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.
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References
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 33:1901–1906
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:E6
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
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 217:877–885
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 35:214–224
Banik R, Lin D, Miller NR (2006) Prevalence of Chiari I malformation and cerebellar ectopia in patients with pseudotumor cerebri. J Neurol Sci 247:71–75
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 196:195–202
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 32:739–742
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 22:1860–1870
Eide PK (2006) A new method for processing of continuous intracranial pressure signals. Med Eng Phys 28:579–587
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
Eide PK, Sorteberg W (2007) Association among intracranial compliance, intracranial pulse pressure amplitude and intracranial pressure in patients with intracranial bleeds. Neurol Res 29:798–802
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 66:80–91
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
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 158:341–347
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 157:1411–1423
Greitz D (2006) Unraveling the riddle of syringomyelia. Neurosurg Rev 29:251–263
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 143:909–917
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
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 31:997–1002
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 33:1326–1330
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 245:532–540
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
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 32:1474–1481
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 31:185–192
Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS (2000) Asymptomatic Chiari type I malformations identified on magnetic resonance imaging. J Neurosurg 92:920–926
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
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 232:229–236
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 33:1756–1762
Shaffer N, Martin B, Loth F (2011) Cerebrospinal fluid hydrodynamics in type I Chiari malformation. Neurol Res 33:247–260
Shah S, Haughton V, del Rio AM (2011) CSF flow through the upper cervical spinal canal in Chiari I malformation. AJNR Am J Neuroradiol 32:1149–1153
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 24:20–23
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 34:1397–1404
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 37:755–758
Urchuk SN, Plewes DB (1994) MR measurements of pulsatile pressure gradients. J Magn Reson Imaging 4:829–836
Wagshul ME, Eide PK, Madsen JR (2011) The pulsating brain: a review of experimental and clinical studies of intracranial pulsatility. Fluids Barriers CNS 8:5
Williams B (1981) Simultaneous cerebral and spinal fluid pressure recordings. 2. Cerebrospinal dissociation with lesions at the foramen magnum. Acta Neurochir 59:123–142
Wolpert SM, Bhadelia RA, Bogdan AR, Cohen AR (1994) Chiari I malformations: assessment with phase-contrast velocity MR. AJNR Am J Neuroradiol 15:1299–1308
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:e52284
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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.
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Frič, R., Lindstrøm, E.K., Ringstad, G. et al. 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. Acta Neurochir 158, 2295–2304 (2016). https://doi.org/10.1007/s00701-016-2979-x
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DOI: https://doi.org/10.1007/s00701-016-2979-x