Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia--an ultrasound and MRI study

Mark H Wilson, Mark E G Edsell, Indran Davagnanam, Shashivadan P Hirani, Dan S Martin, Denny Z H Levett, John S Thornton, Xavier Golay, Lisa Strycharczuk, Stanton P Newman, Hugh E Montgomery, Mike P W Grocott, Christopher H E Imray, Caudwell Xtreme Everest Research Group, V Ahuja, G Aref-Adib, R Burnham, A Chisholm, K Clarke, D Coates, M Coates, D Cook, M Cox, S Dhillon, C Dougall, P Doyle, P Duncan, M Edsell, L Edwards, L Evans, P Gardiner, M Grocott, P Gunning, N Hart, J Harrington, J Harvey, C Holloway, D Howard, D Hurlbut, C Imray, C Ince, M Jonas, J van der Kaaij, M Khosravi, N Kolfschoten, D Levett, H Luery, A Luks, D Martin, R McMorrow, P Meale, K Mitchell, H Montgomery, G Morgan, J Morgan, A Murray, M Mythen, S Newman, M O'Dwyer, J Pate, T Plant, M Pun, P Richards, A Richardson, G Rodway, J Simpson, C Stroud, M Stroud, J Stygal, B Symons, P Szawarski, A Van Tulleken, C Van Tulleken, A Vercueil, L Wandrag, M Wilson, J Windsor, B Basnyat, C Clarke, T Hornbein, J Milledge, J West, Mark H Wilson, Mark E G Edsell, Indran Davagnanam, Shashivadan P Hirani, Dan S Martin, Denny Z H Levett, John S Thornton, Xavier Golay, Lisa Strycharczuk, Stanton P Newman, Hugh E Montgomery, Mike P W Grocott, Christopher H E Imray, Caudwell Xtreme Everest Research Group, V Ahuja, G Aref-Adib, R Burnham, A Chisholm, K Clarke, D Coates, M Coates, D Cook, M Cox, S Dhillon, C Dougall, P Doyle, P Duncan, M Edsell, L Edwards, L Evans, P Gardiner, M Grocott, P Gunning, N Hart, J Harrington, J Harvey, C Holloway, D Howard, D Hurlbut, C Imray, C Ince, M Jonas, J van der Kaaij, M Khosravi, N Kolfschoten, D Levett, H Luery, A Luks, D Martin, R McMorrow, P Meale, K Mitchell, H Montgomery, G Morgan, J Morgan, A Murray, M Mythen, S Newman, M O'Dwyer, J Pate, T Plant, M Pun, P Richards, A Richardson, G Rodway, J Simpson, C Stroud, M Stroud, J Stygal, B Symons, P Szawarski, A Van Tulleken, C Van Tulleken, A Vercueil, L Wandrag, M Wilson, J Windsor, B Basnyat, C Clarke, T Hornbein, J Milledge, J West

Abstract

Transcranial Doppler is a widely used noninvasive technique for assessing cerebral artery blood flow. All previous high altitude studies assessing cerebral blood flow (CBF) in the field that have used Doppler to measure arterial blood velocity have assumed vessel diameter to not alter. Here, we report two studies that demonstrate this is not the case. First, we report the highest recorded study of CBF (7,950 m on Everest) and demonstrate that above 5,300 m, middle cerebral artery (MCA) diameter increases (n=24 at 5,300 m, 14 at 6,400 m, and 5 at 7,950 m). Mean MCA diameter at sea level was 5.30 mm, at 5,300 m was 5.23 mm, at 6,400 m was 6.66 mm, and at 7,950 m was 9.34 mm (P<0.001 for change between 5,300 and 7,950 m). The dilatation at 7,950 m reversed with oxygen. Second, we confirm this dilatation by demonstrating the same effect (and correlating it with ultrasound) during hypoxia (FiO(2)=12% for 3 hours) in a 3-T magnetic resonance imaging study at sea level (n=7). From these results, we conclude that it cannot be assumed that cerebral artery diameter is constant, especially during alterations of inspired oxygen partial pressure, and that transcranial 2D ultrasound is a technique that can be used at the bedside or in the remote setting to assess MCA caliber.

