Research on MR Imaging and CSF Flow for the Chiari I Maformation

Introduction

Here, we review the imaging characteristics of Chiari I, in particular how they relate to the newer CSF (cerebrospinal fluid) flow imaging techniques.

Early observations with MR Imaging

MRI, which produces high-resolution images in sagittal, coronal or axial planes, simplified the detection of tonsillar descent. MR showed that the tonsillar tips were located above the foramen magnum in most individuals, and that in about 0.77% of the general population they extended more than 5 mm below the foramen magnum. 13 A radiologist 3 reported that in patients with tonsils extending more than 5 mm into the spinal canal, symptoms are likely to occur, and with tonsils extending less than 5 mm into the spinal canal, symptoms are unlikely. So traditionally, tonsillar descent of 5 mm or more has been generally accepted as the formal definition of the term Chiari I malformation. However, a subsequent report in a larger group of patients indicated that the degree of tonsillar descent does not predict the type or presence of symptoms. 13 The report demonstrated that some patients with tonsils extending less than 5 mm into the foramen magnum were symptomatic, while others with descent greater than 5 mm were asymptomatic. Therefore, the measurement of tonsillar descent is of questionable value in the selection of patients for treatment.

Observations with MR methods to image CSF flow

MR Imaging strategies (Cardiac Gated Phase Contrast MR or PC MR) were developed to image blood and CSF flow. PC MR in Chiari I patients showed that CSF flow posterior to the cord was obstructed and anterior to the cord was accelerated by the position of the tonsils. 14 These observations, and the improvement in syringomyelia and symptoms after cranio-cervical decompression supported the theory that neurologic signs and symptoms in the Chiari I malformation were due to hyperkinetic CSF flow.

For PC MR flow imaging, images are obtained in one plane at 14 time intervals in a cardiac cycle with techniques optimized for measuring flow in the range of 2 to 20 cm/sec. 2,4,10 Results of imaging differ depending on whether a sagittal plan or an axial plane is selected. If the sagittal plane is selected, flow is imaged over much of the cervical spine, but only in the midline, where the most extreme velocities are not found. If the axial plane is selected, flow is measured only at the foramen magnum or one segment of the spinal canal, but the most extreme velocities lateral to the midline are detected. Compared with normal volunteers, Chiari I patients have uniformly abnormal CSF flow profiles.5 After successful cranio-cervical decompression, CSF flow profiles have a more normal pattern. The investigators concluded that abnormal CSF flow, together with arachnoid scarring and increased vulnerability of the spinal cord to CSF pressures are factors in the pathogenesis of syringomyelia.

Flow velocities reach 12 cm/sec in Chiari I patients and 5 cm/sec in healthy adults. 7 In some regions such as the antero-lateral subarachnoid space CSF velocities are greatly elevated, while in other regions, such as the posterior subarachnoid space and the midline region of the anterior subarachnoid space, CSF flow is reduced or absent. Large jets of flow in the posterior-lateral subarachnoid space, flow in both a craniad and a caudad direction at the same time and unidirectional flow throughout the cardiac cycle were observed in some regions within the subarachnoid space. 14 Criteria based on PC MR for the diagnosis of Chiari I malformation, for selecting patients for surgical intervention or for differentiating symptomatic from asymptomatic Chiari I malformations PC MR are not yet defined. 7 Compliance, that is the relationship between the cranial and spinal CSF volumes and pressures has been found to be lower in Chiari I patients than in controls.

MR Imaging Research

The goal of imaging in patients with the Chiari I malformation is to select patients who will benefit from cranio-cervical decompression. The measurement of tonsillar ectopia does not predict improvement from surgical decompression. PC MR imaging may help distinguish patients who are symptomatic from the malformation from those who are asymptomatic from it. However, routine cine MRI studies have an accuracy of only about 60-70%. 9 Differentiation based on the pattern of flow as opposed to the general extent of flow might be more helpful. Using present methods of flow analysis, a pattern that is found exclusively in the symptomatic patients is synchronous bidirectional flow, that is the simultaneous presence of a jet (high velocity in one region) and a counter jet in an adjacent location in the subarachnoid space (in other words, the simultaneous presence of flow caudad and cephalad).

