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

European Radiology volume 21, pages 1788–1796 (2011)Cite this article

Abstract

Objectives

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.

Methods

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.

Results

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.

Conclusions

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.

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References

  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 104:810–819

    PubMed  Article  Google Scholar 

  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 24:169–176

    PubMed  Google Scholar 

  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 101:169–178

    PubMed  Google Scholar 

  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 63:1139–1144

    PubMed  Article  Google Scholar 

  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 245:532–540

    PubMed  Article  Google Scholar 

  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 232:229–236

    PubMed  Article  Google Scholar 

  7. Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–264

    PubMed  Article  Google Scholar 

  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 24:833–840

    PubMed  Article  Google Scholar 

  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 21:151–158

    PubMed  CAS  Google Scholar 

  10. Ball JR, Little NS (2008) Chiari malformation, cervical disc prolapse and syringomyelia–always think twice. J Clin Neurosci 15:474–476

    PubMed  Article  Google Scholar 

  11. Milhorat TH, Chou MW, Trinidad EM et al (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44:1005–1017

    PubMed  Article  CAS  Google Scholar 

  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 25:689–692

    PubMed  Article  Google Scholar 

  13. Cousins J, Haughton V (2009) Motion of the cerebellar tonsils in the foramen magnum during the cardiac cycle. AJNR Am J Neuroradiol 30:1587–1588

    PubMed  Article  CAS  Google Scholar 

  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 103:46–52

    PubMed  Article  Google Scholar 

  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 30:941–946

    PubMed  Article  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  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 9:741–747

    PubMed  Article  Google Scholar 

  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 31:9–15

    PubMed  Article  Google Scholar 

  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 30:362–366

    PubMed  Article  CAS  Google Scholar 

  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 61:409–417

    PubMed  Article  Google Scholar 

  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 51:42–52

    PubMed  Article  Google Scholar 

  22. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  23. Bland JM, Altman DG (2007) Agreement between methods of measurement with multiple observations per individual. J Biopharm Stat 17:571–582

    PubMed  Article  Google Scholar 

  24. Bland JM, Altman DG (1995) Calculating correlation coefficients with repeated observations: part 1–correlation within subjects. BMJ 310:446

    PubMed  CAS  Google Scholar 

  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 246:249–257

    PubMed  Article  Google Scholar 

  26. Krueger KD, Haughton VM, Hetzel S (2010) Peak CSF velocities in patients with symptomatic and asymptomatic Chiari I malformation. AJNR Am J Neuroradiol 31:1837–1841

    PubMed  Article  CAS  Google Scholar 

  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 62:966–974

    PubMed  Article  Google Scholar 

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Author information

Affiliations

  1. Department of Clinical Radiology, University Hospital of Muenster, Muenster, Germany

    Alexander C. Bunck, Jan-Robert Kröger, Alena Jüttner, Wolfram Schwindt, Walter Heindel, Thomas Niederstadt & David Maintz

  2. Department of Neurosurgery, University Hospital of Muenster, Muenster, Germany

    Angela Brentrup

  3. Department of General Pediatrics, Subdivision Pediatric Neurology, University Hospital of Muenster, Muenster, Germany

    Barbara Fiedler

  4. Institute of Biostatistics, Leibniz University Hannover, Hannover, Germany

    Frank Schaarschmidt

  5. Institute for Biomedical Engineering, ETH and University of Zurich, Zurich, Switzerland

    Gerard R. Crelier

  6. Department of Clinical Radiology, University Hospital Muenster, Albert-Schweitzer-Strasse 33, 48149, Muenster, Germany

    Alexander C. Bunck

Authors
  1. Alexander C. Bunck
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  2. Jan-Robert Kröger
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  3. Alena Jüttner
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  4. Angela Brentrup
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  5. Barbara Fiedler
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  7. Gerard R. Crelier
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  9. Walter Heindel
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  10. Thomas Niederstadt
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  11. David Maintz
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Corresponding author

Correspondence to Alexander C. Bunck.

Electronic supplementary material

Below is the link to the electronic supplementary material.

330_2011_2105_MOESM1_ESM.mpg

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

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)

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

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

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)

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)

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 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)

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Bunck, A.C., Kröger, JR., Jüttner, A. et al. Magnetic resonance 4D flow characteristics of cerebrospinal fluid at the craniocervical junction and the cervical spinal canal. Eur Radiol 21, 1788–1796 (2011). https://doi.org/10.1007/s00330-011-2105-7

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  • DOI: https://doi.org/10.1007/s00330-011-2105-7

Keywords

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