Advertisement

Acta Neurochirurgica

, Volume 158, Issue 12, pp 2295–2304 | Cite as

The association between the pulse pressure gradient at the cranio-cervical junction derived from phase-contrast magnetic resonance imaging and invasively measured pulsatile intracranial pressure in symptomatic patients with Chiari malformation type 1

  • Radek FričEmail author
  • Erika Kristina Lindstrøm
  • Geir Andre Ringstad
  • Kent-André Mardal
  • Per Kristian Eide
Clinical Article - Neurosurgical Anatomy

Abstract

Background

In symptomatic Chiari malformation type 1 (CMI), impaired intracranial compliance (ICC) is associated with an increased cranio-spinal pulsatile pressure gradient. Phase-contrast magnetic resonance imaging (MRI) represents a non-invasive modality for the assessment of the pulse pressure gradient at the cranio-cervical junction (CCJ). We wished to explore how the MRI-derived pulse pressure gradient (MRI-dP) compares with invasively measured pulsatile intracranial pressure (ICP) in CMI, and with healthy controls.

Methods

From phase-contrast MRI of CMI patients and healthy controls, we computed cerebrospinal fluid (CSF) flow velocities and MRI-dP at the CCJ. We assessed bidirectional flow and compared the flow between the anterior and the posterior subarachnoid space at the CCJ. We computed total intracranial volume (ICV), ventricular CSF volume (VV), and posterior cranial fossa volume (PCFV). We analyzed the static and pulsatile ICP scores from overnight monitoring in CMI patients.

Results

Five CMI patients and four healthy subjects were included. The CMI group had a significantly larger extent of tonsillar ectopia, smaller PCFV, and a smaller area of CSF in the FM. The pulsatile ICP (mean ICP wave amplitude, MWA) was abnormally increased in 4/5 CMI patients and correlated positively with MRI-dP. However, the MRI-dP as well as the CSF flow velocities did not differ significantly between CMI and healthy subjects. Moreover, bidirectional flow was observed in both CMI as well as healthy subjects, with no significant difference.

Conclusions

In symptomatic CMI patients, we found a significant association between the pulse pressure gradient at the CCJ derived from phase-contrast MRI and the pulsatile ICP (MWA) measured invasively. However, the MRI-dP was close to identical in CMI patients and healthy subjects. Moreover, the CSF flow velocities at the CCJ and the occurrence of bidirectional flow were not different in CMI patients and healthy individuals. Further studies are required to determine the diagnostic role of phase-contrast MRI in CMI patients.

Keywords

Chiari malformation Phase-contrast magnetic resonance imaging Cerebrospinal fluid flow Intracranial pressure 

Notes

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.

Conflict of interest

The software used for analysis of the ICP recordings (Sensometrics Software) is manufactured by a software company (dPCom AS, Oslo, Norway) in which the last author (PKE) has a financial interest. All other authors declare that they have no conflicts of interest.

