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Annals of Biomedical Engineering

, Volume 43, Issue 12, pp 2911–2923 | Cite as

Neural Tissue Motion Impacts Cerebrospinal Fluid Dynamics at the Cervical Medullary Junction: A Patient-Specific Moving-Boundary Computational Model

  • Soroush Heidari Pahlavian
  • Francis Loth
  • Mark Luciano
  • John Oshinski
  • Bryn A. MartinEmail author
Article

Abstract

Central nervous system (CNS) tissue motion of the brain occurs over 30 million cardiac cycles per year due to intracranial pressure differences caused by the pulsatile blood flow and cerebrospinal fluid (CSF) motion within the intracranial space. This motion has been found to be elevated in type 1 Chiari malformation. The impact of CNS tissue motion on CSF dynamics was assessed using a moving-boundary computational fluid dynamics (CFD) model of the cervical-medullary junction (CMJ). The cerebellar tonsils and spinal cord were modeled as rigid surfaces moving in the caudocranial direction over the cardiac cycle. The CFD boundary conditions were based on in vivo MR imaging of a 35-year old female Chiari malformation patient with ~150–300 µm motion of the cerebellar tonsils and spinal cord, respectively. Results showed that tissue motion increased CSF pressure dissociation across the CMJ and peak velocities up to 120 and 60%, respectively. Alterations in CSF dynamics were most pronounced near the CMJ and during peak tonsillar velocity. These results show a small CNS tissue motion at the CMJ can alter CSF dynamics for a portion of the cardiac cycle and demonstrate the utility of CFD modeling coupled with MR imaging to help understand CSF dynamics.

Keywords

Cerebrospinal fluid Computational fluid dynamics Moving boundary simulation Central nervous system 

Abbreviations

CSF

Cerebrospinal fluid

CNS

Central nervous system

CMJ

Cervical-medullary junction

SAS

Subarachnoid space

CM

Chiari malformation

PCMRI

Phase-contrast magnetic resonance imaging

CFD

Computational fluid dynamics

FM

Foramen magnum

HR

Heart rate

ROI

Region of interest

FOV

Field of view

TR

Repetition time

TE

Echo time

SPACE

Sampling perfection with application optimized contrasts using different flip angle evolutions

ILI

Integrated longitudinal impedance

WSS

Wall shear stress

SBM

Static baseline model

DM

Dynamic model

SSM

Static systolic model

SDM

Static diastolic model

DENSE

Displacement encoded stimulated echo

FSI

Fluid–structure interaction

Notes

Acknowledgments

Authors would like to appreciate Conquer Chiari and National Institutes of Health (NIH) (Grant No. 1R15NS071455-01) for the support of this work. The authors also thank Nicholas Shaffer for helping with the post-processing of MRI data.

Conflict of interest

Authors have no conflict of interests.

Supplementary material

Supplementary material 1 (MOV 29453 kb)

References

  1. 1.
    Alperin, N., J. R. Loftus, C. J. Oliu, A. Bagci, S. H. Lee, B. Ertl-Wagner, B. Green, and R. Sekula. MRI measures of posterior cranial fossa morphology and csf physiology in chiari malformation Type I. Neurosurgery 2014.Google Scholar
  2. 2.
    Bertram, C. D., L. E. Bilston, and M. A. Stoodley. Tensile radial stress in the spinal cord related to arachnoiditis or tethering: a numerical model. Med. Biol. Eng. Comput. 46:701–707, 2008.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 4.
    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.CrossRefPubMedGoogle Scholar
  5. 5.
    Cirovic, S. A coaxial tube model of the cerebrospinal fluid pulse propagation in the spinal column. J. Biomech. Eng. 131:021008, 2009.CrossRefPubMedGoogle Scholar
  6. 6.
    Clarke, E. C., M. A. Stoodley, and L. E. Bilston. Changes in temporal flow characteristics of CSF in Chiari malformation Type I with and without syringomyelia: implications for theory of syrinx development Clinical article. J. Neurosurg. 118:1135–1140, 2013.CrossRefPubMedGoogle Scholar
  7. 7.
    Cousins, J., and V. Haughton. Motion of the cerebellar tonsils in the foramen magnum during the cardiac cycle. AJNR Am. J. Neuroradiol. 30:1587–1588, 2009.CrossRefPubMedGoogle Scholar
  8. 8.
    du Boulay, G., S. H. Shah, J. C. Currie, and V. Logue. The mechanism of hydromyelia in Chiari type 1 malformations. Br. J. Radiol. 47:579–587, 1974.CrossRefPubMedGoogle Scholar
  9. 9.
    Enzmann, D. R., and N. J. Pelc. Brain motion: measurement with phase-contrast MR imaging. Radiology 185:653–660, 1992.CrossRefPubMedGoogle Scholar
  10. 10.
    Feinberg, D. A., and A. S. Mark. Human brain motion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. Radiology 163:793–799, 1987.CrossRefPubMedGoogle Scholar
  11. 11.
    Franze, K., P. A. Janmey, and J. Guck. Mechanics in neuronal development and repair. Annu. Rev. Biomed. Eng. 15:227–251, 2013.CrossRefPubMedGoogle Scholar
  12. 12.
    Hajdu, S. I. A note from history: discovery of the cerebrospinal fluid. Ann. Clin. Lab. Sci. 33:334–336, 2003.PubMedGoogle Scholar
  13. 13.
    Heiss, J. D., G. Suffredini, R. Smith, H. L. DeVroom, N. J. Patronas, J. A. Butman, F. Thomas, and E. H. Oldfield. Pathophysiology of persistent syringomyelia after decompressive craniocervical surgery. Clinical article. J. Neurosurg. Spine 13:729–742, 2010.CrossRefPubMedGoogle Scholar
  14. 14.
    Hofmann, E., M. Warmuth-Metz, M. Bendszus, and L. Solymosi. Phase-contrast MR imaging of the cervical CSF and spinal cord: volumetric motion analysis in patients with Chiari I malformation. AJNR Am. J. Neuroradiol. 21:151–158, 2000.PubMedGoogle Scholar
  15. 15.
    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. Anesth. Analg. 115:386–394, 2012.CrossRefPubMedGoogle Scholar
  16. 16.
    Kalata, W., B. A. Martin, J. N. Oshinski, M. Jerosch-Herold, T. J. Royston, and F. Loth. MR measurement of cerebrospinal fluid velocity wave speed in the spinal canal. IEEE Trans. Biomed. Eng. 56:1765–1768, 2009.CrossRefPubMedGoogle Scholar
  17. 17.
    Lee, L. Riding the wave of ependymal cilia: genetic susceptibility to hydrocephalus in primary ciliary dyskinesia. J. Neurosci. Res. 91:1117–1132, 2013.CrossRefPubMedGoogle Scholar
  18. 18.
    Loth, F., M. A. Yardimci, and N. Alperin. Hydrodynamic modeling of cerebrospinal fluid motion within the spinal cavity. J. Biomech. Eng. 123:71–79, 2001.PubMedGoogle Scholar
  19. 19.
    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 132, 2010.Google Scholar
  20. 20.
    Martin, B. A., W. Kalata, F. Loth, T. J. Royston, and J. N. Oshinski. Syringomyelia hydrodynamics: an in vitro study based on in vivo measurements. J. Biomech. Eng. Trans. ASME 127:1110–1120, 2005.CrossRefGoogle Scholar
  21. 21.
    Martin, B. A., W. Kalata, N. Shaffer, P. Fischer, M. Luciano, and F. Loth. Hydrodynamic and longitudinal impedance analysis of cerebrospinal fluid dynamics at the craniovertebral junction in type I Chiari malformation. PLoS ONE 8:e75335, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Nitz, W. R., W. G. Bradley, Jr, A. S. Watanabe, R. R. Lee, B. Burgoyne, R. M. O’Sullivan, and M. D. Herbst. Flow dynamics of cerebrospinal fluid: assessment with phase-contrast velocity MR imaging performed with retrospective cardiac gating. Radiology 183:395–405, 1992.CrossRefPubMedGoogle Scholar
  23. 23.
    Oldfield, E. H., K. Muraszko, T. H. Shawker, and N. J. Patronas. Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. J. Neurosurg. 80:3–15, 1994.CrossRefPubMedGoogle Scholar
  24. 24.
    Pahlavian, S. H., 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. doi: 10.1371/journal.pone.0091888.
  25. 25.
    Patankar, S. Numerical Heat Transfer and Fluid Flow. Taylor & Francis, 1980.Google Scholar
  26. 26.
    Pujol, J., C. Roig, A. Capdevila, A. Pou, J. L. Marti-Vilalta, J. Kulisevsky, A. Escartin, and G. Zannoli. Motion of the cerebellar tonsils in Chiari type I malformation studied by cine phase-contrast MRI. Neurology 45:1746–1753, 1995.CrossRefPubMedGoogle Scholar
  27. 27.
    Quigley, M. F., B. Iskandar, M. E. Quigley, M. Nicosia, and V. Haughton. Cerebrospinal fluid flow in foramen magnum: temporal and spatial patterns at MR imaging in volunteers and in patients with Chiari I malformation. Radiology 232:229–236, 2004.CrossRefPubMedGoogle Scholar
  28. 28.
    Shaffer, N., B. A. Martin, B. Rocque, C. Madura, O. Wieben, B. J. Iskandar, S. Dombrowski, M. Luciano, J. N. Oshinski, and F. Loth. Cerebrospinal fluid flow impedance is elevated in type I chiari malformation. J. Biomech. Eng. Trans. ASME 136:021012, 2014. doi: 10.1115/1.4026316.
  29. 29.
    Stockman, H. W. Effect of anatomical fine structure on the flow of cerebrospinal fluid in the spinal subarachnoid space. J. Biomech. Eng. 128:106–114, 2006.CrossRefPubMedGoogle Scholar
  30. 30.
    Terae, S., K. Miyasaka, S. Abe, H. Abe, and K. Tashiro. Increased pulsatile movement of the hindbrain in syringomyelia associated with the Chiari malformation: cine-MRI with presaturation bolus tracking. Neuroradiology 36:125–129, 1994.CrossRefPubMedGoogle Scholar
  31. 31.
    Williams, H. A unifying hypothesis for hydrocephalus, Chiari malformation, syringomyelia, anencephaly and spina bifida. Cerebrospinal Fluid Res. 5:7, 2008.PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Wolpert, S. M., R. A. Bhadelia, A. R. Bogdan, and A. R. Cohen. Chiari I malformations: assessment with phase-contrast velocity MR. AJNR Am. J. Neuroradiol. 15:1299–1308, 1994.PubMedGoogle Scholar
  33. 33.
    Wright, B. L., J. T. Lai, and A. J. Sinclair. Cerebrospinal fluid and lumbar puncture: a practical review. J. Neurol. 259:1530–1545, 2012.CrossRefPubMedGoogle Scholar
  34. 34.
    Yiallourou, T. I., J. R. Kroger, N. Stergiopulos, D. Maintz, B. A. Martin, and A. C. Bunck. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Zamir, M. The Physics of Coronary Blood Flow. New York: Springer, 2010.Google Scholar
  36. 36.
    Zhong, X., C. H. Meyer, D. J. Schlesinger, J. P. Sheehan, F. H. Epstein, J. M. Larner, S. H. Benedict, P. W. Read, K. Sheng, and J. Cai. Tracking brain motion during the cardiac cycle using spiral cine-DENSE MRI. Med. Phys. 36:3413–3419, 2009.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2015

Authors and Affiliations

  • Soroush Heidari Pahlavian
    • 1
    • 2
  • Francis Loth
    • 1
    • 2
  • Mark Luciano
    • 3
  • John Oshinski
    • 4
  • Bryn A. Martin
    • 1
    • 2
    Email author
  1. 1.Conquer Chiari Research Center, Department of Mechanical EngineeringThe University of AkronAkronUSA
  2. 2.Department of Mechanical EngineeringThe University of AkronAkronUSA
  3. 3.Department of Pediatric NeurosurgeryCleveland Clinic FoundationClevelandUSA
  4. 4.Department of RadiologyEmory UniversityAtlantaUSA

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