Cardiac-related spinal cord tissue motion at the foramen magnum is elevated in Type I Chiari malformation patients and decreases post-decompression surgery

Objective— Type 1 Chiari malformation (CM-I) is a craniospinal disorder historically defined by cerebellar tonsillar position (TP) greater than 3-5mm below the foramen magnum (FM). This definition has come under question since quantitative measurements of cerebellar herniation do not always correspond with symptom severity. Researchers have proposed several additional radiographic diagnostic criteria based on dynamic motion of fluids and/or tissues. The present study objective was to determine if cardiac-related craniocaudal spinal cord tissue displacement is an accurate indicator of the presence of CM-I and if tissue displacement is altered with decompression. Methods— A cohort of 20 symptomatic patients underwent decompression surgery. Fifteen healthy volunteers were recruited for comparison to the CM-I group. Axial phase-contrast magnetic resonance imaging (PC-MRI) measurements were collected pre- and post-surgery at the FM with cranial-caudal velocity encoding and 20 frames per cardiac cycle with retrospective reconstruction. Spinal cord motion (SCM) at the FM was quantified based on the peak-to-peak integral of average spinal cord velocity. Results— Tissue motion for the pre-surgical group was significantly greater than controls (p=0.0009). Motion decreased following surgery (p=0.058) with an effect size of -0.151 mm and a standard error of 0.066 mm. Post-operatively, no statistical difference from controls in bulk displacement at the FM was found (p=0.200) after post hoc testing using Tukey's adjustment for multiple comparisons. Conclusions— These results support SCM measurement by PC-MRI as a possible non-invasive radiographic diagnostic for CM-I. Dynamic measurement of SCM provides unique diagnostic information about CM-I alongside static quantification of TP and other intracranial morphometrics.

[1]  H. Ozdemir,et al.  Diffusion tensor imaging findings of the brainstem in subjects with tonsillar ectopia , 2018, Acta Neurologica Belgica.

[2]  D. Choi,et al.  Chiari Malformation Type 1: A Systematic Review of Natural History and Conservative Management. , 2017, World neurosurgery.

[3]  El-Sayed H. Ibrahim,et al.  Principles, Techniques, and Clinical Applications of Phase-Contrast Magnetic Resonance Cerebrospinal Fluid Imaging , 2017 .

[4]  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.

[5]  E. Oldfield,et al.  Two distinct populations of Chiari I malformation based on presence or absence of posterior fossa crowdedness on magnetic resonance imaging. , 2016, Journal of neurosurgery.

[6]  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 , 2016, Annals of Biomedical Engineering.

[7]  Francesco Sammartino,et al.  Diffusion tensor imaging assessment of microstructural brainstem integrity in Chiari malformation Type I. , 2016, Journal of neurosurgery.

[8]  J. Heiss,et al.  Pathogenesis and Cerebrospinal Fluid Hydrodynamics of the Chiari I Malformation. , 2015, Neurosurgery clinics of North America.

[9]  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.

[10]  Samuel S. Bruce,et al.  Outcomes after suboccipital decompression without dural opening in children with Chiari malformation Type I. , 2015, Journal of neurosurgery. Pediatrics.

[11]  Ryan A. Grant,et al.  Multimodal evaluation of CSF dynamics following extradural decompression for Chiari malformation Type I. , 2015, Journal of neurosurgery. Spine.

[12]  E. Kuhl,et al.  Mechanics of the brain: perspectives, challenges, and opportunities , 2015, Biomechanics and Modeling in Mechanobiology.

[13]  Jacob K. Greenberg,et al.  Tonsillar pulsatility before and after surgical decompression for children with Chiari malformation type 1: an application for true fast imaging with steady state precession , 2015, Neuroradiology.

[14]  Søren Højsgaard,et al.  A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models: The R Package pbkrtest , 2014 .

[15]  T. Huisman,et al.  Diffusion tensor imaging in pediatric Chiari type I malformation , 2014, Developmental medicine and child neurology.

[16]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[17]  J. Oshinski,et al.  Cerebrospinal fluid flow impedance is elevated in Type I Chiari malformation. , 2014, Journal of biomechanical engineering.

[18]  Francis Loth,et al.  Hydrodynamic and Longitudinal Impedance Analysis of Cerebrospinal Fluid Dynamics at the Craniovertebral Junction in Type I Chiari Malformation , 2013, PloS one.

[19]  K. Muraszko,et al.  Distribution of cerebellar tonsil position: implications for understanding Chiari malformation. , 2013, Journal of neurosurgery.

