Advertisement

European Radiology

, Volume 22, Issue 9, pp 1860–1870 | Cite as

Magnetic resonance 4D flow analysis of cerebrospinal fluid dynamics in Chiari I malformation with and without syringomyelia

  • Alexander C. BunckEmail author
  • Jan Robert Kroeger
  • Alena Juettner
  • Angela Brentrup
  • Barbara Fiedler
  • Gerard R. Crelier
  • Bryn A. Martin
  • Walter Heindel
  • David Maintz
  • Wolfram Schwindt
  • Thomas Niederstadt
Neuro

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.

Keywords

Chiari malformation Syringomyelia Cerebrospinal fluid 4D flow imaging MRI 

Notes

Acknowledgements

B. Martin currently receives funding from the Swiss National Science Foundation. G. Crelier is an employee of Gyrotools Ltd., Zürich, Switzerland.

Supplementary material

Supplemental Digital Content 1

(WMV 3753 kb)

Supplemental Digital Content 2

(WMV 2010 kb)

Supplemental Digital Content 3

(WMV 2932 kb)

Supplemental Digital Content 4

(WMV 2753 kb)

References

  1. 1.
    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
  2. 2.
    Shaffer N, Martin B, Loth F (2011) Cerebrospinal fluid hydrodynamics in type I Chiari malformation. Neurol Res 33:247–260PubMedGoogle Scholar
  3. 3.
    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
  4. 4.
    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
  5. 5.
    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 220:3–21PubMedCrossRefGoogle Scholar
  6. 6.
    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 112:808–813PubMedCrossRefGoogle Scholar
  7. 7.
    Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–264PubMedCrossRefGoogle Scholar
  8. 8.
    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 33:271–284PubMedCrossRefGoogle Scholar
  9. 9.
    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 8:205–213PubMedCrossRefGoogle Scholar
  10. 10.
    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
  11. 11.
    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
  12. 12.
    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 39:206–212PubMedCrossRefGoogle Scholar
  13. 13.
    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
  14. 14.
    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 22:232–242PubMedCrossRefGoogle Scholar
  15. 15.
    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
  16. 16.
    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 21:1788–1796PubMedCrossRefGoogle Scholar
  17. 17.
    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 32:739–742PubMedCrossRefGoogle Scholar
  18. 18.
    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
  19. 19.
    McGirt MJ, Nimjee SM, Floyd J, Bulsara KR, George TM (2005) Correlation of cerebrospinal fluid flow dynamics and headache in Chiari I malformation. Neurosurgery 56:716–721PubMedCrossRefGoogle Scholar
  20. 20.
    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
  21. 21.
    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 59:140–146PubMedCrossRefGoogle Scholar
  22. 22.
    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
  23. 23.
    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:E5PubMedCrossRefGoogle Scholar
  24. 24.
    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
  25. 25.
    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:E3PubMedCrossRefGoogle Scholar
  26. 26.
    Goh S, Bottrell CL, Aiken AH, Dillon WP, Wu YW (2008) Presyrinx in children with Chiari malformations. Neurology 71:351–356PubMedCrossRefGoogle Scholar
  27. 27.
    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 35:214–223PubMedCrossRefGoogle Scholar
  28. 28.
    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
  29. 29.
    Struck AF, Haughton VM (2009) Idiopathic syringomyelia: phase-contrast MR of cerebrospinal fluid flow dynamics at level of foramen magnum. Radiology 253:184–190PubMedCrossRefGoogle Scholar
  30. 30.
    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
  31. 31.
    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 56:1765–1768PubMedCrossRefGoogle Scholar
  32. 32.
    Heiss JD, Patronas N, DeVroom HL et al (1999) Elucidating the pathophysiology of syringomyelia. J Neurosurg 91:553–562PubMedCrossRefGoogle Scholar
  33. 33.
    Frydrychowicz A, Francois CJ, Turski PA (2011) Four-dimensional phase contrast magnetic resonance angiography: potential clinical applications. Eur J Radiol 80:24–35PubMedCrossRefGoogle Scholar
  34. 34.
    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 36:368–377PubMedCrossRefGoogle Scholar
  35. 35.
    Johnson KM, Markl M (2010) Improved SNR in phase contrast velocimetry with five-point balanced flow encoding. Magn Reson Med 63:349–355PubMedCrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2012

Authors and Affiliations

  • Alexander C. Bunck
    • 1
    • 7
    Email author
  • Jan Robert Kroeger
    • 1
  • Alena Juettner
    • 1
  • Angela Brentrup
    • 2
  • Barbara Fiedler
    • 3
  • Gerard R. Crelier
    • 4
  • Bryn A. Martin
    • 5
  • Walter Heindel
    • 1
  • David Maintz
    • 1
    • 6
  • Wolfram Schwindt
    • 1
  • Thomas Niederstadt
    • 1
  1. 1.Department of Clinical RadiologyUniversity Hospital of MuensterMuensterGermany
  2. 2.Department of NeurosurgeryUniversity Hospital of MuensterMuensterGermany
  3. 3.Department of General PediatricsUniversity Hospital of MuensterMuensterGermany
  4. 4.Institute for Biomedical EngineeringETH and University of ZurichZurichSwitzerland
  5. 5.Laboratory of Hemodynamics and Cardiovascular Technology, School of Engineering, Interfaculty Institute of BioengineeringEcole Polytechnique Federale de LausanneLausanneSwitzerland
  6. 6.Department of RadiologyUniversity Hospital of CologneCologneGermany
  7. 7.Department of RadiologyUniversity of CologneCologneGermany

Personalised recommendations