Computational Flow Dynamics in the study of CSF flow

With mathematical equations such as the Navier-Stokes, the pressure and velocity of a fluid in a conduit can be calculated from its shape and size and the volume of flow entering it. Very sophisticated programs have been developed, termed Computational Flow Dynamics or CFD, which have been applied to the flow of CSF in the spinal canal of patients with the Chiari I malformation. In one study, an exact model was created, in which the subarachnoid spaces of a normal subject and of a Chiari I patient are modeled, and pressures and velocities are calculated for each point within the subarachnoid space. The calculations show that fluid flowing in the foramen magnum of the patient with Chiari I malformation has jets anterior to the spinal cord, in the location where they are shown with PC MR. The authors also show that velocities increase with distance along the spinal canal, and that corresponding CSF pressures are elevated as velocities increase. 15 Computational scientists have been able to model CSF flow throughout the cardiac cycle in an idealized model of the subarachnoid space. 11 In this idealized model, flow differences are shown when the tonsils are displaced into the upper cervical spinal canal. This study confirmed that CSF velocities increase with distance from the foramen magnum in the upper cervical spinal canal. With PC MR, the increased CSF velocities predicted from CFD are found in patients studied with multislice PC MR imaging. 16 CFD promises to improve our understanding of CSF flow, because it has extremely good spatial and temporal resolution, because it provides both flow and pressure measurements, and because it demonstrates the internal structure of flow. The flow of CSF is not simple "plug flow" in and out of the cranial vault but complex flow due to the complex anatomy and to inertial effects in fluid streams. 8 Furthermore, the spinal canal is not a rigid structure but an elastic one, so that moving fluids result in pressure waves. These pressure waves may also contribute to the development of syringomyelia and to neurologic signs and symptoms in Chiari I patients. 12 Additional CFD studies will enhance our understanding of CSF flow and will guide our efforts to design simple and accurate clinical and imaging tests to determine which symptoms result from the malformation and which patients will benefit from surgical decompression. CFD creates the possibility of performing a "virtual decompression" on a patient to determine the size and dimension of the surgical intervention in order to restore normal CSF flow to the spinal canal.

References

  1. Alperin N, Kulkarni K, Loth F, et al. Analysis of magnetic resonance imaging-based blood and cerebrospinal fluid flow measurements in patients with Chiari I malformation: a system approach. Neurosurg Focus 2001;11(1):E6.
  2. Armonda RA, Citrin CM, Foley KT, Ellenbogen RG. Quantitative cine-mode magnetic resonance imaging of Chiari I malformations: an analysis of cerebrospinal fluid dynamics. Neurosurgery 1994;35:214-223; discussion 223-214.
  3. Barkovich AJ, Wippold JF, Sherman JL, et al. Significance of cerebellar tonsillar position on MR. Am J Neuroradiol 1986;7:795-799.
  4. Bhadelia RA, Bogdan AR, Wolpert SM, et al. Cerebrospinal fluid flow waveforms: analysis in patients with Chiari I malformation by means of gated phase-contrast MR imaging velocity measurements. Radiology 1995;196:195-202.
  5. Ellenbogen RG, Armonda RA, Shaw DW, Winn HR. Toward a rational treatment of Chiari I malformation and syringomyelia. Neurosurg Focus 2000;8(3):E6
  6. Friede RL, Roessmann U. Chronic tonsillar herniation: an attempt at classifying chronic hernitations at the foramen magnum. Acta Neuropathol. 1976;34(3):219-35.
  7. Heiss JD, Patronas N, DeVroom HL, et al. Elicidating the pathophysiology of syringomyelia. J. Neurosurgery 1999;91:553-562.
  8. Hentschel S, Linge S, Løvgren EA, Mardal K.-A. Cerebrospinal fluid flow. In Automated Scientific Computing (Logg A, Mardal KA, Wells GN, eds). To appear in Springer, 2009.
  9. Hofkes SK, Iskandar BJ, Turski PA, Gentry LR, McCue JB, Haughton VM. Differentiation between symptomatic Chiari I malformation and asymptomatic tonsillar ectopia by using cerebrospinal fluid flow imaging: initial estimate of imaging accuracy. Radiology 2007;245(2):532-540.
  10. Hofman E, Warmuth-Metz M, Bendzus M, Solymosi L. Phase-contrast MR imaging of the cervical CSF and spinal cord: Volumetric motion analysis in patients with Chiari I malformation. American Journal of Neuroradiology 2000;21:151-158.
  11. Linge S, Haughton V, Løvgren AE, Mardal K, Langtangen HP. Effect of tonsillar herniation on cyclic cranio-vertebral CSF fluid flow studied with computational flow analysis. Am J Neuroradiol, in press
  12. Loth F, Yardimci MA, Alperin N. Hydrodynamic modeling of cerebrospinal fluid motion within the spinal cavity. J Biomech Eng 2001;123:71–79.
  13. Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS. Asynmptomatic Chiari Type I malformations identified on magnetic resonance imaging. J Neurosurg. 2000;92:920-6.
  14. Quigley MF, Iskandar BJ, Quigley MA, Nicosia MN, Haughton V. Cerebrospinal fluid flow in foramen magnum: Temporal and spatial patterns at MR imaging in volunteers and in patients with Chiari I malformation. Radiology 2004;232:229–236.
  15. Roldan A, Wieben O, Haughton V, Osswald T, Chesler N. Characterization of CSF hydrodynamics in the presence and absence of tonsillar ectopia by means of computational flow analysis. Am Journal of Neurorad 2009;30:941-946.
  16. Shah S, Haughton V. CSF flow through the upper cervical spinal canal in the Chiari I malformation. (in preparation)



Revised 10/2009

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