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In Vitro Assessment of Flow Variability in an Intracranial Aneurysm Model Using 4D Flow MRI and Tomographic PIV

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A Correction to this article was published on 09 January 2023

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Abstract

Aneurysm rupture has been suggested to be related to aneurysm geometry, morphology, and complex flow activity; therefore, understanding aneurysm-specific hemodynamics is crucial. 4D Flow MRI has been shown to be a feasible tool for assessing hemodynamics in intracranial aneurysms with high spatial resolution. However, it requires averaging over multiple heartbeats and cannot account for cycle-to-cycle hemodynamics variations. This study aimed to assess cycle-to-cycle flow dynamics variations in a patient-specific intracranial aneurysm model using tomographic particle image velocimetry (tomo-PIV) at a high image rate under pulsatile flow conditions. Time-resolved and time-averaged velocity flow fields within the aneurysm sac and estimations of wall shear stress (WSS) were compared with those from 4D Flow MRI. A one-way ANOVA showed a significant difference between cardiac cycles (p value < 0.0001); however, differences were not significant after PIV temporal and spatial resolution was matched to that of MRI (p value 0.9727). This comparison showed the spatial resolution to be the main contributor to assess cycle-to-cycle variability. Furthermore, the comparison with 4D Flow MRI between velocity components, streamlines, and estimated WSS showed good qualitative and quantitative agreement. This study showed the feasibility of patient-specific in-vitro experiments using tomo-PIV to assess 4D Flow MRI with high repeatability in the measurements.

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References

  1. Bieging, E. T., A. Frydrychowicz, A. Wentland, B. R. Landgraf, K. M. Johnson, O. Wieben, and C. J. François. In vivo three-dimensional mr wall shear stress estimation in ascending aortic dilatation. J. Magn. Reson. Imaging 33:589–597, 2011.

    Article  Google Scholar 

  2. Brindise, M. C., S. Rothenberger, B. Dickerhoff, S. Schnell, M. Markl, D. Saloner, V. L. Rayz, and P. P. Vlachos. Multi-modality cerebral aneurysm haemodynamic analysis: in vivo 4D flow MRI, in vitro volumetric particle velocimetry and in silico computational fluid dynamics. J. R. Soc. Interface 16:20190465, 2019.

    Article  CAS  Google Scholar 

  3. Buchmann, N. A., C. Atkinson, M. C. Jeremy, and J. Soria. Tomographic particle image velocimetry investigation of the flow in a modeled human carotid artery bifurcation. Exp. Fluids 50:1131–1151, 2011.

    Article  CAS  Google Scholar 

  4. Chang, W., A. Frydrychowicz, S. Kecskemeti, B. Landgraf, K. Johnson, Y. Wu, O. Wieben, C. Mistretta, and P. Turski. The effect of spatial resolution on wall shear stress measurements acquired using radial phase contrast magnetic resonance angiography in the middle cerebral arteries of healthy volunteers: preliminary results. Neuroradiol. J. 24:115–120, 2011.

    Article  CAS  Google Scholar 

  5. Elkins, C. J., and M. T. Alley. Magnetic resonance velocimetry: applications of magnetic resonance imaging in the measurement of fluid motion. Exp. Fluids 43:823–858, 2007.

    Article  CAS  Google Scholar 

  6. Elsinga, G. E., F. Scarano, B. Wieneke, and B. W. Van Oudheusden. Tomographic particle image velocimetry. Exp. Fluids 41:933–947, 2006.

    Article  Google Scholar 

  7. Ford, M. D., H. N. Nikolov, J. S. Milner, S. P. Lownie, E. M. Demont, W. Kalata, F. Loth, D. W. Holdsworth, and D. A. Steinman. PIV-measured versus CFD-predicted flow dynamics in anatomically realistic cerebral aneurysm models. J. Biomech. Eng. 130:021015, 2008.

    Article  Google Scholar 

  8. Frayne, R., and B. K. Rutt. Understanding acceleration-induced displacement artifacts in phase-contrast MR velocity measurements. J. Magn. Reson. Imaging 5:207–215, 1995.

    Article  CAS  Google Scholar 

  9. Frydrychowicz, A., A. Roldán-Alzate, E. Winslow, D. Consigny, C. A. Campo, U. Motosugi, K. M. Johnson, O. Wieben, and S. B. Reeder. Comparison of radial 4D flow-MRI with perivascular ultrasound to quantify blood flow in the abdomen and introduction of a porcine model of pre-hepatic portal hypertension. Eur. Radiol. 27:5316–5324, 2017.