References

  1. 1.
    Aiken AH, Hoots JA, Saindane AM, Hudgins PA (2012) Incidence of cerebellar tonsillar ectopia in idiopathic intracranial hypertension: a mimic of the Chiari I malformation. AJNR Am J Neuroradiol 33:1901–1906CrossRefPubMedGoogle Scholar
  2. 2.
    Alperin N, Kulkarni K, Loth F, Roitberg B, Foroohar M, Mafee MF, Lichtor T (2001) Analysis of magnetic resonance imaging-based blood and cerebrospinal fluid flow measurements in patients with Chiari I malformation: a system approach. Neurosurg Focus 11:E6CrossRefPubMedGoogle Scholar
  3. 3.
    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 103:46–52CrossRefPubMedGoogle Scholar
  4. 4.
    Alperin NJ, Lee SH, Loth F, Raksin PB, Lichtor T (2000) MR–intracranial pressure (ICP): a method to measure intracranial elastance and pressure noninvasively by means of MR imaging: baboon and human study. Radiology 217:877–885CrossRefPubMedGoogle Scholar
  5. 5.
    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 35:214–224CrossRefPubMedGoogle Scholar
  6. 6.
    Banik R, Lin D, Miller NR (2006) Prevalence of Chiari I malformation and cerebellar ectopia in patients with pseudotumor cerebri. J Neurol Sci 247:71–75CrossRefPubMedGoogle Scholar
  7. 7.
    Bhadelia RA, Bogdan AR, Wolpert SM, Lev S, Appignani BA, Heilman CB (1995) Cerebrospinal fluid flow waveforms: analysis in patients with Chiari I malformation by means of gated phase-contrast MR imaging velocity measurements. Radiology 196:195–202CrossRefPubMedGoogle Scholar
  8. 8.
    Bhadelia RA, Frederick E, Patz S, Dubey P, Erbay SH, Do-Dai D, Heilman C (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 32:739–742CrossRefPubMedGoogle Scholar
  9. 9.
    Bunck AC, Kroeger JR, Juettner A, Brentrup A, Fiedler B, Crelier GR, Martin BA, Heindel W, Maintz D, Schwindt W, Niederstadt T (2012) Magnetic resonance 4D flow analysis of cerebrospinal fluid dynamics in Chiari I malformation with and without syringomyelia. Eur Radiol 22:1860–1870CrossRefPubMedGoogle Scholar
  10. 10.
    Eide PK (2006) A new method for processing of continuous intracranial pressure signals. Med Eng Phys 28:579–587CrossRefPubMedGoogle Scholar
  11. 11.
    Eide PK (2016) The correlation between pulsatile intracranial pressure and indices of intracranial pressure-volume reserve capacity: results from ventricular infusion testing. J Neurosurg. doi: 10.3171/2015.11.JNS151529 Google Scholar
  12. 12.
    Eide PK, Sorteberg W (2007) Association among intracranial compliance, intracranial pulse pressure amplitude and intracranial pressure in patients with intracranial bleeds. Neurol Res 29:798–802CrossRefPubMedGoogle Scholar
  13. 13.
    Eide PK, Sorteberg W (2010) Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-year review of 214 patients. Neurosurgery 66:80–91CrossRefPubMedGoogle Scholar
  14. 14.
    Frič R, Eide PK (2016) Comparative observational study on the clinical presentation, intracranial volume measurements, and intracranial pressure scores in patients with either Chiari malformation type I or idiopathic intracranial hypertension. J Neurosurg. doi: 10.3171/2016.4.JNS152862 PubMedGoogle Scholar
  15. 15.
    Frič R, Eide PK (2016) Perioperative monitoring of pulsatile and static intracranial pressure in patients with Chiari malformation type 1 undergoing foramen magnum decompression. Acta Neurochir 158:341–347CrossRefPubMedGoogle Scholar
  16. 16.
    Frič R, Eide PK (2015) Comparison of pulsatile and static pressures within the intracranial and lumbar compartments in patients with Chiari malformation type 1: a prospective observational study. Acta Neurochir 157:1411–1423CrossRefPubMedGoogle Scholar
  17. 17.
    Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–263CrossRefPubMedGoogle Scholar
  18. 18.
    Häckel M, Beneš V, Mohapl M (2001) Simultaneous cerebral and spinal fluid pressure recordings in surgical indications of the Chiari malformation without myelodysplasia. Acta Neurochir 143:909–917CrossRefPubMedGoogle Scholar
  19. 19.
    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
  20. 20.
    Hentschel S, Mardal KA, Lovgren AE, Linge S, Haughton V (2010) Characterization of cyclic CSF flow in the foramen magnum and upper cervical spinal canal with MR flow imaging and computational fluid dynamics. AJNR Am J Neuroradiol 31:997–1002CrossRefPubMedGoogle Scholar
  21. 21.