[20]  Lance Lee Riding the wave of ependymal cilia: Genetic susceptibility to hydrocephalus in primary ciliary dyskinesia , 2013, Journal of neuroscience research.

[21]  Jochen Guck,et al.  Mechanics in neuronal development and repair. , 2013, Annual review of biomedical engineering.

[22]  N. Selden,et al.  Dura splitting decompression for Chiari I malformation in pediatric patients: clinical outcomes, healthcare costs, and resource utilization. , 2013, Neurosurgery.

[23]  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.

[24]  J. Klekamp Surgical treatment of Chiari I malformation--analysis of intraoperative findings, complications, and outcome for 371 foramen magnum decompressions. , 2012, Neurosurgery.

[25]  R. Yassari,et al.  A novel scoring system for assessing Chiari malformation type I treatment outcomes. , 2012, Neurosurgery.

[26]  K. Muraszko,et al.  Chiari malformation Type I and syrinx in children undergoing magnetic resonance imaging. , 2011, Journal of neurosurgery. Pediatrics.

[27]  K. Muraszko,et al.  Natural history of Chiari malformation Type I following decision for conservative treatment. , 2011, Journal of neurosurgery. Pediatrics.

[28]  M. Kumar,et al.  Correlation of diffusion tensor imaging metrics with neurocognitive function in Chiari I malformation. , 2011, World neurosurgery.

[29]  N. Bulakbaşı,et al.  Cerebrospinal fluid flow imaging by using phase-contrast MR technique. , 2011, The British journal of radiology.

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

[31]  K. Slavin,et al.  National Institutes of Health Chiari Research Conference: state of the research and new directions , 2011, Neurological research.

[32]  W. J. Oakes,et al.  Institutional experience with 500 cases of surgically treated pediatric Chiari malformation Type I. , 2011, Journal of neurosurgery. Pediatrics.

[33]  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.

[34]  K. Houkin,et al.  Pathogenesis of syringomyelia associated with Chiari type 1 malformation: review of evidences and proposal of a new hypothesis , 2010, Neurosurgical Review.

[35]  T. Moriarty,et al.  Decompression of Chiari malformation with and without duraplasty: morbidity versus recurrence. , 2010, Journal of neurosurgery. Pediatrics.

[36]  V. Haughton,et al.  Motion of the Cerebellar Tonsils in the Foramen Magnum during the Cardiac Cycle , 2009, American Journal of Neuroradiology.

[37]  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.

[38]  Benedetta Pettorini,et al.  The natural history of the Chiari Type I anomaly. , 2008, Journal of neurosurgery. Pediatrics.

[39]  M. McGirt,et al.  Symptom recurrence after suboccipital decompression for pediatric Chiari I malformation: analysis of 256 consecutive cases , 2008, Child's Nervous System.

[40]  X. Wu,et al.  Chiari I malformation associated with syringomyelia: a retrospective study of 316 surgically treated patients , 2008, Spinal Cord.

[41]  N. Wetjen,et al.  Time course of syringomyelia resolution following decompression of Chiari malformation Type I. , 2008, Journal of neurosurgery. Pediatrics.

[42]  Michael J. Lyerly,et al.  The pediatric Chiari I malformation: a review , 2007, Child's Nervous System.

[43]  D. Greitz Unraveling the riddle of syringomyelia , 2006, Neurosurgical Review.

[44]  P. Jannetta,et al.  Dimensions of the posterior fossa in patients symptomatic for Chiari I malformation but without cerebellar tonsillar descent , 2005, Cerebrospinal Fluid Research.

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

[46]  Andrew P. McMahon,et al.  Neural crest origins of the neck and shoulder , 2005, Nature.

[47]  Anusha Sivaramakrishnan,et al.  Magnetic resonance imaging-based measurements of cerebrospinal fluid and blood flow as indicators of intracranial compliance in patients with Chiari malformation. , 2005, Journal of neurosurgery.

[48]  M. B. Royo-Salvador,et al.  Results of the section of the filum terminale in 20 patients with syringomyelia, scoliosis and Chiari malformation , 2005, Acta Neurochirurgica.

[49]  D. Mueller,et al.  Prospective analysis of self-perceived quality of life before and after posterior fossa decompression in 112 patients with Chiari malformation with or without syringomyelia. , 2005, Neurosurgical focus.

[50]  R. Tubbs,et al.  A critical analysis of the Chiari 1.5 malformation. , 2004, Journal of neurosurgery.

[51]  Tadanori Tomita,et al.  Surgical results of posterior fossa decompression for patients with Chiari I malformation , 2004, Child's Nervous System.

