Blood Flow Volume Measurement in Cervical and Intracranial Arteries using Quantitative Magnetic Resonance Angiography and Duplex Sonography (Bocaccia) – A Prospective Observational Study

Abstract

Purpose Cerebral blood flow volume is an important factor for the accurate diagnosis of neurovascular diseases and treatment indication. This study aims to assess correlations of blood flow volume measurements in cervical and intracranial arteries between duplex sonography and quantitative magnetic resonance angiography (qMRA).

Materials and Methods Consecutive patients with suspicion of cerebral vascular pathology underwent qMRA and duplex sonography of cervical and intracranial arteries with measurement of blood flow volume in bilateral common (CCA), internal (ICA) and external carotid arteries, vertebral and basilar arteries, middle, anterior, posterior cerebral and posterior communicating arteries using 2 different ultrasound machines. Ten patients underwent all examinations twice. Correlations between blood flow volume measurements were evaluated using Spearman’s correlation coefficient and inter-class correlation coefficient (ICC).

Results In total, 21 subjects (15 males, mean age: 56.3 ± 6.2 years) were included in the study. Duplex sonography inter-investigator correlation was excellent (ICC = 0.972, p < 0.0001) as well as intra-investigator correlations of both qMRA and duplex sonography (ICC ˃ 0.990, p < 0.0001). Mostly high correlations were recorded between qMRA and duplex sonography in particular cervical arteries but only low to moderate correlations were obtained for intracranial arteries. The mean differences between blood flow volume measurements were 10.9 ± 8.1 % in the CCA and its branches when using qMRA and 15.0 ± 11.9 % when using duplex sonography, 13.5 ± 11.8 %/35.4 ± 34.2 % in the ICA siphon and its branches when using qMRA/duplex sonography, and 24.1 ± 19.7 %/44.9 ± 44.0 % in both vertebral arteries and the basilar artery when using qMRA/duplex sonography.

Conclusion Duplex sonography as well as qMRA allow for highly reproducible measurement of blood flow volume in cervical and intracranial arteries in routine clinical practice.

Zusammenfassung

Ziel Das zerebrale Blutflussvolumen ist ein wichtiger Parameter für die Diagnosestellung bei neurovaskulären Erkrankungen und die Therapieindikation. Ziel dieser Studie ist es, die Übereinstimmung von Blutflussvolumenmessungen zwischen Duplex-Sonografie und quantitativer Magnetresonanzangiografie (qMRA) in zervikalen und intrakraniellen Arterien zu beurteilen.

Material und Methoden Bei konsekutiven Patienten mit Verdacht auf zerebrale Gefäßpathologie wurden eine qMRA und Duplex-Sonografie der zervikalen und intrakraniellen Arterien mit Blutflussvolumenmessung mit 2 verschiedenen Ultraschallgeräten in der bilateralen A. carotis communis (CCA), A. carotis interna (ICA) und externa, A. vertebralis und A. basilaris und in der A. cerebri media, anterior und posterior und in der A. communicans posterior durchgeführt. Zehn Patienten wurden 2-mal untersucht. Die Übereinstimmungen zwischen den Blutflussvolumenmessungen wurden mittels Spearman-Korrelationskoeffizient und Interklassen-Korrelationskoeffizient (ICC) bewertet.

Ergebnisse Insgesamt wurden 21 Probanden (15 Männer, Durchschnittsalter 56,3 ± 6,2 Jahre) in die Studie eingeschlossen. Die Übereinstimmung zwischen den Untersuchern der Duplex-Sonografie war ausgezeichnet (ICC = 0,972; p < 0,0001), ebenso die Übereinstimmung zwischen Untersuchern in der qMRA und der Duplex-Sonografie (ICC ˃ 0,990; p < 0,0001). Meistens wurden hohe Korrelationen zwischen qMRA und Duplex-Sonografie insbesondere für zervikale Arterien festgestellt, jedoch nur geringe bis mäßige Korrelationen für intrakranielle Arterien. Die mittleren Differenzen zwischen den Blutflussvolumenmessungen in der CCA und ihren Ästen betrugen 10,9 ± 8,1 % in der qMRA und 15,0 ± 11,9 % in der Duplex-Sonografie, im ICA-Siphon und seinen Ästen 13,5 ± 11,8 % (qMRA) und 35,4 ± 34,2 % (Duplex) und in beiden A. vertebralis und A. basilaris 24,1 ± 19,7 % (qMRA) und 44,9 ± 44,0 % (Duplex).

Schlussfolgerung Sowohl die Duplex-Sonografie als auch die qMRA erlauben eine gut reproduzierbare Messung des Blutflussvolumens in zervikalen und intrakraniellen Arterien in der klinischen Routinepraxis.

Key words

magnetic resonance - duplex sonography - blood flow volume - cervical arteries - brain arteries