    Hirano M, Haughton V, Munoz del Rio A (2012) Tapering of the cervical spinal canal in patients with Chiari I malformations. AJNR Am J Neuroradiol 33:1326–1330CrossRefPubMedGoogle Scholar
  22. 22.
    Hofkes SK, Iskandar BJ, Turski PA, Gentry LR, McCue JB, Haughton VM (2007) Differentiation between symptomatic Chiari I malformation and asymptomatic tonsillar ectopia by using cerebrospinal fluid flow imaging: initial estimate of imaging accuracy. Radiology 245:532–540CrossRefPubMedGoogle Scholar
  23. 23.
    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
  24. 24.
    Linge SO, Haughton V, Lovgren AE, Mardal KA, Helgeland A, Langtangen HP (2011) Effect of tonsillar herniation on cyclic CSF flow studied with computational flow analysis. AJNR Am J Neuroradiol 32:1474–1481CrossRefPubMedGoogle Scholar
  25. 25.
    Linge SO, Haughton V, Lovgren AE, Mardal KA, Langtangen HP (2010) CSF flow dynamics at the craniovertebral junction studied with an idealized model of the subarachnoid space and computational flow analysis. AJNR Am J Neuroradiol 31:185–192CrossRefPubMedGoogle Scholar
  26. 26.
    Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS (2000) Asymptomatic Chiari type I malformations identified on magnetic resonance imaging. J Neurosurg 92:920–926CrossRefPubMedGoogle Scholar
  27. 27.
    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:E3CrossRefPubMedGoogle Scholar
  28. 28.
    Quigley MF, Iskandar B, Quigley MA, 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 232:229–236CrossRefPubMedGoogle Scholar
  29. 29.
    Rutkowska G, Haughton V, Linge S, Mardal K-A (2012) Patient-specific 3D simulation of cyclic CSF flow at the craniocervical region. AJNR Am J Neuroradiol 33:1756–1762CrossRefPubMedGoogle Scholar
  30. 30.
    Shaffer N, Martin B, Loth F (2011) Cerebrospinal fluid hydrodynamics in type I Chiari malformation. Neurol Res 33:247–260CrossRefPubMedGoogle Scholar
  31. 31.
    Shah S, Haughton V, del Rio AM (2011) CSF flow through the upper cervical spinal canal in Chiari I malformation. AJNR Am J Neuroradiol 32:1149–1153CrossRefPubMedGoogle Scholar
  32. 32.
    Stoverud KH, Mardal KA, Haughton V, Langtangen HP (2011) CSF flow in Chiari I and syringomyelia from the perspective of computational fluid dynamics. Neuroradiol J 24:20–23CrossRefPubMedGoogle Scholar
  33. 33.
    Tain RW, Bagci AM, Lam BL, Sklar EM, Ertl-Wagner B, Alperin N (2011) Determination of cranio-spinal canal compliance distribution by MRI: methodology and early application in idiopathic intracranial hypertension. J Magn Reson Imaging 34:1397–1404CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Thompson A, Madan N, Hesselink JR, Weinstein G, Munoz Del Rio A, Haughton V (2016) The cervical spinal canal tapers differently in patients with Chiari I with and without syringomyelia. AJNR Am J Neuroradiol 37:755–758CrossRefPubMedGoogle Scholar
  35. 35.
    Urchuk SN, Plewes DB (1994) MR measurements of pulsatile pressure gradients. J Magn Reson Imaging 4:829–836CrossRefPubMedGoogle Scholar
  36. 36.
    Wagshul ME, Eide PK, Madsen JR (2011) The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 8:5CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Williams B (1981) Simultaneous cerebral and spinal fluid pressure recordings. 2. Cerebrospinal dissociation with lesions at the foramen magnum. Acta Neurochir 59:123–142CrossRefPubMedGoogle Scholar
  38. 38.
    Wolpert SM, Bhadelia RA, Bogdan AR, Cohen AR (1994) Chiari I malformations: assessment with phase-contrast velocity MR. AJNR Am J Neuroradiol 15:1299–1308PubMedGoogle Scholar
  39. 39.
    Yiallourou TI, Kroger JR, Stergiopulos N, Maintz D, Martin BA, Bunck AC (2012) Comparison of 4D phase-contrast MRI flow measurements to computational fluid dynamics simulations of cerebrospinal fluid motion in the cervical spine. PLoS One 7:e52284CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  • Radek Frič
    • 1
    Email author
  • Erika Kristina Lindstrøm
    • 2
  • Geir Andre Ringstad
    • 3
  • Kent-André Mardal
    • 2
  • Per Kristian Eide
    • 1
    • 4
  1. 1.Department of NeurosurgeryOslo University Hospital – RikshospitaletOsloNorway
  2. 2.Department of Mathematics, Faculty of Mathematics and Natural SciencesUniversity of OsloOsloNorway
  3. 3.Department of Radiology and Nuclear MedicineOslo University Hospital – RikshospitaletOsloNorway
  4. 4.Faculty of MedicineUniversity of OsloOsloNorway

Personalised recommendations