# Quantitative Blood Flow Measurements in the Common Carotid Artery: A Comparative Study of High-Frame-Rate Ultrasound Vector Flow Imaging, Pulsed Wave Doppler, and Phase Contrast Magnetic Resonance Imaging

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## Abstract

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## 1. Introduction

## 2. Materials and Methods

#### 2.1. V Flow Technique Description

#### 2.2. Ultrasound Scan Setup

#### 2.3. PC-MRI Scan Setup

^{2}; imaging resolution—1.17 by 1.17 mm

^{2}, reconstructed into 0.59 by 0.59 mm

^{2}; slice thickness—5 mm; spoiled gradient echo (SPGR) as readout with flip angle—10°; and TR/TE—13.0/7.9 ms. The phase contrast flow direction was the foot–head direction with a velocity encoding (VENC) of 90 cm/s. The peripheral pulse unit (PPU) was used to synchronize the scan with 15 heart phases. The maximum and time-averaged mean velocities and the volume flow rate are estimated for both the left and right common carotid arteries (a total of 64 CCAs). One example is shown in Figure 3. Results from 3 CCAs had to be abandoned due to aliasing (i.e., the real velocity being larger than the detectable 90 cm/s). Therefore, the PC-MRI results for 61 CCAs are used in the comparison studies.

