 1857 .
5. Bå l fors EM, Franklin K A. I mpairment of cerebral perfusion during obstructive sleep apneas . Am J Respir Crit Care Med. 1994; 150 : 1587 - 1591 .
6. Klingelh öf er J, H ajak G, S ander D, S chulz-Varszegi M, R ü ther E, Conrad B. Assessment of intracranial hemodynamics in sleep apnea syndrome . Stroke. 1992; 23 : 1427 - 1433 .
7. Narkiewicz K, S omers V K. The sympathetic nervous system and obstructive sleep apnea: Implications for hypertension . J Hypertens. 1997; 15 : 1613 - 1619 .
8. Narkiewicz K, v an de Borne P J, M ontano N, D yken M E, Phillips BG, Somers VK. Contribution of tonic chemorefl ex activation to sympathetic activity and blood pressure in patients with obstructive sleep apnea . Circulation. 1998; 97 : 943 - 945 .
9. O goh S. Comments on Point:Counterpoint: Sympathetic activity does/does not infl uence cerebral blood fl ow. Autonomic nervous system infl uences dynamic cerebral blood fl ow . J Appl Physiol. 2008; 105 : 1370 .
10. Ogoh S, Ainslie PN. Cerebral blood fl ow during exercise: Mechanisms of regulation . J Appl Physiol. 2009; 107 : 1370 - 1380 .
11. Van Lieshout J J, S echer N H. P oint: Counterpoint: Sympathetic activity does/does not infl uence cerebral blood fl ow. Point: Sympathetic activity does infl uence cerebral blood fl ow . J Appl Physiol. 2008; 105 : 1364 - 1366 .
12. Heistad D D, M arcus M L. E ffect of sympathetic stimulation on permeability of the blood - brain barrier to albumin during acute hypertension in cats . Circ Res 1979; 45 : 331 - 338 .
13. Cassaglia P A, G riffi ths R I, W alker AM. S ympathetic nerve activity in the superior cervical ganglia increases in response to imposed increases in arterial pressure . Am J Physiol Regul Integr Comp Physiol. 2008; 294 : R1255 - R1261 .
14. Loos N, Grant DA, Wild J, Paul S, Barfi eld C, Zoccoli G, et al . Sympathetic nervous control of the cerebral circulation in sleep . J Sleep Res. 2005; 14 : 275 - 283 .
15. Cassaglia PA, Griffi ths RI, Walker AM. Cerebral sympathetic nerve activity has a major regulatory role in the cerebral circulation in REM sleep . J Appl Physiol. 2009; 106 : 1050 - 1056 .
16. Bhambhani Y, M aikala R, F arag M, R owland G. R eliability of near-infrared spectroscopy measures of cerebral oxygenation and blood volume during handgrip exercise in nondisabled and traumatic brain-injured subjects . J Rehabil Res Dev. 2006; 43 : 845 - 856 .
17. Ogoh S, Sato K, Fisher JP, Seifert T, Overgaard M, Secher NH. The effect of phenylephrine on arterial and venous cerebral blood fl ow in healthy subjects . Clin Physiol Funct Imaging. 2011; 31 : 445 - 451 .
18. Wszedybyl-Winklewska M, F rydrychowski AF, W inklewski P J. Assessing changes in pial artery resistance and subarachnoid space width using a non-invasive method in healthy humans during the handgrip test . Acta Neurobiol Exp. 2012; 72 : 80 - 88 .
19. Edvinsson L, McCulloch J, Uddman R. Feline cerebral veins and arteries: Comparison of autonomic innervation and vasomotor responses . J Physiol. 1982; 325 : 161 - 173 .
20. Gulbenkian S, U ddman R, E dvinsson L. N euronal messengers in the human cerebral circulation . Peptides. 2001; 22 : 995 - 1007 .
21. Arbab MA, Wiklund L, Svendgaard NA. Origin and distribution of cerebral vascular innervation from superior cervical, trigeminal and spinal ganglia investigated with retrograde and anterograde WGA-HRP tracing in the rat . Neuroscience. 1986; 19 : 695 - 708.
22. Cuevas P, Gutierrez-Diaz JA, Reimers D, Dujovny M, Diaz FG, Ausman JI. Adrenergic innervation of human middle cerebral artery . Ultrastructural observations. Surg Neurol. 1987; 27 : 113 - 116 .
