Technical recommendations for the use of carotid duplex ultrasound for the assessment of extracranial blood flow

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 309, Issue 7, 2015, Pages R707-R720

  Thomas, Kate N ^a   Lewis, Nia C S ^b   Hill, Brigid G ^a   Ainslie, Philip N ^b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Carotid artery; Cerebral blood flow measurement; Cerebral hemodynamics; Transcranial doppler; Ultrasound

Indexed keywords

ARTERY DIAMETER; ARTICLE; BLOOD FLOW VELOCITY; BRAIN BLOOD FLOW; CAROTID ARTERY; CAROTID DUPLEX ULTRASOUND; COLOR; COLOR ULTRASOUND FLOWMETRY; DOPPLER ECHOGRAPHY; DOPPLER FLOWMETRY; EXTRACRANIAL BLOOD FLOW; HUMAN; MEDICAL RESEARCH; PRACTICE GUIDELINE; PRIORITY JOURNAL; PULSED WAVE DOPPLER; SCREENING; ULTRASOUND TRANSDUCER; VERTEBRAL ARTERY; BLOOD FLOW; BRAIN CIRCULATION; ECHOCARDIOGRAPHY; ECHOGRAPHY; PHYSIOLOGY; PROCEDURES;

CAROTID ARTERIES; CEREBROVASCULAR CIRCULATION; ECHOCARDIOGRAPHY; HUMANS; REGIONAL BLOOD FLOW; ULTRASONOGRAPHY, DOPPLER, DUPLEX; VERTEBRAL ARTERY;

EID: 84943178731     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00211.2015     Document Type: Article

References (79)

1. Adkisson EJ, Casey DP, Beck DT, Gurovich AN, Martin JS, Braith RW. Central, peripheral and resistance arterial reactivity: fluctuates during the phases of the menstrual cycle. Exp Biol Med (Maywood) 235: 111-118, 2010.
2. Ainslie PN, Hoiland RL. Transcranial Doppler ultrasound: valid, invalid, or both? J Appl Physiol (1985) 117: 1081-1083, 2014.
3. Atkinson G, Batterham AM, Black MA, Cable NT, Hopkins ND, Dawson EA, Thijssen DH, Jones H, Tinken TM, Green DJ. Is the ratio of flow-mediated dilation and shear rate a statistically sound approach to normalization in cross-sectional studies on endothelial function? J Appl Physiol 107: 1893-1899, 2009.
4. Bakker FC, Klijn CJ, Jennekens-Schinkel A, van der Tweel I, Tulleken CA, Kappelle LJ. Cognitive impairment in patients with carotid artery occlusion and ipsilateral transient ischemic attacks. J Neurol 250: 1340-1347, 2003.
5. Bianchini E, Bozec E, Gemignani V, Faita F, Giannarelli C, Ghiadoni L, Demi M, Boutouyrie P, Laurent S. Assessment of carotid stiffness and intima-media thickness from ultrasound data: comparison between two methods. J Ultrasound Med 29: 1169-1175, 2010.
6. Billinger SA, Mattlage AE, Ashenden AL, Lentz AA, Harter G, Rippee MA. Aerobic exercise in subacute stroke improves cardiovascular health and physical performance. J Neurol Physical Ther 36: 159-165, 2012.
7. Black MA, Cable NT, Thijssen DH, Green DJ. Importance of measuring the time course of flow-mediated dilatation in humans. Hypertension 51: 203-210, 2008.
8. Bornstein RA, Starling RC, Myerowitz PD, Haas GJ. Neuropsychological function in patients with end-stage heart failure before and after cardiac transplantation. Acta Neurol Scand 91: 260-265, 1995.
9. Brandt WE. Vascular ultrasound In: Ultrasound, edited by Battaglia SE. Philadelphia, PA: Lippincott Williams & Wilkins, 2001, p. 412-420.
10. Browne JE. A review of Doppler ultrasound quality assurance protocols and test devices. Phys Med 30: 742-751, 2014.
11. Carter HH, Spence AL, Pugh CJ, Ainslie P, Naylor LH, Green DJ. Cardiovascular responses to water immersion in humans: impact on cerebral perfusion. Am J Physiol Regul Integr Comp Physiol 306: R636-R640, 2014.
12. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 39: 257-265, 2002.
13. Coverdale NS, Gati JS, Opalevych O, Perrotta A, Shoemaker JK. Cerebral blood flow velocity underestimates cerebral blood flow during modest hypercapnia and hypocapnia. J Appl Physiol (1985) 117: 1090-1096, 2014.
14. Coverdale NS, Lalande S, Perrotta A, Shoemaker JK. Heterogeneous patterns of vasoreactivity in the middle cerebral and internal carotid arteries. Am J Physiol Heart Circ Physiol 308: H1030-H1038, 2015.
15. Dawson EA, Whyte GP, Black MA, Jones H, Hopkins N, Oxborough D, Gaze D, Shave RE, Wilson M, George KP, Green DJ. Changes in vascular and cardiac function after prolonged strenuous exercise in humans. J Appl Physiol 105: 1562-1568, 2008.
16. Evans DH. On the measurement of the mean velocity of blood flow over the cardiac cycle using Doppler ultrasound. Ultrasound Med Biol 11: 735-741, 1985.
17. Evans DH. Some aspects of the relationship between instantaneous volumetric blood flow and continuous wave Doppler ultrasound recordings. I. The effect of ultrasonic beam width on the output of maximum, mean and RMS frequency processors. Ultrasound Med Biol 8: 605-609, 1982.
18. Faita F, Masi S, Loukogeorgakis S, Gemignani V, Okorie M, Bianchini E, Charakida M, Demi M, Ghiadoni L, Deanfield JE. Comparison of two automatic methods for the assessment of brachial artery flow-mediated dilation. J Hypertens 29: 85-90, 2011.
19. Fan JL, Burgess KR, Thomas KN, Peebles KC, Lucas SJ, Lucas RA, Cotter JD, Ainslie PN. Influence of indomethacin on ventilatory and cerebrovascular responsiveness to CO2 and breathing stability: the influence of PCO2 gradients. Am J Physiol Regul Integr Comp Physiol 298: R1648-R1658, 2010.
20. Gemignani V, Bianchini E, Faita F, Giannarelli C, Plantinga Y, Ghiadoni L, Demi M. Ultrasound measurement of the brachial artery flow-mediated dilation without ECG gating. Ultrasound Med Biol 34: 385-391, 2008.
21. Gent R. Applied Physics and Technology of Diagnostic Ultrasound. Binda, New South Wales, Australia: Milner Publishing, 1997.
22. Ghiadoni L, Magagna A, Versari D, Kardasz I, Huang Y, Taddei S, Salvetti A. Different effect of antihypertensive drugs on conduit artery endothelial function. Hypertension 41: 1281-1286, 2003.
23. Gill RW. Measurement of blood flow by ultrasound: accuracy and sources of error. Ultrasound Med Biol 11: 625-641, 1985.
24. Giller CA, Bowman G, Dyer H, Mootz L, Krippner W. Cerebral arterial diameters during changes in blood pressure and carbon dioxide during craniotomy. Neurosurgery 32: 737-741; discussion 741-732, 1993.
25. Goodsitt MM, Carson PL, Witt S, Hykes DL, Kofler JM Jr. Real-time B-mode ultrasound quality control test procedures. Report of AAPM Ultrasound Task Group No 1. Med Phys 25: 1385-1406, 1998.
26. Guiney H, Lucas SJ, Cotter JD, Machado L. Evidence cerebral bloodflow regulation mediates exercise-cognition links in healthy young adults. Neuropsychology 29: 1-9, 2015.
27. Gupta A, Chazen JL, Hartman M, Delgado D, Anumula N, Shao H, Mazumdar M, Segal AZ, Kamel H, Leifer D, Sanelli PC. Cerebrovascular reserve and stroke risk in patients with carotid stenosis or occlusion: a systematic review and meta-analysis. Stroke 43: 2884-2891, 2012.
28. Harris RA, Nishiyama SK, Wray DW, Richardson RS. Ultrasound assessment of flow-mediated dilation. Hypertension 55: 1075-1085, 2010.