Figures

Figure 1
Figure 1
Ultrasound images demonstrating (A) velocity/ratio and (B) vessel diameter measurement and (C) composite of four magnetic resonance imaging (MRI) images, demonstrating middle cerebral artery (MCA) multiplanar reconstruction and analysis.
Figure 2
Figure 2
Composite of seven graphs, demonstrating changes in blood pressure, arterial oxygen saturation (SaO2), regional cerebral oxygenation (rSO2), end tidal CO2 (ETCO2), peak systolic, end diastolic and mean velocities, middle cerebral artery (MCA) diameter (MCADiam), calculated MCA flow (MCAFlow), and oxygen delivery (note: blood pressure and EtCO2 were not reassessed after oxygen administration at 7,950 m).
Figure 3
Figure 3
A graph demonstrating the correlation between transcranial Doppler (TCD) and magnetic resonance imaging (MRI) measurements of middle cerebral artery (MCA) diameter.

References

    1. Ainslie PN, Burgess K, Subedi P, Burgess KR. Alterations in cerebral dynamics at high altitude following partial acclimatization in humans: wakefulness and sleep. J Appl Physiol. 2007;102:658–664.
    1. Ainslie PN, Ogoh S, Burgess K, Celi L, McGrattan K, Peebles K, Murrell C, Subedi P, Burgess KR. Differential effects of acute hypoxia and high altitude on cerebral blood flow velocity and dynamic cerebral autoregulation: alterations with hyperoxia. J Appl Physiol. 2008;104:490–498.
    1. Appenzeller O, Passino C, Roach R, Gamboa J, Gamboa A, Bernardi L, Bonfichi M, Malcovati L. Cerebral vasoreactivity in Andeans and headache at sea level. J Neurol Sci. 2004;219:101–106.
    1. Baumgartner RW, Bartsch P, Maggiorini M, Waber U, Oelz O. Enhanced cerebral blood flow in acute mountain sickness. Aviat Space Environ Med. 1994;65:726–729.
    1. Baumgartner RW, Spyridopoulos I, Bartsch P, Maggiorini M, Oelz O. Acute mountain sickness is not related to cerebral blood flow: a decompression chamber study. J Appl Physiol. 1999;86:1578–1582.
    1. Beckmann N. High resolution magnetic resonance angiography non-invasively reveals mouse strain differences in the cerebrovascular anatomy in vivo. Magn Reson Med. 2000;44:252–258.
    1. Besselmann M, Liu M, Diedenhofen M, Franke C, Hoehn M. MR angiographic investigation of transient focal cerebral ischemia in rat. NMR Biomed. 2001;14:289–296.
    1. Brugniaux JV, Hodges AN, Hanly PJ, Poulin MJ. Cerebrovascular responses to altitude. Respir Physiol Neurobiol. 2007;158:212–223.
    1. Chan CW, Hoar H, Pattinson K, Bradwell AR, Wright AD, Imray CH. Effect of sildenafil and acclimatization on cerebral oxygenation at altitude. Clin Sci (Lond) 2005;109:319–324.
    1. Choy M, Ganesan V, Thomas DL, Thornton JS, Proctor E, King MD, van der Weerd L, Gadian DG, Lythgoe MF. The chronic vascular and haemodynamic response after permanent bilateral common carotid occlusion in newborn and adult rats. J Cereb Blood Flow Metab. 2006;26:1066–1075.
    1. Du Boulay GH, Symon L. The anaesthetist's effect upon the cerebral arteries. Proc R Soc Med. 1971;64:77–80.
    1. Feddersen B, Ausserer H, Neupane P, Thanbichler F, Depaulis A, Waanders R, Noachtar S. Right temporal cerebral dysfunction heralds symptoms of acute mountain sickness. J Neurol. 2007;254:359–363.
    1. Firth PG, Zheng H, Windsor JS, Sutherland AI, Imray CH, Moore GW, Semple JL, Roach RC, Salisbury RA. Mortality on Mount Everest, 1921 to 2006: descriptive study. BMJ. 2008;337:a2654.
    1. Giller CA. The Emperor has no clothes: velocity, flow, and the use of TCD. J Neuroimaging. 2003;13:97–98.