• References

• 1 Amin-Hanjani S, Du X, Zhao M. et al. Use of quantitative magnetic resonance angiography to stratify stroke risk in symptomatic vertebrobasilar disease. Stroke 2005; 36: 1140-1145
• 2 Amin-Hanjani S, Turan TN, Du X. et al. Higher Stroke Risk with Lower Blood Pressure in Hemodynamic Vertebrobasilar Disease: Analysis from the VERiTAS Study. J Stroke Cerebrovasc Dis 2017; 26: 403-410
• 3 Amin-Hanjani S, Stapleton CJ, Du X. et al. Hypoperfusion Symptoms Poorly Predict Hemodynamic Compromise and Stroke Risk in Vertebrobasilar Disease. Stroke 2019; 50: 495-497
• 4 Payen DM, Levy BI, Menegalli DJ. et al. Evaluation of human hemispheric blood flow based on non invasive carotid blood flow measurements using the range-gated Doppler technique. Stroke 1982; 13: 392-398
• 5 Burns PN. The physical principles of Doppler and spectral analysis. J Clin Ultrasound 1987; 15: 567-590
• 6 Marks MP, Pelc NJ, Ross MR. et al. Determination of cerebral blood flow with a phase-contrast cine MR imaging technique: evaluation of normal subjects and patients with arteriovenous malformations. Radiology 1992; 182: 467-476
• 7 Eicke BM, Tegeler CH. Ultrasonic quantitative flow volumetry of the carotid arteries: initial experience with a color flow M-mode system. Cerebrovasc Dis 1995; 5: 145-149
• 8 Zhao M, Amin-Hanjani S, Ruland S. et al. Regional cerebral blood flow using quantitative MR angiography. AJNR Am J Neuroradiol 2007; 28: 1470-1473
• 9 Bauer AM, Amin-Hanjani S, Alaraj A. et al. Quantitative magnetic resonance angiography in the evaluation of the subclavian steal syndrome: report of 5 patients. J Neuroimaging 2009; 19: 250-252
• 10 Prabhakaran S, Warrior L, Wells KR. et al. The utility of quantitative magnetic resonance angiography in the assessment of intracranial in-stent stenosis. Stroke 2009; 40: 991-993
• 11 Brisman JL. Wingspan stenting of symptomatic extracranial vertebral artery stenosis and perioperative evaluation using quantitative magnetic resonance angiography: report of two cases. Neurosurg Focus 2008; 24: E14
• 12 Ruland S, Ahmed A, Thomas K. et al. Leptomeningeal collateral volume flow assessed by quantitative magnetic resonance angiography in large-vessel cerebrovascular disease. J Neuroimaging 2009; 19: 27-30
• 13 Langer DJ, Song JK, Niimi Y. et al. Transarterial embolization of vein of Galen malformations: the use of magnetic resonance imaging noninvasive optimal vessel analysis to quantify shunt reduction. Report of two cases. J Neurosurg 2006; 104 (Suppl. 01) 41-45
• 14 Uematsu S, Yang A, Preziosi TJ. et al. Measurement of carotid blood flow in man and its clinical application. Stroke 1983; 14: 256-266
• 15 Oktar SO, Yücel C, Karaosmanoglu D. et al. Blood-flow volume quantification in internal carotid and vertebral arteries: comparison of 3 different ultrasound techniques with phase-contrast MR imaging. AJNR Am J Neuroradiol 2006; 27: 363-969
• 16 Schöning M, Walter J, Scheel P. Estimation of cerebral blood flow through color duplex sonography of the carotid and vertebral arteries in healthy adults. Stroke 1994; 25: 17-22
• 17 Dörfler P, Puls I, Schliesser M. et al. Measurement of cerebral blood flow volume by extracranial sonography. J Cereb Blood Flow Metab 2000; 20: 269-271
• 18 Ho SS, Metreweli C. Preferred technique for blood flow volume measurement in cerebrovascular disease. Stroke 2000; 31: 1342-1345
• 19 Ruland S, Zhao M, Pandey D. et al. Reproducibility of cerebral blood flow analysis using quantitative magnetic resonance angiography. AANS/CNS Cerebrovascular Section 9th Joint Annual Meeting; 2006: 17-20
• 20 Ho SS, Chan YL, Yeung DK. et al. Blood flow volume quantification of cerebral ischemia: comparison of three noninvasive imaging techniques of carotid and vertebral arteries. Am J Roentgenol 2002; 178: 551-556
• 21 Banis Jr JC, Schwartz KS, Acland RD. Electromagnetic flowmetry – an experimental method for continuous blood flow measurement using a new island flap model. Plast Reconstr Surg 1980; 66: 534-544
• 22 Schöning M, Hartig B. Age dependence of total cerebral blood flow volume from childhood to adulthood. J Cereb Blood Flow Metab 1996; 16: 827-833
• 23 Scheel P, Ruge C, Petruch UR. et al. Color duplex measurement of cerebral blood flow volume in healthy adults. Stroke 2000; 31: 147-150
• 24 Buijs PC, Krabbe-Hartkamp MJ, Bakker CJ. et al. Effect of age on cerebral blood flow: measurement with ungated two-dimensional phase-contrast MR angiography in 250 adults. Radiology 1998; 209: 667-674
• 25 Kashimada A, Machida K, Honda N. et al. Measurement of cerebral blood flow with two-dimensional cine phase-contrast MR imaging: evaluation of normal subjects and patients with vertigo. Radiat Med 1995; 13: 95-102
• 26 Winkler AJ. An experimental study of the accuracy of volume flow measurements using commercial ultrasound systems. J Vasc Technol 1995; 19: 175-180
• 27 Soustiel JF, Glenn TC, Vespa P. et al. Assessment of cerebral blood flow by means of blood-flow-volume measurement in the internal carotid artery: comparative study with a 133xenon clearance technique. Stroke 2003; 34: 1876-1880
• 28 Hasegawa H. Improvement of range spatial resolution of medical ultrasound imaging element-domain signal processing. Jpn J Appl Phys 2017; 56: 07JF02
• 29 Bianchini E, Bozec E, Gemignani V. et al. Assessment of carotid stiffness and intima-media thickness from ultrasound data: comparison between two methods. J Ultrasound Med 2010; 29: 1169-1175