#### 2.4. Statistical Analysis

## 3. Results

## 4. Discussion

## 5. Conclusions

## Author Contributions

## Funding

## Institutional Review Board Statement

## Informed Consent Statement

## Data Availability Statement

## Acknowledgments

## Conflicts of Interest

## List of Abbreviations

## References

- North American Symptomatic Carotid Endarterectomy Trial (NASCET) Steering Committee. North American Symptomatic Cartotid Endarterectomy Trial: Methods, patient characteristics, and progress. Stroke
**1991**, 22, 711–720. [Google Scholar] [CrossRef] [PubMed][Green Version] - European Carotid Surgery Trialists’ Collaborative Group. Randomised trial of endarterectomy for recently symptomatic carotid stenosis: Final results of the MRC European Carotid Surgery Trial (ECST). Lancet
**1998**, 351, 1379–1387. [Google Scholar] [CrossRef] - Grant, E.G.; Benson, C.B.; Moneta, G.L.; Alexandrov, A.V.; Baker, J.D.; Bluth, E.I.; Carroll, B.A.; Eliasziw, M.; Gocke, J.; Hertzberg, B.S.; et al. Carotid artery stenosis: Gray-scale and Doppler US diagnosis—Society of Radiologists in Ultrasound Consensus Conference. Radiology
**2003**, 229, 340–346. [Google Scholar] [CrossRef] [PubMed] - Carpenter, J.P.; Lexa, F.J.; Davis, J.T. Determination of sixty percent or greater carotid artery stenosis by duplex Doppler ultrasonography. J. Vasc. Surg.
**1995**, 22, 697–703. [Google Scholar] [CrossRef][Green Version] - Moneta, G.L.; Edwards, J.M.; Papanicolaou, G.; Hatsukami, T.; Taylor, L.M., Jr.; Strandness, D.E., Jr.; Porter, J.M. Screening for asymptomatic internal carotid artery stenosis: Duplex criteria for discriminating 60% to 99% stenosis. J. Vasc. Surg.
**1995**, 21, 989–994. [Google Scholar] [CrossRef][Green Version] - Jensen, J.A. Estimation of Blood Velocities using Ultrasound: A Signal Processing Approach; Cambridge University Press: New York, NY, USA, 1996. [Google Scholar]
- Ford, M.D.; Xie, Y.J.; Wasserman, B.A.; Steinman, D.A. Is flow in the common carotid artery fully developed? Physiol. Meas.
**2008**, 29, 1335–1349. [Google Scholar] [CrossRef] [PubMed] - Manbachi, A.; Hoi, Y.; Wasserman, B.A.; Lakatta, E.G.; Steinman, D.A. On the shape of the common carotid artery with implications for blood velocity profiles. Physiol. Meas.
**2011**, 32, 1885–1897. [Google Scholar] [CrossRef][Green Version] - Hansen, K.L.; Udesen, J.; Gran, F.; Jensen, J.A.; Nielsen, M.B. In-vivo examples of flow patterns with the fast vector velocity ultrasound method. Ultraschall Med.
**2009**, 30, 471–477. [Google Scholar] [CrossRef] - Jensen, J.A.; Nikolov, S.I.; Hansen, K.L.; Stuart, M.B.; Hoyos, C.A.V.; Schou, M.; Ommen, M.L.; Øygard, S.H.; Jørgensen, L.T.; Traberg, M.S.; et al. History and latest advances in flow estimation technology: From 1-D in 2-D to 3-D in 4-D. In Proceedings of the 2019 IEEE International Ultrasonics Symposium (IUS), Glasgow, UK, 6–9 October 2019. [Google Scholar]
- Goddi, A.; Fanizza, M.; Bortolotto, C.; Raciti, M.V.; Fiorina, I.; He, X.; Du, Y.; Calliada, F. Vector flow imaging techniques: An innovative ultrasonographic technique for the study of blood flow. J. Clin. Ultrasound
**2017**, 45, 582–588. [Google Scholar] [CrossRef] - Trahey, G.E.; Allison, J.W.; Von, R.O.T. Angle independent ultrasonic detection of blood flow. IEEE Trans. Biomed. Eng.
**1987**, 34, 965–967. [Google Scholar] [CrossRef] - Jensen, J.A.; Nikolov, S.I.; Yu, A.C.H.; Garcia, D. Ultrasound vector flow imaging–Part I: Sequential systems. IEEE Trans. Ultrason. Ferroelectr. Freq. Control
**2016**, 63, 1704–1723. [Google Scholar] [CrossRef] [PubMed][Green Version] - Jensen, J.A.; Nikolov, S.I.; Yu, A.C.H.; Garcia, D. Ultrasound vector flow imaging–Part II: Parallel systems. IEEE Trans Ultrason. Ferroelectr. Freq. Control
**2016**, 63, 1722–1732. [Google Scholar] [CrossRef] [PubMed][Green Version] - Udesen, J.; Gran, F.; Hansen, K.L.; Jensen, J.A.; Thomsen, C.; Nielsen, M.B. High framerate blood vector velocity imaging using plane waves: Simulations and preliminary experiments. IEEE Trans. Ultrason. Ferroelectr. Freq. Control
**2008**, 55, 1729–1743. [Google Scholar] [CrossRef] [PubMed] - Jensen, J.A. A new estimator for vector velocity estimation. IEEE Trans. Ultrason. Ferroelectr. Freq. Control
**2001**, 48, 886–894. [Google Scholar] [CrossRef] [PubMed][Green Version] - Uejima, T.; Koike, A.; Sawada, H.; Aizawa, T.; Ohtsuki, S.; Tanaka, M.; Furukawa, T.; Fraser, A.G. A new echocardiographic method for identifying vortex flow in the left ventricle: Numerical validation. Ultrasound Med. Biol.
**2010**, 36, 772–788. [Google Scholar] [CrossRef] - Dunmire, B.; Beach, K.W.; Labs, K.