    1. Giller CA, Bowman G, Dyer H, Mootz L, Krippner W.1993Cerebral arterial diameters during changes in blood pressure and carbon dioxide during craniotomy Neurosurgery 32737–741.discussion 41–42
    1. Giller CA, Giller AM, Cooper CR, Hatab MR. Evaluation of the cerebral hemodynamic response to rhythmic handgrip. J Appl Physiol. 2000;88:2205–2213.
    1. Gonzalez NR, Boscardin WJ, Glenn T, Vinuela F, Martin NA. Vasospasm probability index: a combination of transcranial Doppler velocities, cerebral blood flow, and clinical risk factors to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2007;107:1101–1112.
    1. Grocott MP, Martin DS, Levett DZ, McMorrow R, Windsor J, Montgomery HE. Arterial blood gases and oxygen content in climbers on Mount Everest. N Engl J Med. 2009;360:140–149.
    1. Grocott MP, Martin DS, Wilson MH, Mitchell K, Dhillon S, Mythen MG, Montgomery HE, Levett DZ. Caudwell xtreme Everest expedition. High Alt Med Biol. 2010;11:133–137.
    1. Hansen JM, Pedersen D, Larsen VA, et al. Magnetic resonance angiography shows dilatation of the middle cerebral artery after infusion of glyceryl trinitrate in healthy volunteers. Cephalalgia. 2007;27:118–27.
    1. Imray CH, Myers SD, Pattinson KT, Bradwell AR, Chan CW, Harris S, Collins P, Wright AD. Effect of exercise on cerebral perfusion in humans at high altitude. J Appl Physiol. 2005;99:699–706.
    1. Jansen GF, Kagenaar DA, Basnyat B, Odoom JA. Basilar artery blood flow velocity and the ventilatory response to acute hypoxia in mountaineers. Respir Physiol Neurobiol. 2002;133:65–74.
    1. Jansen GF, Krins A, Basnyat B, Bosch A, Odoom JA. Cerebral autoregulation in subjects adapted and not adapted to high altitude. Stroke. 2000;31:2314–2318.
    1. Lysakowski C, Von Elm E, Dumont L, Junod JD, Tassonyi E, Kayser B, Tramer MR. Effect of magnesium, high altitude and acute mountain sickness on blood flow velocity in the middle cerebral artery. Clin Sci (Lond) 2004;106:279–285.
    1. Martinoli C, Derchi LE. Gain setting in power Doppler US. Radiology. 1997;202:284–285.
    1. Moller K, Paulson OB, Hornbein TF, Colier WN, Paulson AS, Roach RC, Holm S, Knudsen GM. Unchanged cerebral blood flow and oxidative metabolism after acclimatization to high altitude. J Cereb Blood Flow Metab. 2002;22:118–126.
    1. Muller M, Schwerdtfeger K, Zieroth S. Assessment of middle cerebral artery diameter after aneurysmal subarachnoid hemorrhage by transcranial color-coded duplex sonography. Eur J Ultrasound. 2000;11:15–9.
    1. Norcliffe LJ, Rivera-Ch M, Claydon VE, Moore JP, Leon-Velarde F, Appenzeller O, Hainsworth R. Cerebrovascular responses to hypoxia and hypocapnia in high-altitude dwellers. J Physiol. 2005;566:287–294.
    1. Nuttall GA, Cook DJ, Fulgham JR, Oliver WC, Jr, Proper JA. The relationship between cerebral blood flow and transcranial Doppler blood flow velocity during hypothermic cardiopulmonary bypass in adults. Anesth Analg. 1996;82:1146–1151.
    1. Otis SM, Rossman ME, Schneider PA, Rush MP, Ringelstein EB. Relationship of cerebral blood flow regulation to acute mountain sickness. J Ultrasound Med. 1989;8:143–148.
    1. Pai SB, Varma RG, Kulkarni RN. Microsurgical anatomy of the middle cerebral artery. Neurol India. 2005;53:186–90.
    1. Palma J, Macedonia C, Deuster P, Olsen C, Mozayeni BR, Crutchfield KE. Cerebrovascular dynamics and vascular endothelial growth factor in acute mountain sickness. Wilderness Environ Med. 2006;17:1–7.