23. Edvinsson L, Owman C. P harmacological characterization of adrenergic alpha and beta receptors mediating the vasomotor responses of cerebral arteries in vitro . Circ Res. 1974; 35 : 835 - 849 .
24. Frydrychowski AF, Wszedybyl-Winklewska M, Guminski W, Przyborska A, Kaczmarek J, Winklewski PJ. Use of near infrared transillumination/back scattering sounding (NIR-T/BSS) to assess effects of elevated intracranial pressure on width of subarachnoid space and cerebrovascular pulsation in animals . Acta Neurobiol Exp. 2011; 71 : 313 - 321 .
25. Lee TJ, Su C, Bevan JA. Neurogenic sympathetic vasoconstriction of the rabbit basilar artery . Circ Res. 1976; 39 : 120 - 126 .
26. Roatta S, Canova D, Bosone D, Micieli G, Passatore M. Noradrenergic constriction of cerebral arteries as detected by transcranial Doppler (TCD) in the rabbit . Ultrasound Med Biol. 2003; 29 : 1397 - 1404 .
27. Visocchi M, Chiappini F, Cioni B, Meglio M. Cerebral blood fl ow velocities and trigeminal ganglion stimulation. A transcranial Doppler study . Stereotact Funct Neurosurg. 1996; 66 : 184 - 192 .
28. Giller CA. T he Emperor has no clothes: Velocity, fl ow, and the use of TCD. J Neuroimaging. 2003; 13 : 97 - 98 .
29. Lunt MJ, Ragab S, Birch AA, Schley D, Jenkinson DF. Comparison of caffeine-induced changes in cerebral blood fl ow and middle cerebral artery blood velocity shows that caffeine reduces middle cerebral artery diameter . Physiol Meas. 2004; 25 : 467 - 474
30. Wilson MH, Eds ell ME, Davagnanam I, Hirani SP, Martin DS, Levett DZ, et al.; Caudwell Xtreme Everest Research Group . Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia - An ultrasound and MRI study . J Cereb Blood Flow Metab. 2011; 31 : 2019 - 2029 .
31. Brassard P, Seifert T, Secher NH. Is cerebral oxygenation negatively affected by infusion of norepinephrine in healthy subjects? Br J Anaesth. 2009; 102 : 800 - 805 .
32. Brassard P, Seifert T, Wissenberg M, Jensen PM, Hansen CK, Secher NH. Phenylephrine decreases frontal lobe oxygenation at rest but not during moderately intense exercise . J Appl Physiol. 2010; 108 : 1472 - 1478 .
33. Nissen P, Brassard P, J ø r gensen TB, S echer N H. P henylephrine but not ephedrine reduces frontal lobe oxygenation following anesthesia-induced hypotension . Neurocrit Care. 2010; 12 : 17 - 23 .
34. Lucas SJ, T zeng YC, Galvin SD, T homas KN, Ogoh S, Ainslie PN. Infl uence of changes in blood pressure on cerebral perfusion and oxygenation . Hypertension. 2010; 55 : 698 - 705 .
35. Sato K, S adamoto T. D ifferent blood fl ow responses to dynamic exercise between internal carotid and vertebral arteries in women . J Appl Physiol. 2010; 109 : 864 - 869 .
36. Ainslie PN, A shmead JC, Ide K, Morgan BJ, Poulin MJ. Differential responses to CO 2 and sympathetic stimulation in the cerebral and femoral circulations in humans . J Physiol. 2005; 566 : 613 - 624 .
37. Ikemura T, Someya N, Hayashi N. A utoregulation in the ocular and cerebral arteries during the cold pressor test. and handgrip exercise . Eur J Appl Physiol . 2011; DOI: 10.1007/ s00421-011-2016-y.
38. Sohn YH. Cerebral hemodynamic changes induced by sympathetic stimulation tests . Yonsei Med J. 1998; 39 : 322 - 327 .
39. Rasmussen P, Plomgaard P, Krogh-Madsen R, Kim YS, van Lieshout JJ, Secher NH, et al . MCA Vmean and the arterial lactate-to-pyruvate ratio correlate during rhythmic handgrip . J Appl Physiol. 2006; 101 : 1406 - 1411 .
