Abstract
Objective
To analyse cerebrospinal fluid (CSF) hydrodynamics in patients with Chiari type I malformation (CM) with and without syringomyelia using 4D magnetic resonance (MR) phase contrast (PC) flow imaging.
Methods
4D-PC CSF flow data were acquired in 20 patients with CM (12 patients with presyrinx/syrinx). Characteristic 4D-CSF flow patterns were identified. Quantitative CSF flow parameters were assessed at the craniocervical junction and the cervical spinal canal and compared with healthy volunteers and between patients with and without syringomyelia.
Results
Compared with healthy volunteers, 17 CM patients showed flow abnormalities at the craniocervical junction in the form of heterogeneous flow (n = 3), anterolateral flow jets (n = 14) and flow vortex formation (n = 5), most prevalent in patients with syringomyelia. Peak flow velocities at the craniocervical junction were significantly increased in patients (−15.5 ± 11.3 vs. −4.7 ± 0.7 cm/s in healthy volunteers, P < 0.001). At the level of C1, maximum systolic flow was found to be significantly later in the cardiac cycle in patients (30.8 ± 10.3 vs. 22.7 ± 4.1%, P < 0.05).
Conclusions
4D-PC flow imaging allowed comprehensive analysis of CSF flow in patients with Chiari I malformation. Alterations of CSF hydrodynamics were most pronounced in patients with syringomyelia.
Key Points
• Analysis of CSF flow is important in patients with Chiari I malformation
• 4D-PC MRI allows analysis of CSF in patients with Chiari I.
• Chiari I patients show characteristic qualitative and quantitative alterations of CSF flow.
• Alterations of CSF hydrodynamics are most pronounced in patients with associated syringomyelia.
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References
Milhorat TH, Chou MW, Trinidad EM et al (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44:1005–1017
Shaffer N, Martin B, Loth F (2011) Cerebrospinal fluid hydrodynamics in type I Chiari malformation. Neurol Res 33:247–260
Haughton VM, Korosec FR, Medow JE, Dolar MT, Iskandar BJ (2003) Peak systolic and diastolic CSF velocity in the foramen magnum in adult patients with Chiari I malformations and in normal control participants. AJNR Am J Neuroradiol 24:169–176
Alperin N, Sivaramakrishnan A, Lichtor T (2005) Magnetic resonance imaging-based measurements of cerebrospinal fluid and blood flow as indicators of intracranial compliance in patients with Chiari malformation. J Neurosurg 103:46–52
Levine DN (2004) The pathogenesis of syringomyelia associated with lesions at the foramen magnum: a critical review of existing theories and proposal of a new hypothesis. J Neurol Sci 220:3–21
Bilston LE, Stoodley MA, Fletcher DF (2010) The influence of the relative timing of arterial and subarachnoid space pulse waves on spinal perivascular cerebrospinal fluid flow as a possible factor in syrinx development. J Neurosurg 112:808–813
Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–264
Koyanagi I, Houkin K (2010) Pathogenesis of syringomyelia associated with Chiari type 1 malformation: review of evidences and proposal of a new hypothesis. Neurosurg Rev 33:271–284
Strahle J, Muraszko KM, Kapurch J, Bapuraj JR, Garton HJ, Maher CO (2011) Chiari malformation type I and syrinx in children undergoing magnetic resonance imaging. J Neurosurg Pediatr 8:205–213
Iskandar BJ, Quigley M, Haughton VM (2004) Foramen magnum cerebrospinal fluid flow characteristics in children with Chiari I malformation before and after craniocervical decompression. J Neurosurg 101:169–178
Hofkes SK, Iskandar BJ, Turski PA, Gentry LR, McCue JB, Haughton VM (2007) Differentiation between symptomatic Chiari I malformation and asymptomatic tonsilar ectopia by using cerebrospinal fluid flow imaging: initial estimate of imaging accuracy. Radiology 245:532–540
Markl M, Geiger J, Kilner PJ et al (2011) Time-resolved three-dimensional magnetic resonance velocity mapping of cardiovascular flow paths in volunteers and patients with Fontan circulation. Eur J Cardiothorac Surg 39:206–212
Stadlbauer A, Salomonowitz E, van der Riet W, Buchfelder M, Ganslandt O (2010) Insight into the patterns of cerebrospinal fluid flow in the human ventricular system using MR velocity mapping. NeuroImage 51:42–52
Stadlbauer A, Salomonowitz E, Brenneis C et al (2012) Magnetic resonance velocity mapping of 3D cerebrospinal fluid flow dynamics in hydrocephalus: preliminary results. Eur Radiol 22:232–242