-H.; Plett, M.; Strandness, D.E., Jr. Cross-beam vector Doppler ultrasound for angle-independent velocity measurements. Ultrasound Med. Biol.
**2000**, 26, 1213–1235. [Google Scholar] [CrossRef] - Yiu, B.Y.S.; Lai, S.S.M.; Yu, A.C.H. Vector projectile imaging: Time-resolved dynamic visualization of complex flow patterns. Ultrasound Med. Biol.
**2014**, 40, 2295–2309. [Google Scholar] [CrossRef] - Leow, C.H.; Bazigou, E.; Eckersley, R.J.; Yu, A.C.H.; Weinberg, P.D.; Tang, M.-X. Flow velocity mapping using contrast enhanced high-frame-rate plane wave ultrasound and image tracking: Methods and initial in vitro and in vivo evaluation. Ultrasound Med. Biol.
**2015**, 41, 2913–2925. [Google Scholar] [CrossRef][Green Version] - Hansen, K.L.; Udesen, J.; Oddershede, N.; Henze, L.; Thomsen, C.; Jensen, J.A.; Nielsen, M.B. In vivo comparison of three ultrasound vector velocity techniques to MR phase contrast angiography. Ultrasonics
**2009**, 49, 659–667. [Google Scholar] [CrossRef] - Brandt, A.H.; Hansen, K.L.; Ewertsen, C.; Holbek, S.; Olesen, J.B.; Moshavegh, R.; Thomsen, C.; Jensen, J.A.; Nielsen, M.B. A comparison study of vector velocity, spectral Doppler and magnetic resonance of blood flow in the common carotid artery. Ultrasound Med. Biol.
**2018**, 44, 1751–1761. [Google Scholar] [CrossRef] - Du, Y.; Shen, Y.; Yiu, B.Y.S.; Yu, A.C.H.; Zhu, L. High frame rate vector flow imaging: Development as a new diagnostic mode on a clinical scanner. In Proceedings of the 2018 IEEE International Ultrasonics Symposium (IUS), Kobe, Japan, 22–25 October 2018. [Google Scholar]
- Du, Y.; Fan, R.; Li, Y. Ultrasound Imaging Method and System. U.S. Application Patent US20170071576A1, 16 March 2017. [Google Scholar]
- Yu, A.C.H.; Yiu, Y.S. Apparatus for Ultrasound Flow Vector Imaging and Methods Thereof. U.S. Patent US10231695B2, 19 March 2019. [Google Scholar]
- Kasai, C.; Namekawa, K.; Koyano, A.; Omoto, R. Real time two-dimensional blood flow imaging using an autocorrelation technique. IEEE Trans. Sonics Ultrason.
**1985**, 32, 458–464. [Google Scholar] [CrossRef] - Newhouse, V.L.; Furgason, E.S.; Johnson, G.F.; Wolf, D.A. The dependence of ultrasound Doppler bandwidth on beam geometry. IEEE Trans Sonics Ultrason.
**1980**, 27, 50–59. [Google Scholar] [CrossRef] - Hoskins, P.R.; Fish, P.J.; Pye, S.D.; Anderson, T. Finite beam-width ray model for geometric spectral broadening. Ultrasound Med. Biol.
**1999**, 25, 391–404. [Google Scholar] [CrossRef] - Fish, P.J. Nonstationarity broadening in pulsed Doppler spectrum measurements. Ultrasound Med. Biol.
**1991**, 17, 147–155. [Google Scholar] [CrossRef] - Du, Y.; Ding, H.; He, L.; Deng, L.; Alfred, C.H.; Yiu, B.Y.; Zhu, L. Ultrasound vector flow imaging compared with phase contrast magnetic resonance imaging for estimating blood flow velocity and volume flow in the common carotid artery. In Proceedings of the 2021 IEEE International Ultrasonics Symposium (IUS), Xi’an, China, 11–16 September 2021. [Google Scholar]
- Hansen, K.L.; Møller-Sørensen, H.; Kjaergaard, J.; Jensen, M.B.; Lund, J.T.; Pedersen, M.M.; Lange, T.; Jensen, J.A.; Nielsen, M.B. Intra-operative vector flow imaging using ultrasound of the ascending aorta among 40 patients with normal, stenotic and replaced aortic valves. Ultrasound Med. Biol.
**2016**, 42, 2412–2422. [Google Scholar] [CrossRef] [PubMed] - Hansen, K.L.; Moller-Sorensen, H.; Kjaergaard, J.; Jensen, M.B.; Lund, J.T.; Pedersen, M.M.; Lange, T.; Jensen, J.A.; Nielsen, M.B. Aortic valve stenosis increase helical flow and flow complexity: A study of intra-operative cardiac vector flow imaging. Ultrasound Med. Biol.
**2017**, 43, 1607–1617. [Google Scholar] [CrossRef] [PubMed][Green Version] - Hansen, K.L.; Moller-Sorensen, H.; Kjaergaard, J.; Jensen, M.B.; Jensen, J.A.; Nielsen, M.B. Vector flow imaging of the ascending aorta in patients with tricuspid and bicuspid aortic valve stenosis treated with biological and mechanical implants. Ultrasound Med. Biol.
**2020**, 46, 64–72. [Google Scholar] [CrossRef][Green Version] - Holbek, S.; Ewertsen, C.; Bouzari, H.; Pihl, M.J.; Hansen, K.L.; Stuart, M.B.; Thomsen, C.; Nielsen, M.B.; Jensen, J.A. Ultrasonic 3-D vector flow method for quantitative in vivo peak velocity and flow rate estimation. IEEE Trans. Ultrason. Ferroelectr. Freq. Control
**2017**, 64, 544–554. [Google Scholar] [CrossRef][Green Version] - Holbek, S.; Hansen, K.L.; Bouzari, H.; Ewertsen, C.; Stuart, M.B.; Thomsen, C.; Nielsen, M.B.; Jensen, J.A. Common carotid artery flow measured by 3-D ultrasonic vector flow imaging and validated with magnetic resonance imaging. Ultrasound Med. Biol.
**2017**, 43, 2213–2220. [Google Scholar] [CrossRef]