    1. Poulin MJ, Robbins PA. Indexes of flow and cross-sectional area of the middle cerebral artery using Doppler ultrasound during hypoxia and hypercapnia in humans. Stroke. 1996;27:2244–2250.
    1. Reese T, Bochelen D, Sauter A, Beckmann N, Rudin M. Magnetic resonance angiography of the rat cerebrovascular system without the use of contrast agents. NMR Biomed. 1999;12:189–196.
    1. Schreiber SJ, Gottschalk S, Weih M, Villringer A, Valdueza JM. Assessment of blood flow velocity and diameter of the middle cerebral artery during the acetazolamide provocation test by use of transcranial Doppler sonography and MR imaging. AJNR Am J Neuroradiol. 2000;21:1207–11.
    1. Serrador JM, Picot PA, Rutt BK, Shoemaker JK, Bondar RL. MRI measures of middle cerebral artery diameter in conscious humans during simulated orthostasis. Stroke. 2000;31:1672–8.
    1. Subudhi AW, Dimmen AC, Roach RC. Effects of acute hypoxia on cerebral and muscle oxygenation during incremental exercise. J Appl Physiol. 2007;103:177–183.
    1. Tarasow E, Abdulwahed Saleh Ali A, Lewszuk A, Walecki J. Measurements of the middle cerebral artery in digital subtraction angiography and MR angiography. Med Sci Monit. 2007;13 Suppl 1:65–72.
    1. Ter Minassian A, Beydon L, Ursino M, Gardette B, Gortan C, Richalet JP. Doppler study of middle cerebral artery blood flow velocity and cerebral autoregulation during a simulated ascent of Mount Everest. Wilderness Environ Med. 2001;12:175–183.
    1. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group Tissue plasminogen activator for acute ischemic stroke. N Engl J Med. 1995;333:1581–1587.
    1. Valdueza JM, Balzer JO, Villringer A, Vogl TJ, Kutter R, Einhaupl KM. Changes in blood flow velocity and diameter of the middle cerebral artery during hyperventilation: assessment with MR and transcranial Doppler sonography. AJNR Am J Neuroradiol. 1997;18:1929–34.
    1. Van Osta A, Moraine JJ, Melot C, Mairbaurl H, Maggiorini M, Naeije R. Effects of high altitude exposure on cerebral hemodynamics in normal subjects. Stroke. 2005;36:557–560.
    1. Virues-Ortega J, Buela-Casal G, Garrido E, Alcazar B. Neuropsychological functioning associated with high-altitude exposure. Neuropsychol Rev. 2004;14:197–224.
    1. Ward M, Milledge JS, West JB.2000High Altitude Physiology3rd edn.London: Arnold Publishers
    1. Weyland A, Stephan H, Kazmaier S, Weyland W, Schorn B, Grune F, Sonntag H. Flow velocity measurements as an index of cerebral blood flow. Validity of transcranial Doppler sonographic monitoring during cardiac surgery. Anesthesiology. 1994;81:1401–1410.
    1. Wilson MH, Levett DZ, Dhillon S, Mitchell K, Morgan J, Grocott MP, Imray C. Stroke at high altitude diagnosed in the field using portable ultrasound. Wilderness Environ Med. 2011;22:54–57.
    1. Wilson MH, Newman S, Imray CH. The cerebral effects of ascent to high altitudes. Lancet Neurol. 2009;8:175–191.
    1. Wolff CB, Richardson N, Kemp O, Kuttler A, McMorrow R, Hart N, Imray CH. Near infra-red spectroscopy and arterial oxygen extraction at altitude. Adv Exp Med Biol. 2007;599:183–189.
    1. Wollman H, Smith TC, Stephen GW, Colton ET, III, Gleaton HE, Alexander SC. Effects of extremes of respiratory and metabolic alkalosis on cerebral blood flow in man. J Appl Physiol. 1968;24:60–65.
    1. Zuj KA, Greaves DK, Hughson RL. WISE-2005: reduced cerebral blood flow velocity with nitroglycerin--comparison with common carotid artery blood flow. J Gravit Physiol. 2007;14:P65–P66.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner