An MRI-Compatible Hydrodynamic Simulator of Cerebrospinal Fluid Motion in the Cervical Spine

Goal: Develop and test an MRI-compatible hydrodynamic simulator of cerebrospinal fluid (CSF) motion in the cervical spinal subarachnoid space. Four anatomically realistic subject-specific models were created based on a 22-year-old healthy volunteer and a five-year-old patient diagnosed with Chiari I malformation. Methods : The in vitro models were based on manual segmentation of high-resolution T2-weighted MRI of the cervical spine. Anatomically realistic dorsal and ventral spinal cord nerve rootlets (NR) were added. Models were three dimensional (3-D) printed by stereolithography with 50-μm layer thickness. A computer controlled pump system was used to replicate the shape of the subject specific in vivo CSF flow measured by phase-contrast MRI. Each model was then scanned by T2-weighted and 4-D phase contrast MRI (4D flow). Results: Cross-sectional area, wetted perimeter, and hydraulic diameter were quantified for each model. The oscillatory CSF velocity field (flow jets near NR, velocity profile shape, and magnitude) had similar characteristics to previously reported studies in the literature measured by in vivo MRI. Conclusion: This study describes the first MRI-compatible hydrodynamic simulator of CSF motion in the cervical spine with anatomically realistic NR. NR were found to impact CSF velocity profiles to a great degree. Significance: CSF hydrodynamics are thought to be altered in craniospinal disorders such as Chiari I malformation. MRI scanning techniques and protocols can be used to quantify CSF flow alterations in disease states. The provided in vitro models can be used to test the reliability of these protocols across MRI scanner manufacturers and machines.

[1]  Johannes Lang,et al.  Clinical Anatomy of the Cervical Spine , 1993 .

[2]  David N. Firmin,et al.  Rapid 7-dimensional imaging of pulsatile flow , 1993, Proceedings of Computers in Cardiology Conference.

[3]  I. Idy-Peretti,et al.  Cerebrospinal Fluid Dynamics and Relation with Blood Flow: A Magnetic Resonance Study with Semiautomated Cerebrospinal Fluid Segmentation , 2001, Investigative radiology.

[4]  V. Haughton,et al.  Cerebrospinal fluid flow in foramen magnum: temporal and spatial patterns at MR imaging in volunteers and in patients with Chiari I malformation. , 2004, Radiology.

[5]  D. Maintz,et al.  Comparison of 4D Phase-Contrast MRI Flow Measurements to Computational Fluid Dynamics Simulations of Cerebrospinal Fluid Motion in the Cervical Spine , 2012, PloS one.

[6]  S. Patz,et al.  Physiology-Based MR Imaging Assessment of CSF Flow at the Foramen Magnum with a Valsalva Maneuver , 2013, American Journal of Neuroradiology.

[7]  Michael Markl,et al.  Bicuspid Aortic Valve Is Associated With Altered Wall Shear Stress in the Ascending Aorta , 2012, Circulation. Cardiovascular imaging.

[8]  Francis Loth,et al.  Spinal subarachnoid space pressure measurements in an in vitro spinal stenosis model: implications on syringomyelia theories. , 2010, Journal of biomechanical engineering.

[9]  P. Sharrock,et al.  Stereolithographic models derived from X-ray computed tomography - Reproduction accuracy , 1997, Surgical and Radiologic Anatomy.

[10]  Kent-André Mardal,et al.  Direct numerical simulation of transitional hydrodynamics of the cerebrospinal fluid in Chiari I malformation: The role of cranio‐vertebral junction , 2017, International journal for numerical methods in biomedical engineering.

[11]  W. J. Oakes,et al.  Analysis of the Posterior Fossa in Children with the Chiari 0 Malformation , 2001, Neurosurgery.

[12]  J. Oshinski,et al.  Neural Tissue Motion Impacts Cerebrospinal Fluid Dynamics at the Cervical Medullary Junction: A Patient-Specific Moving-Boundary Computational Model , 2015, Annals of Biomedical Engineering.

[13]  Theresia I. Yiallourou,et al.  Inter-operator Reliability of Magnetic Resonance Image-Based Computational Fluid Dynamics Prediction of Cerebrospinal Fluid Motion in the Cervical Spine , 2015, Annals of Biomedical Engineering.

[14]  Andreas A. Linninger,et al.  Three-dimensional computational prediction of cerebrospinal fluid flow in the human brain , 2011, Comput. Biol. Medicine.

[15]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[16]  Theresia I. Yiallourou,et al.  Continuous positive airway pressure alters cranial blood flow and cerebrospinal fluid dynamics at the craniovertebral junction , 2015 .

[17]  D. Holdsworth,et al.  A three-dimensional cerebrovascular flow phantom. , 1999, Medical physics.

[18]  Walter Heindel,et al.  Magnetic resonance 4D flow analysis of cerebrospinal fluid dynamics in Chiari I malformation with and without syringomyelia , 2012, European Radiology.

[19]  William C. Barrow,et al.  Morphometric analysis of the craniocervical juncture in children with Chiari I malformation and concomitant syringobulbia , 2009, Child's Nervous System.

[20]  B. Martin,et al.  A numerical investigation of intrathecal isobaric drug dispersion within the cervical subarachnoid space , 2017, PloS one.

[21]  G. Crelier,et al.  Magnetic resonance 4D flow characteristics of cerebrospinal fluid at the craniocervical junction and the cervical spinal canal , 2011, European Radiology.

[22]  H. Nauta,et al.  Microsurgical anatomy of spinal subarachnoid space. , 1983, Surgical neurology.

[23]  C Coolens,et al.  Development of a dynamic flow imaging phantom for dynamic contrast-enhanced CT. , 2011, Medical physics.

[25]  T. M. Barker,et al.  Accuracy of stereolithographic models of human anatomy , 1994 .

[26]  David A. Feinberg,et al.  Dynamics of respiratory and cardiac CSF motion revealed with real-time simultaneous multi-slice EPI velocity phase contrast imaging , 2015, NeuroImage.

[27]  Frank R Korosec,et al.  Peak systolic and diastolic CSF velocity in the foramen magnum in adult patients with Chiari I malformations and in normal control participants. , 2003, AJNR. American journal of neuroradiology.

[28]  J. Dyke,et al.  Automated segmentation of MR imaging to determine normative central nervous system cerebrospinal fluid volumes in healthy volunteers. , 2017, Clinical imaging.

[29]  Francis Loth,et al.  The influence of coughing on cerebrospinal fluid pressure in an in vitro syringomyelia model with spinal subarachnoid space stenosis , 2009, Cerebrospinal Fluid Research.

[30]  H. Stockman,et al.  Effect of anatomical fine structure on the flow of cerebrospinal fluid in the spinal subarachnoid space. , 2006, Journal of biomechanical engineering.

[31]  Francis Loth,et al.  Accuracy of 4D Flow Measurement of Cerebrospinal Fluid Dynamics in the Cervical Spine: An In Vitro Verification Against Numerical Simulation , 2016, Annals of Biomedical Engineering.

[32]  B. Williams A demonstration analogue for ventricular and intraspinal dynamics (DAVID). , 1974, Journal of the neurological sciences.

[33]  M. Langer,et al.  4D-MR flow analysis in patients after repair for tetralogy of Fallot , 2011, European Radiology.

[34]  J. Oshinski,et al.  Quantifying the influence of respiration and cardiac pulsations on cerebrospinal fluid dynamics using real‐time phase‐contrast MRI , 2017, Journal of magnetic resonance imaging : JMRI.

[35]  M. Czosnyka,et al.  Physical phantom of craniospinal hydrodynamics. , 2012, Acta neurochirurgica. Supplement.

[36]  Francis Loth,et al.  Characterization of the discrepancies between four-dimensional phase-contrast magnetic resonance imaging and in-silico simulations of cerebrospinal fluid dynamics. , 2015, Journal of biomechanical engineering.

[37]  W. J. Oakes,et al.  The denticulate ligament: anatomy and functional significance. , 2001, Journal of neurosurgery.

[38]  Vartan Kurtcuoglu,et al.  Phantom Model of Physiologic Intracranial Pressure and Cerebrospinal Fluid Dynamics , 2012, IEEE Transactions on Biomedical Engineering.

[39]  D. Sakas,et al.  Chiari malformation: CSF flow dynamics in the craniocervical junction and syrinx , 2005, Acta Neurochirurgica.

[40]  Ikuo Aoki,et al.  Influence of respiration on cerebrospinal fluid movement using magnetic resonance spin labeling , 2013, Fluids and Barriers of the CNS.

[41]  B. Martin,et al.  Cerebrospinal fluid hydrodynamics in type I Chiari malformation , 2011, Neurological research.

[42]  Mehrdad Raisee,et al.  The Impact of Spinal Cord Nerve Roots and Denticulate Ligaments on Cerebrospinal Fluid Dynamics in the Cervical Spine , 2014, PloS one.

[43]  Andreas A. Linninger,et al.  CNS wide simulation of flow resistance and drug transport due to spinal microanatomy. , 2015, Journal of biomechanics.

[44]  Jeroen J. Bax,et al.  Validation of a high-resolution, phase contrast cardiovascular magnetic resonance sequence for evaluation of flow in coronary artery bypass grafts. , 2007, Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance.

[45]  Jens Frahm,et al.  Inspiration Is the Major Regulator of Human CSF Flow , 2015, The Journal of Neuroscience.

[46]  Francis Loth,et al.  Syringomyelia hydrodynamics: an in vitro study based on in vivo measurements. , 2005, Journal of biomechanical engineering.

[47]  M. McGirt,et al.  Correlation of hindbrain CSF flow and outcome after surgical decompression for Chiari I malformation , 2008, Child's Nervous System.