29. Harris RA, Nishiyama SK, Wray DW, Tedjasaputra V, Bailey DM, Richardson RS. The effect of oral antioxidants on brachial artery flowmediated dilation following 5 and 10 min of ischemia. Eur J Appl Physiol 107: 445-453, 2009.
30. Hijmering ML, de Lange DW, Lorsheyd A, Kraaijenhagen RJ, van de Wiel A. Binge drinking causes endothelial dysfunction, which is not prevented by wine polyphenols: a small trial in healthy volunteers. Netherlands J Med 65: 29-35, 2007.
31. Inaba Y, Chen JA, Bergmann SR. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a metaanalysis. Int J Cardiovasc Imag 26: 631-640, 2010.
32. Iooss B, Lhuillier C, Jeanneau H. Numerical simulation of transit-time ultrasonic flowmeters: uncertainties due to flow profile and fluid turbulence. Ultrasonics 40: 1009-1015, 2002.
33. Jara H, Yu BC, Caruthers SD, Melhem ER, Yucel EK. Voxel sensitivity function description of flow-induced signal loss in MR imaging: implications for black-blood MR angiography with turbo spin-echo sequences. Magn Reson Med 41: 575-590, 1999.
34. Jones H, Lewis NC, Thompson A, Marrin K, Green DJ, Atkinson G. Diurnal variation in vascular function: role of sleep. Chronobiol Int 29: 271-277, 2012.
35. Kirkham FJ, Padayachee TS, Parsons S, Seargeant LS, House FR, Gosling RG. Transcranial measurement of blood velocities in the basal cerebral arteries using pulsed Doppler ultrasound: velocity as an index of flow. Ultrasound Med Biol 12: 15-21, 1986.
36. Lavi T, Karasik A, Koren-Morag N, Kanety H, Feinberg MS, Shechter M. The acute effect of various glycemic index dietary carbohydrates on endothelial function in nondiabetic overweight and obese subjects. J Am Coll Cardiol 53: 2283-2287, 2009.
37. Lewis NC, Bailey DM, Dumanoir GR, Messinger L, Lucas SJ, Cotter JD, Donnelly J, McEneny J, Young IS, Stembridge M, Burgess KR, Basnet AS, Ainslie PN. Conduit artery structure and function in lowlanders and native highlanders: relationships with oxidative stress and role of sympathoexcitation. J Physiol 592: 1009-1024, 2014.
38. Lewis NC, Smith KJ, Bain AR, Wildfong KW, Numan T, Ainslie PN. Impact of transient hypotension on regional cerebral blood flow in humans. Clin Sci (Lond) 129: 169-178, 2015.
39. Li S, Hoskins PR, Anderson T, McDicken WN. Measurement of mean velocity during pulsatile flow using time-averaged maximum frequency of Doppler ultrasound waveforms. Ultrasound Med Biol 19: 105-113, 1993.
40. Lucas SJ, Ainslie PN, Murrell CJ, Thomas KN, Franz EA, Cotter JD. Effect of age on exercise-induced alterations in cognitive executive function: relationship to cerebral perfusion. Exp Gerontol 47: 541-551, 2012.
41. Mancini GB, Yeoh E, Abbott D, Chan S. Validation of an automated method for assessing brachial artery endothelial dysfunction. Can J Cardiol 18: 259-262, 2002.
42. Markus HS, Vallance P, Brown MM. Differential effect of three cyclooxygenase inhibitors on human cerebral blood flow velocity and carbon dioxide reactivity. Stroke 25: 1760-1764, 1994.
43. Marshall RS. Effects of altered cerebral hemodynamics on cognitive function. J Alzheimer's Dis 32: 633-642, 2012.
44. Otto ME, Svatikova A, Barretto RB, Santos S, Hoffmann M, Khandheria B, Somers V. Early morning attenuation of endothelial function in healthy humans. Circulation 109: 2507-2510, 2004.
45. Padilla J, Young CN, Simmons GH, Deo SH, Newcomer SC, Sullivan JP, Laughlin MH, Fadel PJ. Increased muscle sympathetic nerve activity acutely alters conduit artery shear rate patterns. Am J Physiol Heart Circ Physiol 298: H1128-H1135, 2010.
46. Papaioannou TG, Stefanadis C. Vascular wall shear stress: basic principles and methods. Hellenic J Cardiol 46: 9-15, 2005.
47. Papamichael CM, Aznaouridis KA, Karatzis EN, Karatzi KN, Stamatelopoulos KS, Vamvakou G, Lekakis JP, Mavrikakis ME. Effect of coffee on endothelial function in healthy subjects: the role of caffeine. Clin Sci (Lond) 109: 55-60, 2005.
48. Paulson OB, Jarden JO, Godtfredsen J, Vorstrup S. Cerebral blood flow in patients with congestive heart failure treated with captopril. Am J Med 76: 91-95, 1984.
49. Prendes JL, McKinney WM, Buonanno FS, Jones AM. Anatomic variations of the carotid bifurcation affecting Doppler scan interpretation. J Clin Ultrasound 8: 147-150, 1980.
50. Primozich JF. Extracranial arterial system. In: Duplex Scanning in Vascular Disorders, edited by Strandness DE. Philadelphia, PA: Lippincott Williams & Wilkins, 2002, p. 192-231.
51. Reinhard M, Schwarzer G, Briel M, Altamura C, Palazzo P, King A, Bornstein NM, Petersen N, Motschall E, Hetzel A, Marshall RS, Klijn CJ, Silvestrini M, Markus HS, Vernieri F. Cerebrovascular reactivity predicts stroke in high-grade carotid artery disease. Neurology 83: 1424-1431, 2014.
52. Ritz K, Denswil NP, Stam OC, van Lieshout JJ, Daemen MJ. Cause and mechanisms of intracranial atherosclerosis. Circulation 130: 1407-1414, 2014.
53. Rognmo O, Bjornstad TH, Kahrs C, Tjonna AE, Bye A, Haram PM, Stolen T, Slordahl SA, Wisloff U. Endothelial function in highly endurance-trained men: effects of acute exercise. J Strength Cond Res 22: 535-542, 2008.
54. Rohren EM, Kliewer MA, Carroll BA, Hertzberg BS. A spectrum of Doppler waveforms in the carotid and vertebral arteries. Am J Roentgenol 181: 1695-1704, 2003.
55. Sasoh M, Ogasawara K, Kuroda K, Okuguchi T, Terasaki K, Yamadate K, Ogawa A. Effects of EC-IC bypass surgery on cognitive impairment in patients with hemodynamic cerebral ischemia. Surg Neurol 59: 455-460; discussion 460-453, 2003.
56. Sato K, Sadamoto T. Different blood flow responses to dynamic exercise between internal carotid and vertebral arteries in women. J Appl Physiol (1985) 109: 864-869, 2010.
57. Schoning M, Walter J, Scheel P. Estimation of cerebral blood flow through color duplex sonography of the carotid and vertebral arteries in healthy adults. Stroke 25: 17-22, 1994.
58. Seidel E, Eicke BM, Tettenborn B, Krummenauer F. Reference values for vertebral artery flow volume by duplex sonography in young and elderly adults. Stroke 30: 2692-2696, 1999.
59. Serrador JM, Picot PA, Rutt BK, Shoemaker JK, Bondar RL. MRI measures of middle cerebral artery diameter in conscious humans during simulated orthostasis. Stroke 31: 1672-1678, 2000.
60. Skulas-Ray AC, Kris-Etherton PM, Harris WS, Vanden Heuvel JP, Wagner PR, West SG. Dose-response effects of omega-3 fatty acids on triglycerides, inflammation, and endothelial function in healthy persons with moderate hypertriglyceridemia. Am J Clin Nutr 93: 243-252, 2011.
61. Stary HC. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis 9: I19-I32, 1989.
62. Steinman AH, Tavakkoli J, Myers JG Jr, Cobbold RS, Johnston KW. Sources of error in maximum velocity estimation using linear phased-array Doppler systems with steady flow. Ultrasound Med Biol 27: 655-664, 2001.