    Article  CAS  Google Scholar 

  10. Gatehouse, P. D., J. Keegan, L. A. Crowe, S. Masood, R. H. Mohiaddin, K. F. Kreitner, and D. N. Firmin. Applications of phase-contrast flow and velocity imaging in cardiovascular MRI. Eur. Radiol. 15:2172–2184, 2005.

    Article  Google Scholar 

  11. Cerebral, J., and E. Ollikainen. B. J. C. flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall. AJNR Am J Neuroradiol 2017. https://doi.org/10.1001/jama.1953.02940200020005.

    Article  Google Scholar 

  12. Johnson, K. M., and M. Markl. Improved SNR in phase contrast velocimetry with five-point balanced flow encoding. Magn. Reson. Med. 63:349–355, 2010.

    Article  Google Scholar 

  13. Kang, H., W. Ji, Z. Qian, Y. Li, C. Jiang, Z. Wu, X. Wen, W. Xu, and A. Liu. Aneurysm characteristics associated with the rupture risk of intracranial aneurysms: a self-controlled study. PLoS ONE 10:1–10, 2015.

    Article  Google Scholar 

  14. Keedy, A. An overview of intracranial aneurysms. McGill J. Med. 9:141–146, 2006.

    Google Scholar 

  15. Kouwenhoven, M., M. B. M. Hofman, and M. Sprenger. Motion induced phase shifts in MR: acceleration effects in quantitative flow measurements—a reconsideration. Magn. Reson. Med. 33:766–777, 1995.

    Article  CAS  Google Scholar 

  16. Markl, M., A. Frydrychowicz, S. Kozerke, M. Hope, and O. Wieben. 4D flow MRI. J. Magn. Reson. Imaging 36:1015–1036, 2012.

    Article  Google Scholar 

  17. Meckel, S., L. Leitner, L. H. Bonati, F. Santini, T. Schubert, A. F. Stalder, P. Lyrer, M. Markl, and S. G. Wetzel. Intracranial artery velocity measurement using 4D PC MRI at 3 T: comparison with transcranial ultrasound techniques and 2D PC MRI. Neuroradiology 55:389–398, 2013.

    Article  Google Scholar 

  18. Medero, R., C. Hoffman, and A. Roldán-Alzate. Comparison of 4D flow MRI and particle image velocimetry using an in vitro carotid bifurcation model. Ann. Biomed. Eng. 2018. https://doi.org/10.1007/s10439-018-02109-9.

    Article  Google Scholar 

  19. van Ooij, P., A. Guédon, C. Poelma, J. Schneiders, M. C. M. Rutten, H. A. Marquering, C. B. Majoie, E. van Bavel, and A. J. Nederveen. Complex flow patterns in a real-size intracranial aneurysm phantom: phase contrast MRI compared with particle image velocimetry and computational fluid dynamics. NMR Biomed. 25:14–26, 2012.

    Article  Google Scholar 

  20. Qiu, T., G. Jin, H. Xing, and H. Lu. Association between hemodynamics, morphology, and rupture risk of intracranial aneurysms: a computational fluid modeling study. Neurol. Sci. 38:1009–1018, 2017.

    Article  Google Scholar 

  21. Rinkel, G. J. E., M. Djibuti, A. Algra, and J. van Gijn. Prevalence and risk of rupture of intracranial aneurysms. Stroke 29:251–256, 1998.

    Article  CAS  Google Scholar 

  22. Roldán-Alzate, A., S. García-Rodríguez, P. V. Anagnostopoulos, S. Srinivasan, O. Wieben, and C. J. François. Hemodynamic study of TCPC using in vivo and in vitro 4D flow MRI and numerical simulation. J. Biomech. 48:1325–1330, 2015.

    Article  Google Scholar 

  23. Roloff, C., D. Stucht, O. Beuing, and P. Berg. Comparison of intracranial aneurysm flow quantification techniques: standard PIV vs stereoscopic PIV vs tomographic PIV vs phase-contrast MRI vs CFD. J. Neurointerv. Surg. Neurintsurg 2018. https://doi.org/10.1136/neurintsurg-2018-013921.

