Skip to main content
Springer Nature Link
Log in

Accuracy of 4D Flow Measurement of Cerebrospinal Fluid Dynamics in the Cervical Spine: An In Vitro Verification Against Numerical Simulation

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Abnormal alterations in cerebrospinal fluid (CSF) flow are thought to play an important role in pathophysiology of various craniospinal disorders such as hydrocephalus and Chiari malformation. Three directional phase contrast MRI (4D Flow) has been proposed as one method for quantification of the CSF dynamics in healthy and disease states, but prior to further implementation of this technique, its accuracy in measuring CSF velocity magnitude and distribution must be evaluated. In this study, an MR-compatible experimental platform was developed based on an anatomically detailed 3D printed model of the cervical subarachnoid space and subject specific flow boundary conditions. Accuracy of 4D Flow measurements was assessed by comparison of CSF velocities obtained within the in vitro model with the numerically predicted velocities calculated from a spatially averaged computational fluid dynamics (CFD) model based on the same geometry and flow boundary conditions. Good agreement was observed between CFD and 4D Flow in terms of spatial distribution and peak magnitude of through-plane velocities with an average difference of 7.5 and 10.6% for peak systolic and diastolic velocities, respectively. Regression analysis showed lower accuracy of 4D Flow measurement at the timeframes corresponding to low CSF flow rate and poor correlation between CFD and 4D Flow in-plane velocities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9

Similar content being viewed by others

Abbreviations

CSF:

Cerebrospinal fluid

CNS:

Central nervous system

SAS:

Subarachnoid space

PCMRI:

Phase-contrast magnetic resonance imaging

CFD:

Computational fluid dynamics

FM:

Foramen magnum

TR:

Repetition time

TE:

Echo time

VENC:

Encoding velocity

VNR:

Velocity to noise ratio

References

  1. Alleyne, Jr, C. H., C. M. Cawley, D. L. Barrow, and G. D. Bonner. Microsurgical anatomy of the dorsal cervical nerve roots and the cervical dorsal root ganglion/ventral root complexes. Surg. Neurol. 50:213–218, 1998.

    Article  PubMed  Google Scholar 

  2. Bernstein, M. A., X. J. Zhou, J. A. Polzin, K. F. King, A. Ganin, N. J. Pelc, and G. H. Glover. Concomitant gradient terms in phase contrast MR: analysis and correction. Magn. Reson. Med. 39:300–308, 1998.

    Article  CAS  PubMed  Google Scholar 

  3. Bloomfield, I. G., I. H. Johnston, and L. E. Bilston. Effects of proteins, blood cells and glucose on the viscosity of cerebrospinal fluid. Pediatr. Neurosurg. 28:246–251, 1998.

    Article  CAS  PubMed  Google Scholar 

  4. Bradley, Jr, W. G., D. Scalzo, J. Queralt, W. N. Nitz, D. J. Atkinson, and P. Wong. Normal-pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 198:523–529, 1996.

    Article  PubMed  Google Scholar 

  5. Bunck, A. C., J. R. Kroeger, A. Juettner, A. Brentrup, B. Fiedler, G. R. Crelier, B. A. Martin, W. Heindel, D. Maintz, W. Schwindt, and T. Niederstadt. Magnetic resonance 4D flow analysis of cerebrospinal fluid dynamics in Chiari I malformation with and without syringomyelia. Eur. Radiol. 22:1860–1870, 2012.

    Article  PubMed  Google Scholar 

  6. Bunck, A. C., J. R. Kroger, A. Juttner, A. Brentrup, B. Fiedler, F. Schaarschmidt, G. R. Crelier, W. Schwindt, W. Heindel, T. Niederstadt, and D. Maintz. Magnetic resonance 4D flow characteristics of cerebrospinal fluid at the craniocervical junction and the cervical spinal canal. Eur. Radiol. 21:1788–1796, 2011.

    Article  PubMed  Google Scholar 

  7. Busch, J., D. Giese, L. Wissmann, and S. Kozerke. Reconstruction of divergence-free velocity fields from cine 3D phase-contrast flow measurements. Magn. Reson. Med. 69:200–210, 2013.

    Article  PubMed  Google Scholar 

  8. Canstein, C., P. Cachot, A. Faust, A. F. Stalder, J. Bock, A. Frydrychowicz, J. Kuffer, J. Hennig, and M. Markl. 3D MR flow analysis in realistic rapid-prototyping model systems of the thoracic aorta: comparison with in vivo data and computational fluid dynamics in identical vessel geometries. Magn. Reson. Med. 59:535–546, 2008.

    Article  CAS  PubMed  Google Scholar 

  9. Clarke, E. C., D. F. Fletcher, M. A. Stoodley, and L. E. Bilston. Computational fluid dynamics modelling of cerebrospinal fluid pressure in Chiari malformation and syringomyelia. J. Biomech. 46:1801–1809, 2013.

    Article  PubMed  Google Scholar 

  10. Giese, D., M. Haeberlin, C. Barmet, K. P. Pruessmann, T. Schaeffter, and S. Kozerke. Analysis and correction of background velocity offsets in phase-contrast flow measurements using magnetic field monitoring. Magn. Reson. Med. 67:1294–1302, 2012.

    Article  PubMed  Google Scholar 

  11. Ha, H., G. B. Kim, J. Kweon, Y.-H. Kim, N. Kim, D. H. Yang, and S. J. Lee. Multi-VENC acquisition of four-dimensional phase-contrast MRI to improve precision of velocity field measurement. Magn. Reson. Med., 2015. doi:10.1002/mrm.25715.

    Google Scholar 

  12. Hayashi, N., M. Matsumae, S. Yatsushiro, A. Hirayama, A. Abdullah, and K. Kuroda. Quantitative analysis of cerebrospinal fluid pressure gradients in healthy volunteers and patients with normal pressure hydrocephalus. Neurol. Med. Chir. (Tokyo) 55:657–662, 2015.

    Article  Google Scholar 

  13. Heidari Pahlavian, S., A. C. Bunck, F. Loth, R. Shane Tubbs, T. Yiallourou, J. R. Kroeger, W. Heindel, and B. A. Martin. Characterization of the discrepancies between four-dimensional phase-contrast magnetic resonance imaging and in silico simulations of cerebrospinal fluid dynamics. J Biomech Eng 137:051002, 2015.

    Article  PubMed  Google Scholar 

  14. Heidari Pahlavian, S., T. Yiallourou, R. S. Tubbs, A. C. Bunck, F. Loth, M. Goodin, M. Raisee, and B. A. Martin. The impact of spinal cord nerve roots and denticulate ligaments on cerebrospinal fluid dynamics in the cervical spine. PLoS ONE 9:e91888, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Helgeland, A., K. A. Mardal, V. Haughton, and B. A. Reif. Numerical simulations of the pulsating flow of cerebrospinal fluid flow in the cervical spinal canal of a Chiari patient. J. Biomech. 47:1082–1090, 2014.

    Article  PubMed  Google Scholar 

  16. Hsu, Y., H. D. Hettiarachchi, D. C. Zhu, and A. A. Linninger. The frequency and magnitude of cerebrospinal fluid pulsations influence intrathecal drug distribution: key factors for interpatient variability (vol 115, pg 386, 2012). Anesth. Analg. 115:879–879, 2012.

    Article  Google Scholar 

  17. Iliff, J. J., M. Wang, Y. Liao, B. A. Plogg, W. Peng, G. A. Gundersen, H. Benveniste, G. E. Vates, R. Deane, S. A. Goldman, E. A. Nagelhus, and M. Nedergaard. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4:147ra111, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Jacobs, P. F., D. T. Reid, and Computer and A. S. A. o. SME. Rapid Prototyping & Manufacturing: Fundamentals of Stereolithography. Dearborn: Society of Manufacturing Engineers, 1992.

    Google Scholar 

  19. Jones, C. F., J. H. Lee, B. K. Kwon, and P. A. Cripton. Development of a large-animal model to measure dynamic cerebrospinal fluid pressure during spinal cord injury: laboratory investigation. J. Neurosurg. Spine. 16:624–635, 2012.

    Article  PubMed  Google Scholar 

  20. Kress, B. T., J. J. Iliff, M. Xia, M. Wang, H. S. Wei, D. Zeppenfeld, L. Xie, H. Kang, Q. Xu, J. A. Liew, B. A. Plog, F. Ding, R. Deane, and M. Nedergaard. Impairment of paravascular clearance pathways in the aging brain. Ann. Neurol. 76:845–861, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ku, J. P., C. J. Elkins, and C. A. Taylor. Comparison of CFD and MRI flow and velocities in an in vitro large artery bypass graft model. Ann. Biomed. Eng. 33:257–269, 2005.

    Article  PubMed  Google Scholar 

  22. Lagana, M. M., A. Chaudhary, D. Balagurunathan, D. Utriainen, P. Kokeny, W. Feng, P. Cecconi, D. Hubbard, and E. M. Haacke. Cerebrospinal fluid flow dynamics in multiple sclerosis patients through phase contrast magnetic resonance imaging. Curr. Neurovasc. Res. 11:349–358, 2014.

    Article  PubMed  Google Scholar 

  23. Markl, M., R. Bammer, M. Alley, C. Elkins, M. Draney, A. Barnett, M. Moseley, G. Glover, and N. Pelc. Generalized reconstruction of phase contrast MRI: analysis and correction of the effect of gradient field distortions. Magn. Reson. Med. 50:791–801, 2003.

    Article  CAS  PubMed  Google Scholar 

  24. Martin, B. A., R. Labuda, T. J. Royston, J. N. Oshinski, B. Iskandar, and F. Loth. Spinal subarachnoid space pressure measurements in an in vitro spinal stenosis model: implications on syringomyelia theories. J. Biomech. Eng. Trans. Asme. (2010). doi:10.1115/1.4000089.

    PubMed  Google Scholar 

  25. Martin, B. A., T. I. Yiallourou, S. H. Pahlavian, S. Thyagaraj, A. C. Bunck, F. Loth, D. B. Sheffer, J. R. Kroger, and N. Stergiopulos. Inter-operator reliability of magnetic resonance image-based computational fluid dynamics prediction of cerebrospinal fluid motion in the cervical spine. Ann. Biomed. Eng. 43:1–14, 2015.

    Article  Google Scholar 

  26. McCauley, T. R., C. S. Pena, C. K. Holland, T. B. Price, and J. C. Gore. Validation of volume flow measurements with cine phase-contrast MR imaging for peripheral arterial waveforms. J. Magn. Reson. Imaging 5:663–668, 1995.

    Article  CAS  PubMed  Google Scholar 

  27. Nelissen, R. M. Fluid Mechanics of Intrathecal Drug Delivery, Doctoral Thesis. EPFL, Lausanne, Switzerland: Citeseer, 2008.

  28. Ong, F., M. Uecker, U. Tariq, A. Hsiao, M. T. Alley, S. S. Vasanawala, and M. Lustig. Robust 4D flow denoising using divergence-free wavelet transform. Magn. Reson. Med. 73:828–842, 2015.

    Article  PubMed  Google Scholar 

  29. Papisov, M. I., V. V. Belov, and K. S. Gannon. Physiology of the intrathecal bolus: the leptomeningeal route for macromolecule and particle delivery to CNS. Mol. Pharm. 10(5):1522–1532, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Silverberg, G., M. Mayo, T. Saul, J. Fellmann, and D. McGuire. Elevated cerebrospinal fluid pressure in patients with Alzheimer’s disease. Cerebrospinal. Fluid Res. 3:7, 2006.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Simpson, K., G. Baranidharan, and S. Gupta. Spinal Interventions in Pain Management. UK: Oxford University Press, 2012.