63. Taneva E, Borucki K, Wiens L, Makarova R, Schmidt-Lucke C, Luley C, Westphal S. Early effects on endothelial function of atorvastatin 40 mg twice daily and its withdrawal. Am J Cardiol 97: 1002-1006, 2006.
64. Taylor CE, Willie CK, Ainslie PN, Tzeng YC. Assessment of human baroreflex function using carotid ultrasonography: what have we learnt? Acta Physiol (Oxf) 211: 297-313, 2014.
65. Thijssen DH, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, Parker B, Widlansky ME, Tschakovsky ME, Green DJ. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 300: H2-H12, 2011.
66. Tinken TM, Thijssen DH, Black MA, Cable NT, Green DJ. Time course of change in vasodilator function and capacity in response to exercise training in humans. J Physiol 586: 5003-5012, 2008.
67. Tortoli P, Guidi F, Guidi G, Atzeni C. Spectral velocity profiles for detailed ultrasound flow analysis. IEEE Trans Ultrason Ferr 43: 654-659, 1996.
68. Totosy de Zepetnek JO, Jermey TL, MacDonald MJ. Superficial femoral artery endothelial responses to a short-term altered shear rate intervention in healthy men. PloS One 9: e113407, 2014.
69. Tyldum GA, Schjerve IE, Tjonna AE, Kirkeby-Garstad I, Stolen TO, Richardson RS, Wisloff U. Endothelial dysfunction induced by postprandial lipemia: complete protection afforded by high-intensity aerobic interval exercise. J Am Coll Cardiol 53: 200-206, 2009.
70. 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. Am J Neuroradiol 18: 1929-1934, 1997.
71. Van Bortel LM, Laurent S, Boutouyrie P, Chowienczyk P, Cruickshank JK, De Backer T, Filipovsky J, Huybrechts S, Mattace-Raso FU, Protogerou AD, Schillaci G, Segers P, Vermeersch S, Weber T. Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens 30: 445-448, 2012.
72. Verbree J, Bronzwaer AS, Ghariq E, Versluis MJ, Daemen MJ, van Buchem MA, Dahan A, van Lieshout JJ, van Osch MJ. Assessment of middle cerebral artery diameter during hypocapnia and hypercapnia in humans using ultra-high-field MRI. J Appl Physiol (1985) 117: 1084-1089, 2014.
73. Willie CK, Macleod DB, Shaw AD, Smith KJ, Tzeng YC, Eves ND, Ikeda K, Graham J, Lewis NC, Day TA, Ainslie PN. Regional brain blood flow in man during acute changes in arterial blood gases. J Physiol 590: 3261-3275, 2012.
74. Willie CK, Tzeng YC, Fisher JA, Ainslie PN. Integrative regulation of human brain blood flow. J Physiol 592: 841-859, 2014.
75. Wilson MH, Edsell ME, Davagnanam I, Hirani SP, Martin DS, Levett DZ, Thornton JS, Golay X, Strycharczuk L, Newman SP, Montgomery HE, Grocott MP, Imray CH. Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia-an ultrasound and MRI study. J Cereb Blood Flow Metab 31: 2019-2029, 2011.
76. Woodman RJ, Playford DA, Watts GF, Cheetham C, Reed C, Taylor RR, Puddey IB, Beilin LJ, Burke V, Mori TA, Green D. Improved analysis of brachial artery ultrasound using a novel edge-detection software system. J Appl Physiol 91: 929-937, 2001.
77. Yeboah J, Crouse JR, Hsu FC, Burke GL, Herrington DM. Brachial flow-mediated dilation predicts incident cardiovascular events in older adults: the Cardiovascular Health Study. Circulation 115: 2390-2397, 2007.
78. Yonan KA, Greene ER, Sharrar JM, Caprihan A, Qualls C, Roldan CA. Middle cerebral artery blood flows by combining TCD velocities and MRA diameters: in vitro and in vivo validations. Ultrasound Med Biol 40: 2692-2699, 2014.
79. Zuccala G, Onder G, Marzetti E, Monaco MR, Cesari M, Cocchi A, Carbonin P, Bernabei R. Use of angiotensin-converting enzyme inhibitors and variations in cognitive performance among patients with heart failure. Eur Heart J 26: 226-233, 2005.