40. Seifert T, F isher J P, Y oung C N, H artwich D, O goh S, Raven PB, et al . Glycopyrrolate abolishes the exercise-induced increase in cerebral perfusion in humans . Exp Physiol. 2010; 95 : 1016 - 1025 .
41. Johansson B, Li CL, Olsson Y, Klatzo I. The effect of acute arterial hypertension on the blood - brain barrier to protein tracers . Acta Neuropathol. 1970; 16 : 117 - 124 .
42. Somers V K, D yken M E, M ark AL, Abboud FM. S ympatheticnerve activity during sleep in normal subjects . N Engl J Med. 1993; 328 : 303 - 307 .
43. Somers V K, D yken M E, C lary M P, Abboud F M. S ympathetic neural mechanisms in obstructive sleep apnea . J Clin Invest. 1995; 96 : 1897 - 1904 .
44. LeMarbre G, Stauber S, Khayat RN, Puleo DS, Skatrud JB, Morgan BJ. Barorefl ex-induced sympathetic activation does not alter cerebrovascular CO 2 responsiveness in humans . J Physiol. 2003; 551 : 609 - 616 .
45. Wilson T D, S hoemaker J K, K ozak R, L ee T Y, G elb AW. Refl ex-mediated reduction in human cerebral blood volume . J Cereb Blood Flow Metab. 2005; 25 : 136 - 143 .
46. Traystman RJ, Rapela CE. Effect of sympathetic nerve stimulation on cerebral and cephalic blood fl ow in dogs . Circ Res. 1975; 36 : 620 - 630 .
47. Ulrich K, K uschinsky W . In vivo effects of alpha-adrenoceptor agonists and antagonists on pial veins of cats . Stroke. 1985; 16 : 880 - 884 .
48. Brown W R, M oody D M, Thore C R, Anstrom J A, C halla V R. Microvascular changes in the white mater in dementia . J Neurol Sci. 2009; 283 : 28 - 31 .
49. Nation DA, Hong S, Jak A J, Delano-Wood L, Mills PJ, Bondi MW, et al . Stress, exercise, and Alzheimer ' s disease: A neurovascular pathway . Med Hypotheses. 2011; 76 : 847 - 854 .
50. Kontos HA, Wei EP, Navari RM, Levasseur JE, Rosenblum WI, Patterson JL Jr . Responses of cerebral arteries and arterioles to acute hypotension and hypertension . Am J Physiol. 1978; 234 : H371 - H383 .
51. Narayanan N, Leffl er CW, Daley ML. Infl uence of hypercapnic vasodilation on cerebrovascular autoregulation and pial arteriolar bed resistance in piglets . J Appl Physiol. 2008; 105 : 152 - 157 .
52. Kagstrom E, Smith ML, Siesjo BK. Cerebral circulatory responses to hypercapnia and hypoxia in the recovery period following complete and incomplete cerebral ischemia in the rat . Acta Physiol Scand. 1983; 118 : 281 - 291 .
53. Vorstrup S, Henriksen L, Paulson OB. Effect of acetazolamide on cerebral blood fl ow and cerebral metabolic rate for oxygen . J Clin Invest. 1984; 74 : 1634 - 1639 .
54. Brian JE J r. C arbon dioxide and the cerebral circulation. Anesthesiology. 1998; 88 : 1365 - 1386 .
55. Domoki F, Z immermann A, T ót h-Szuki V, B usija D W, Bari F. Acetazolamide induces indomethacin and ischaemiasensitive pial arteriolar vasodilation in the piglet . Acta Paediatr. 2008; 97 : 280 - 284 .
56. Frydrychowski A F, Rojewski M, Guminski W, Kaczmarek J, Juzwa W. Technical foundation for non-invasive assessment of changes in the width of the subarachnoid space with near-infrared transillumination-back scattering sounding (NIR-TBSS) . IEEE Trans Biomed Eng. 2002; 49 : 887 - 904 .
57. Frydrychowski AF, Wszedybyl-Winklewska M, Bandurski T, Winklewski PJ. Flow-induced changes in pial artery compliance registered with a non-invasive method in rabbits . Microvasc Res. 2011; 82 : 156 - 162 .
58. Frydrychowski AF, Wszedybyl-Winklewska M, Guminski W, Lass P, Bandurski T, Winklewski PJ. Effects of acute hypercapnia on the amplitude of cerebrovascular pulsation in humans registered with a non-invasive method . Microvasc Res. 2012; 83 : 229 - 236 .
59. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans . Stroke. 1989; 20 : 45 - 52 .
60. Birch AA, Dirnhuber MJ, Hartley-Davies R, Iannotti F, Neil-Dwyer G. Assessment of autoregulation by means of periodic changes in blood pressure . Stroke. 1995; 26 : 834 - 837 .
61. Panerai R B. Assessment of cerebral pressure autoregulation in humans - A review of measurement methods . Physiol Meas. 1998; 19 : 305 - 338 .
62. Zhang R, Zuckerman JH, Giller CA, Levine BD. Transfer function analysis of dynamic cerebral autoregulation in humans . Am J Physiol. 1998; 274 : H233 - H241 .
63. Ainslie P N, Celi L, McGrattan K, Peebles K, Ogoh S. Dynamic cerebral autoregulation and barorefl ex sensitivity during modest and severe step changes in arterial PCO 2 . Brain Res. 2008; 1230 : 115 - 124 .
64. Jordan J, S hannon J R, D iedrich A, Black B, C osta F, Robertson D, et al . Interaction of carbon dioxide and sympathetic nervous system activity in the regulation of cerebral perfusion in humans . Hypertension. 2000; 36 : 383 - 388 .
65. Przybył owski T, Bangash MF, Reichmuth K, Morgan BJ, Skatrud JB, Dempsey JA. Mechanisms of the cerebrovascular response to apnoea in humans . J Physiol. 2003; 548 : 323 - 332 .
66. D ujic Z, U glesic L, B reskovic T, V alic Z, H eusser K, Marinovic J, et al . Involuntary breathing movements improve cerebral oxygenation during apnea struggle phase in elite divers . J Appl Physiol. 2009; 107 : 1840 - 1846 .
67. Cassaglia P A, G riffi ths R I, W alker AM. S ympathetic withdrawal augments cerebral blood fl ow during acute hypercapnia in sleeping lambs . Sleep. 2008; 31 : 1729 - 1734 .
68. Hayakawa T, T erashima M, Kayukawa Y, Ohta T, Okada T. Changes in cerebral oxygenation and hemodynamics during obstructive sleep apneas . Chest. 1996; 109 : 916 - 921 .
69. Valipour A, McGown AD, Makker H, O' S ullivan C, Spiro SG. Some factors affecting cerebral tissue saturation during obstructive sleep apnoea . Eur Respir J. 2002; 20 : 444 - 450 .
70. Placidi F, D iomedi M, C upini L M, B ernardi G, S ilvestrini M. Impairment of daytime cerebrovascular reactivity in patients with obstructive sleep apnoea syndrome . J Sleep Res. 1998; 7 : 288 - 292 .
71. Reichmuth KJ, Dopp JM, Barczi SR, Skatrud JB, Wojdyla P, Hayes D Jr, et al . Impaired vascular regulation in patients with obstructive sleep apnea: Effects of continuous positive airway pressure treatment . Am J Respir Crit Care Med. 2009; 180 : 1143 - 1150 .
72. Morgan BJ, Reichmuth KJ, P eppard P E, F inn L, B arczi S R, Young T, et al . Effects of sleep-disordered breathing on cerebrovascular regulation: A population-based study . Am J Respir Crit Care Med. 2010; 182 : 1445 - 1452 .
73. Sugita Y, I ijima S, T eshima Y, S himizu T, N ishimura N, Tsutsumi T, et al . Marked episodic elevation of cerebrospinal fl uid pressure during nocturnal sleep in patients with sleep apnea hypersomnia syndrome . Electroencephalogr Clin Neurophysiol. 1985; 60 : 214 - 219 .
74. Jennum P, B ø r gesen S E. Intracranial pressure and obstructive sleep apnea . Chest. 1989; 95 : 279 - 283 .
75. Parati G, Lombardi C, Hedner J, Bonsignore MR, Grote L, Tkacova R, et al.; European Respiratory Society; EU COST ACTION B26 members. Position paper on the management of patients with obstructive sleep apnea and hypertension: Joint recommendations by the European Society of Hypertension, by the European Respiratory Society and by the members of European COST (CO-operation in Scientifi c and Technological research) ACTION B26 on obstructive sleep apnea . J Hypertens . 2012; 30 : 633 - 646 .