European Radiology

, Volume 21, Issue 8, pp 1788–1796 | Cite as

Magnetic resonance 4D flow characteristics of cerebrospinal fluid at the craniocervical junction and the cervical spinal canal

  • Alexander C. BunckEmail author
  • Jan-Robert Kröger
  • Alena Jüttner
  • Angela Brentrup
  • Barbara Fiedler
  • Frank Schaarschmidt
  • Gerard R. Crelier
  • Wolfram Schwindt
  • Walter Heindel
  • Thomas Niederstadt
  • David Maintz



To evaluate the applicability of 4D phase contrast (4D PC) MR imaging in the assessment of cerebrospinal fluid dynamics in healthy volunteers and patients with lesions at the craniocervical junction or the cervical spinal canal.


Ten healthy volunteers and four patients with lesions including Chiari I malformation and cervical canal stenoses were examined by a cardiac-gated 4D PC imaging sequence on 1.5T MRI. Phase contrast images were postprocessed allowing for flow quantification and flow pathline visualisation. Velocity data were compared with conventional axial 2D phase contrast images.


The 4D PC sequence allowed for flow quantification and visualisation in all individuals. Bland-Altman analysis showed good agreement of 2D and 4D PC velocity data. In healthy volunteers, CSF flow was homogeneously distributed in the anterior and anterolateral subarachnoid space with the flow directed caudally during systole and cranially during diastole. Flow velocities were closely related to the width of the subarachnoid space. Patients showed grossly altered CSF flow patterns with formation of flow jets with increased flow velocities.


4D PC MR imaging allows for a detailed assessment of CSF flow dynamics helping to distinguish physiological from complex pathological flow patterns at the craniocervical junction and the cervical spine.


Cerebrospinal fluid Flow-sensitive 4D MRI Chiari malformation Cervical canal stenosis Syringomyelia 

Supplementary material

330_2011_2105_MOESM1_ESM.mpg (9.8 mb)
Movie 1 In healthy volunteers the main CSF flow component was evenly distributed across the anterior and anterolateral subarachnoid space extending from the craniocervical junction throughout the entire cervical spinal canal. (MPG 10050 kb)
330_2011_2105_MOESM2_ESM.mpg (8.2 mb)
Movie 2 Patient 1 with pronounced Chiari I malformation and presyrinx at the level of C2 showing two flow vortices located bilaterally in the anterolateral subarachnoid space extending from the foramen magnum to the level of C2/C3. (MPG 8426 kb)
Movie 3

SSFP Cine imaging showing increased motion of cerebellar tonsils and brain stem in patient 1. (AVI 636 kb)

Movie 4

On SSFP cine images in patient 2 only a little excursion of the cerebellar tonsils was observed (1 mm), anterior subarachnoid space at the level of C1 narrowed by 0.3 mm. (AVI 496 kb)

330_2011_2105_MOESM5_ESM.mpg (6.1 mb)
Movie 5 4D flow imaging showing severe flow acceleration in patient 2 with two flow jets located bilaterally in the anterolateral subarachnoid space extending from the foramen magnum to the level of C2/C3 with accentuation on the right side (MPG 6200 kb)