**Figure 1.**PW measurements: (

**a**) big SV covering the vessel for measuring time-averaged mean velocity (TAMEAN) and volume flow (Vol Flow); (

**b**) small SV for measuring the maximum velocity (PS).

**Figure 2.**V Flow measurements: long ROI spanning the vessel diameter for measuring the maximum velocity (T-Max), time-averaged mean velocity (TAMean), and volume flow (Flow1).

**Figure 3.**PC-MRI measurements of both the left and right common carotid arteries for the maximum and time-averaged mean velocities, and volume flow rate (“Peak velocity”, “Mean velocity”, and “Mean flux” denoted in the figure).

**Figure 4.**Boxplot for the relative errors of PW and V Flow compared to PC-MRI for maximum velocity, mean velocity and volume flow measurements.

**Figure 5.**Linear regression plots of maximum velocities with 95% PI and 95% CI for PW and V Flow relative to PC-MRI.

**Figure 6.**Bland–Altman plots for illustrating the differences in the estimated maximum velocities for PW and V Flow relative to PC-MRI.

**Figure 7.**Linear regression plots of mean velocities with 95% PI and 95% CI for PW and V Flow relative to PC-MRI.

**Figure 8.**Bland–Altman plots for illustrating the differences in the estimated mean velocities for PW and V Flow relative to PC-MRI.

**Figure 9.**Linear regression plots of volume flow measurements with 95% PI and 95% CI for PW and V Flow relative to PC-MRI.

**Figure 10.**Bland–Altman plots for illustrating the differences in the estimated volume flow for PW and V Flow relative to PC-MRI.

**Table 1.**The mean error with standard deviation (Std), the median of absolute errors, and the r-value of V Flow and PW relative to the PC-MRI results.

Error [%]: Mean ± Std | Maximum Velocity | Mean Velocity | Volume Flow |
---|---|---|---|

PW | 53.44 ± 29.68 | 27.83 ± 31.60 | 21.01 ± 29.64 |

V Flow | 9.40 ± 14.91 | 21.52 ± 14.46 | −2.80 ± 14.01 |

Error [%]: Median | Maximum Velocity | Mean Velocity | Volume Flow |

PW | 49.79 | 23.83 | 25.48 |

V Flow | 11.84 | 19.28 | 10.38 |

r-Value (no. of Vessels) | Maximum Velocity | Mean Velocity | Volume Flow |

PW | 0.74 (60 CCAs) | 0.71 (61 CCAs) | 0.34 (61 CCAs) |

V Flow | 0.84 (61 CCAs) | 0.86 (61 CCAs) | 0.7 (61 CCAs) |

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**MDPI and ACS Style**

Du, Y.; Ding, H.; He, L.; Yiu, B.Y.S.; Deng, L.; Yu, A.C.H.; Zhu, L.
Quantitative Blood Flow Measurements in the Common Carotid Artery: A Comparative Study of High-Frame-Rate Ultrasound Vector Flow Imaging, Pulsed Wave Doppler, and Phase Contrast Magnetic Resonance Imaging. *Diagnostics* **2022**, *12*, 690.
https://doi.org/10.3390/diagnostics12030690

**AMA Style**

Du Y, Ding H, He L, Yiu BYS, Deng L, Yu ACH, Zhu L.
Quantitative Blood Flow Measurements in the Common Carotid Artery: A Comparative Study of High-Frame-Rate Ultrasound Vector Flow Imaging, Pulsed Wave Doppler, and Phase Contrast Magnetic Resonance Imaging. *Diagnostics*. 2022; 12(3):690.
https://doi.org/10.3390/diagnostics12030690

**Chicago/Turabian Style**

Du, Yigang, Haiyan Ding, Le He, Billy Y. S. Yiu, Linsong Deng, Alfred C. H. Yu, and Lei Zhu.
2022. "Quantitative Blood Flow Measurements in the Common Carotid Artery: A Comparative Study of High-Frame-Rate Ultrasound Vector Flow Imaging, Pulsed Wave Doppler, and Phase Contrast Magnetic Resonance Imaging" *Diagnostics* 12, no. 3: 690.
https://doi.org/10.3390/diagnostics12030690