    Book  Google Scholar 

  32. Stadlbauer, A., E. Salomonowitz, C. Brenneis, K. Ungersbock, W. van der Riet, M. Buchfelder, and O. Ganslandt. Magnetic resonance velocity mapping of 3D cerebrospinal fluid flow dynamics in hydrocephalus: preliminary results. Eur. Radiol. 22:232–242, 2012.

    Article  PubMed  Google Scholar 

  33. Traber, J., L. Wurche, M. A. Dieringer, W. Utz, F. von Knobelsdorff-Brenkenhoff, A. Greiser, N. Jin, and J. Schulz-Menger. Real-time phase contrast magnetic resonance imaging for assessment of haemodynamics: from phantom to patients. Eur. Radiol. 26:986–996, 2015.

    Article  PubMed  Google Scholar 

  34. Walker, P. G., G. B. Cranney, M. B. Scheidegger, G. Waseleski, G. M. Pohost, and A. P. Yoganathan. Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J. Magn. Reson. Imaging 3:521–530, 1993.

    Article  CAS  PubMed  Google Scholar 

  35. Wostyn, P., K. Audenaert, and P. P. De Deyn. More advanced Alzheimer’s disease may be associated with a decrease in cerebrospinal fluid pressure. Cerebrospinal Fluid Res. 6:14, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Yiallourou, T. I., J. R. Kroger, N. Stergiopulos, D. Maintz, A. C. Bunck, and B. A. Martin. Comparison of 4D phase-contrast MRI flow measurements to computational fluid dynamics simulations of cerebrospinal fluid motion in the cervical spine. PLoS ONE 7:e52284, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yushkevich, P. A., J. Piven, H. C. Hazlett, R. G. Smith, S. Ho, J. C. Gee, and G. Gerig. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128, 2006.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Authors would like to appreciate Conquer Chiari and American Syringomyelia Alliance Project for the support of this work. Authors would also like to acknowledge Dr. Jae-Won Choi and Dr. Morteza Vatani for the helpful discussions and assistance in the rapid-prototyping of the phantom model.

Conflict of interest

Authors have no conflict of interests.

Author information

Authors and Affiliations

  1. Conquer Chiari Research Center, The University of Akron, Akron, OH, USA

    Soroush Heidari Pahlavian, Suraj Thyagaraj & Francis Loth

  2. Department of Mechanical Engineering, The University of Akron, Akron, OH, USA

    Soroush Heidari Pahlavian, Suraj Thyagaraj & Francis Loth

  3. Department of Radiology, University Hospital of Cologne, Cologne, Germany

    Alexander C. Bunck, Daniel Giese & Dennis M. Hedderich

  4. Department of Radiology, University Hospital of Muenster, Muenster, Germany

    Alexander C. Bunck & Jan Robert Kröger

  5. Department of Biological Engineering, The University of Idaho, 875 Perimeter Drive MS 0904, Moscow, ID, 83844-0904, USA

    Bryn A. Martin

Authors
  1. Soroush Heidari Pahlavian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander C. Bunck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suraj Thyagaraj
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel Giese
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francis Loth
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dennis M. Hedderich
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jan Robert Kröger
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bryn A. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bryn A. Martin.

Additional information

Associate Editor Agata A. Exner oversaw the review of this article.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Heidari Pahlavian, S., Bunck, A.C., Thyagaraj, S. et al. Accuracy of 4D Flow Measurement of Cerebrospinal Fluid Dynamics in the Cervical Spine: An In Vitro Verification Against Numerical Simulation. Ann Biomed Eng 44, 3202–3214 (2016). https://doi.org/10.1007/s10439-016-1602-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-016-1602-x

Keywords

Search

Navigation