  1. 1.
    Wagshul ME, Chen JJ, Egnor MR, McCormack EJ, Roche PE (2006) Amplitude and phase of cerebrospinal fluid pulsations: experimental studies and review of the literature. J Neurosurg 104:810–819PubMedCrossRefGoogle Scholar
  2. 2.
    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 24:169–176PubMedGoogle Scholar
  3. 3.
    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 101:169–178PubMedGoogle Scholar
  4. 4.
    Mauer UM, Freude G, Danz B, Kunz U (2008) Cardiac-gated phase-contrast magnetic resonance imaging of cerebrospinal fluid flow in the diagnosis of idiopathic syringomyelia. Neurosurgery 63:1139–1144PubMedCrossRefGoogle Scholar
  5. 5.
    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 245:532–540PubMedCrossRefGoogle Scholar
  6. 6.
    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 232:229–236PubMedCrossRefGoogle Scholar
  7. 7.
    Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–264PubMedCrossRefGoogle Scholar
  8. 8.
    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 24:833–840PubMedCrossRefGoogle Scholar
  9. 9.
    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 21:151–158PubMedGoogle Scholar
  10. 10.
    Ball JR, Little NS (2008) Chiari malformation, cervical disc prolapse and syringomyelia–always think twice. J Clin Neurosci 15:474–476PubMedCrossRefGoogle Scholar
  11. 11.
    Milhorat TH, Chou MW, Trinidad EM et al (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44:1005–1017PubMedCrossRefGoogle Scholar
  12. 12.
    Tubbs RS, Bailey M, Barrow WC, Loukas M, Shoja MM, Oakes WJ (2009) Morphometric analysis of the craniocervical juncture in children with Chiari I malformation and concomitant syringobulbia. Childs Nerv Syst 25:689–692PubMedCrossRefGoogle Scholar
  13. 13.
    Cousins J, Haughton V (2009) Motion of the cerebellar tonsils in the foramen magnum during the cardiac cycle. AJNR Am J Neuroradiol 30:1587–1588PubMedCrossRefGoogle Scholar
  14. 14.
    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 103:46–52PubMedCrossRefGoogle Scholar
  15. 15.
    Roldan A, Wieben O, Haughton V, Osswald T, Chesler N (2009) Characterization of CSF hydrodynamics in the presence and absence of tonsillar ectopia by means of computational flow analysis. AJNR Am J Neuroradiol 30:941–946PubMedCrossRefGoogle Scholar
  16. 16.
    Sweetman B, Linninger AA (2010) Cerebrospinal fluid flow dynamics in the central nervous system. Ann Biomed Eng. doi: 10.1007/s10439-010-0141-0 PubMedGoogle Scholar
  17. 17.
    Bolger AF, Heiberg E, Karlsson M et al (2007) Transit of blood flow through the human left ventricle mapped by cardiovascular magnetic resonance. J Cardiovasc Magn Reson 9:741–747PubMedCrossRefGoogle Scholar
  18. 18.
    Frydrychowicz A, Harloff A, Jung B et al (2007) Time-resolved, 3-dimensional magnetic resonance flow analysis at 3 T: visualization of normal and pathological aortic vascular hemodynamics. J Comput Assist Tomogr 31:9–15PubMedCrossRefGoogle Scholar
  19. 19.
    Hope MD, Purcell DD, Hope TA et al (2009) Complete intracranial arterial and venous blood flow evaluation with 4D flow MR imaging. AJNR Am J Neuroradiol 30:362–366PubMedCrossRefGoogle Scholar
  20. 20.
    Boussel L, Rayz V, Martin A et al (2009) Phase-contrast magnetic resonance imaging measurements in intracranial aneurysms in vivo of flow patterns, velocity fields, and wall shear stress: comparison with computational fluid dynamics. Magn Reson Med 61:409–417PubMedCrossRefGoogle Scholar
  21. 21.
    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 51:42–52PubMedCrossRefGoogle Scholar
  22. 22.
    Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New YorkCrossRefGoogle Scholar
  23. 23.
    Bland JM, Altman DG (2007) Agreement between methods of measurement with multiple observations per individual. J Biopharm Stat 17:571–582PubMedCrossRefGoogle Scholar
  24. 24.
    Bland JM, Altman DG (1995) Calculating correlation coefficients with repeated observations: part 1–correlation within subjects. BMJ 310:446PubMedGoogle Scholar
  25. 25.
    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 246:249–257PubMedCrossRefGoogle Scholar
  26. 26.
    Krueger KD, Haughton VM, Hetzel S (2010) Peak CSF velocities in patients with symptomatic and asymptomatic Chiari I malformation. AJNR Am J Neuroradiol 31:1837–1841PubMedCrossRefGoogle Scholar
  27. 27.
    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 62:966–974PubMedCrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2011

Authors and Affiliations

  • Alexander C. Bunck
    • 1
    • 6
    Email author
  • Jan-Robert Kröger
    • 1
  • Alena Jüttner
    • 1
  • Angela Brentrup
    • 2
  • Barbara Fiedler
    • 3
  • Frank Schaarschmidt
    • 4
  • Gerard R. Crelier
    • 5
  • Wolfram Schwindt
    • 1
  • Walter Heindel
    • 1
  • Thomas Niederstadt
    • 1
  • David Maintz
    • 1
  1. 1.Department of Clinical RadiologyUniversity Hospital of MuensterMuensterGermany
  2. 2.Department of NeurosurgeryUniversity Hospital of MuensterMuensterGermany
  3. 3.Department of General Pediatrics, Subdivision Pediatric NeurologyUniversity Hospital of MuensterMuensterGermany
  4. 4.Institute of BiostatisticsLeibniz University HannoverHannoverGermany
  5. 5.Institute for Biomedical EngineeringETH and University of ZurichZurichSwitzerland
  6. 6.Department of Clinical RadiologyUniversity Hospital MuensterMuensterGermany

Personalised recommendations