    Article  Google Scholar 

  24. Falk, K. L., R. Medero, and A. Roldán-Alzate. Fabrication of low-cost patient-specific vascular models for particle image velocimetry. Cardiovasc. Eng. Technol. 10:500–507, 2019.

    Article  Google Scholar 

  25. Scarano, F. Tomographic PIV: principles and practice. Meas. Sci. Technol. 2013. https://doi.org/10.1088/0957-0233/24/1/012001.

    Article  Google Scholar 

  26. Schnell, S., S. A. Ansari, P. Vakil, M. Wasielewski, M. L. Carr, M. C. Hurley, B. R. Bendok, H. Batjer, T. J. Carroll, J. Carr, and M. Markl. Three-dimensional hemodynamics in intracranial aneurysms: influence of size and morphology. J. Magn. Reson. Imaging 39:120–131, 2014.

    Article  Google Scholar 

  27. Sciacchitano, A., and B. Wieneke. PIV uncertainty propagation. Meas Sci Technol 2016. https://doi.org/10.1088/0957-0233/27/8/084006.

    Article  Google Scholar 

  28. Stankovic, Z., B. D. Allen, J. Garcia, K. B. Jarvis, and M. Markl. 4D flow imaging with MRI. Cardiovasc. Diagn. Ther. 4:173–192, 2014.

    Google Scholar 

  29. Stankovic, Z., Z. Csatari, P. Deibert, W. Euringer, B. Jung, W. Kreisel, J. Geiger, M. F. Russe, M. Langer, and M. Markl. A feasibility study to evaluate splanchnic arterial and venous hemodynamics by flow-sensitive 4D MRI compared with Doppler ultrasound in patients with cirrhosis and controls. Eur. J. Gastroenterol. Hepatol. 25:669–675, 2013.

    Article  Google Scholar 

  30. Ugron, Á., M. I. Farinas, L. Kiss, and G. Paál. Unsteady velocity measurements in a realistic intracranial aneurysm model. Exp. Fluids 52:37–52, 2012.

    Article  Google Scholar 

  31. Wentland, A. L., T. M. Grist, and O. Wieben. Repeatability and internal consistency of abdominal 2D and 4D phase contrast MR flow measurements. Acad. Radiol. 20:699–704, 2013.

    Article  Google Scholar 

  32. Wieneke, B. Volume self-calibration for 3D particle image velocimetry. Exp. Fluids 45:549–556, 2008.

    Article  Google Scholar 

  33. Yagi, T., A. Sato, M. Shinke, S. Takahashi, Y. Tobe, H. Takao, Y. Murayama, and M. Umezu. Experimental insights into flow impingement in cerebral aneurysm by stereoscopic particle image velocimetry: transition from a laminar regime. J. R. Soc. Interface 2013. https://doi.org/10.1098/rsif.2012.1031.

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the Medical Physics Department for the MRI acquisition support at the University of Wisconsin-Madison, Carson Hoffman for his assistance with writing scripts in MATLAB, and Dr. Charles Strother for his critical comments preparing the manuscript. This study was partially supported by a K12 Career Development Award, K12DK100022. Funding was provided by American Heart Association (Grant No. 14SDG19690010).

Conflict of interest

The authors state that there are no conflicts of interest related to this research study.

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Authors and Affiliations

  1. Department of Mechanical Engineering, University of Wisconsin-Madison, Madison, WI, USA

    Rafael Medero, David Rutkowski & Alejandro Roldán-Alzate

  2. Department of Radiology, University of Wisconsin-Madison, WIMR 2476, 1111 Highland Ave, Madison, WI, 53705, USA

    Rafael Medero, David Rutkowski & Alejandro Roldán-Alzate

  3. Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, WI, USA

    Katrina Falk & Alejandro Roldán-Alzate

  4. School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI, USA

    Katrina Falk

  5. Department of Medical Physics, University of Wisconsin-Madison, Madison, WI, USA

    Kevin Johnson

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Correspondence to Alejandro Roldán-Alzate.

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Medero, R., Falk, K., Rutkowski, D. et al. In Vitro Assessment of Flow Variability in an Intracranial Aneurysm Model Using 4D Flow MRI and Tomographic PIV. Ann Biomed Eng 48, 2484–2493 (2020). https://doi.org/10.1007/s10439-020-02543-8

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  • DOI: https://doi.org/10.1007/s10439-020-02543-8

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