Santini F, Wetzel SG, Bock J, Markl M, Scheffler K (2009) Time-resolved three-dimensional (3D) phase-contrast (PC) balanced steady-state free precession (bSSFP). Magn Reson Med 62:966–974
Bunck AC, Kroger JR, Juttner A et al (2011) Magnetic resonance 4D flow characteristics of cerebrospinal fluid at the craniocervical junction and the cervical spinal canal. Eur Radiol 21:1788–1796
Bhadelia RA, Frederick E, Patz S et al (2011) Cough-associated headache in patients with Chiari I malformation: CSF flow analysis by means of cine phase-contrast MR imaging. AJNR Am J Neuroradiol 32:739–742
Krueger KD, Haughton VM, Hetzel S (2010) Peak CSF velocities in patients with symptomatic and asymptomatic Chiari I malformation. AJNR Am J Neuroradiol 31:1837–1841
McGirt MJ, Nimjee SM, Floyd J, Bulsara KR, George TM (2005) Correlation of cerebrospinal fluid flow dynamics and headache in Chiari I malformation. Neurosurgery 56:716–721
Quigley MF, Iskandar B, Quigley ME, Nicosia M, Haughton V (2004) 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
McGirt MJ, Nimjee SM, Fuchs HE, George TM (2006) Relationship of cine phase-contrast magnetic resonance imaging with outcome after decompression for Chiari I malformations. Neurosurgery 59:140–146
McGirt MJ, Atiba A, Attenello FJ et al (2008) Correlation of hindbrain CSF flow and outcome after surgical decompression for Chiari I malformation. Childs Nerv Syst 24:833–840
Mauer UM, Gottschalk A, Mueller C, Weselek L, Kunz U, Schulz C (2011) Standard and cardiac-gated phase-contrast magnetic resonance imaging in the clinical course of patients with Chiari malformation type I. Neurosurg Focus 31:E5
Hofmann E, Warmuth-Metz M, Bendszus M, Solymosi L (2000) 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
Pinna G, Alessandrini F, Alfieri A, Rossi M, Bricolo A (2000) Cerebrospinal fluid flow dynamics study in Chiari I malformation: implications for syrinx formation. Neurosurg Focus 8:E3
Goh S, Bottrell CL, Aiken AH, Dillon WP, Wu YW (2008) Presyrinx in children with Chiari malformations. Neurology 71:351–356
Armonda RA, Citrin CM, Foley KT, Ellenbogen RG (1994) Quantitative cine-mode magnetic resonance imaging of Chiari I malformations: an analysis of cerebrospinal fluid dynamics. Neurosurgery 35:214–223
Baltes C, Hansen MS, Tsao J et al (2008) Determination of peak velocity in stenotic areas: echocardiography versus k-t SENSE accelerated MR Fourier velocity encoding. Radiology 246:249–257
Struck AF, Haughton VM (2009) Idiopathic syringomyelia: phase-contrast MR of cerebrospinal fluid flow dynamics at level of foramen magnum. Radiology 253:184–190
Martin BA, Reymond P, Novy J, Baledent O, Stergiopulos N (2012) A coupled hydrodynamic model of the cardiovascular and cerebrospinal fluid system. Am J Physiol Heart Circ Physiol. doi:10.1152/ajpheart.00658.2011
Kalata W, Martin BA, Oshinski JN, Jerosch-Herold M, Royston TJ, Loth F (2009) MR measurement of cerebrospinal fluid velocity wave speed in the spinal canal. IEEE Trans Biomed Eng 56:1765–1768
Heiss JD, Patronas N, DeVroom HL et al (1999) Elucidating the pathophysiology of syringomyelia. J Neurosurg 91:553–562
Frydrychowicz A, Francois CJ, Turski PA (2011) Four-dimensional phase contrast magnetic resonance angiography: potential clinical applications. Eur J Radiol 80:24–35
Baledent O, Henry-Feugeas MC, Idy-Peretti I (2001) Cerebrospinal fluid dynamics and relation with blood flow: a magnetic resonance study with semiautomated cerebrospinal fluid segmentation. Invest Radiol 36:368–377
Johnson KM, Markl M (2010) Improved SNR in phase contrast velocimetry with five-point balanced flow encoding. Magn Reson Med 63:349–355
Acknowledgements
B. Martin currently receives funding from the Swiss National Science Foundation. G. Crelier is an employee of Gyrotools Ltd., Zürich, Switzerland.
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W. Schwindt and T. Niederstadt contributed equally as senior authors.
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Bunck, A.C., Kroeger, J.R., Juettner, A. et al. Magnetic resonance 4D flow analysis of cerebrospinal fluid dynamics in Chiari I malformation with and without syringomyelia. Eur Radiol 22, 1860–1870 (2012). https://doi.org/10.1007/s00330-012-2457-7
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DOI: https://doi.org/10.1007/s00330-012-2457-7