[52]  P. Steinbok,et al.  International survey on the management of Chiari I malformation and syringomyelia , 2004, Child's Nervous System.

[53]  Richard G. Ellenbogen,et al.  Review Article: Chiari Type I Malformation with or Without Syringomyelia: Prevalence and Genetics , 2003, Journal of Genetic Counseling.

[54]  W. J. Oakes,et al.  Surgical experience in 130 pediatric patients with Chiari I malformations. , 2003, Journal of neurosurgery.

[55]  Charles A Sansur,et al.  Pathophysiology of headache associated with cough in patients with Chiari I malformation. , 2003, Journal of neurosurgery.

[56]  E. Ventureyra,et al.  The role of cine flow MRI in children with Chiari I malformation , 2003, Child's Nervous System.

[57]  J. Klekamp,et al.  The Pathophysiology of Syringomyelia – Historical Overview and Current Concept , 2002, Acta Neurochirurgica.

[58]  M. Kraut,et al.  Asymptomatic Chiari Type I malformations identified on magnetic resonance imaging. , 2000, Journal of neurosurgery.

[59]  H. Winn,et al.  Toward a rational treatment of Chiari I malformation and syringomyelia. , 2000, Neurosurgical focus.

[60]  M C Speer,et al.  Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. , 1999, Neurosurgery.

[61]  A Capdevila,et al.  Motion of the cerebellar tonsils in Chiari type I malformation studied by cine phase-contrast MRI , 1995, Neurology.

[62]  A. Elster,et al.  Chiari I malformations: clinical and radiologic reappraisal. , 1992, Radiology.

[63]  J. Hahn,et al.  Symptomatic Chiari malformation in adults: a new classification based on magnetic resonance imaging with clinical and prognostic significance. , 1991, Neurosurgery.

[64]  A. Barkovich,et al.  Significance of cerebellar tonsillar position on MR. , 1986, AJNR. American journal of neuroradiology.

[65]  K. Sartor,et al.  Position of Cerebellar Tonsils in the Normal Population and in Patients with Chiari Malformation: A Quantitative Approach with MR Imaging , 1985, Journal of computer assisted tomography.

[66]  B Williams,et al.  Simultaneous cerebral and spinal fluid pressure recordings , 1981, Acta Neurochirurgica.

[67]  G. du Boulay,et al.  The mechanism of hydromyelia in Chiari type 1 malformations. , 1974, The British journal of radiology.

[68]  I. Kricheff,et al.  Cerebrospinal fluid pulsations at myelography: a videodensitometric study. , 1974, Radiology.

[69]  B. Williams Further Thoughts on the Valvular Action of the Arnold‐Chiari Malformation , 1971 .

[70]  B. Williams The distending force in the production of communicating syringomyelia. , 1969, Lancet.

[71]  D. L. Mcrae Bony abnormalities in the region of the foramen magnum: correlation of the anatomic and neurologic findings. , 1953, Acta radiologica.

[72]  Lynne E Bilston,et al.  Cerebellar and hindbrain motion in Chiari malformation with and without syringomyelia. , 2016, Journal of neurosurgery. Spine.

[73]  K. Akkan,et al.  Assessment of 3D T2-weighted high-sampling-efficiency technique (SPACE) for detection of cerebellar tonsillar motion: new useful sign for Chiari I malformation. , 2015, Clinical imaging.

[74]  M. Samii,et al.  The surgical treatment of Chiari I malformation , 2005, Acta Neurochirurgica.

[75]  B. Williams Simultaneous cerebral and spinal fluid pressure recordings , 2005, Acta Neurochirurgica.

[76]  H. Abe,et al.  Increased pulsatile movement of the hindbrain in syringomyelia associated with the Chiari malformation: cine-MRI with presaturation bolus tracking , 2004, Neuroradiology.

[77]  L Solymosi,et al.  Phase-contrast MR imaging of the cervical CSF and spinal cord: volumetric motion analysis in patients with Chiari I malformation. , 2000, AJNR. American journal of neuroradiology.

[78]  T H Shawker,et al.  Pathophysiology of syringomyelia associated with Chiari I malformation of the cerebellar tonsils. Implications for diagnosis and treatment. , 1994, Journal of neurosurgery.

[79]  J. L. Harrison,et al.  The Government Printing Office , 1968, American Journal of Pharmaceutical Education.

[80]  W. Gardner,et al.  The mechanism of syringomyelia and its surgical correction. , 1958, Clinical neurosurgery.