PowerPoint Presentation
CSF flow imaging in Chiari 1 malformationWende Gibbs, MD,
Department of NeuroradiologyGabriel Zada, MD, Department of
NeurosurgeryJohn Liu, MD, Department of NeurosurgeryPatrick Hsieh,
MD, Department of NeurosurgeryMeng Law, MD, MBBS, Department of
Neuroradiology
University of Southern California, Keck School of
MedicineControl # 1775eEdE-227
1DisclosuresWende Gibbs: noneGabriel Zada: noneJohn Liu:
nonePatrick Hsieh: noneMeng Law: Toshiba Grant Speakers Bureau;
Bracco speaker and consultant; Guerbet Medical Advisory Board;
Prism Stock; Fuji speaker and consultant2PurposeChiari 1
malformation (CM1) has traditionally been defined by morphologic
criteria: cerebellar tonsil herniation 3-6mm below the foramen
magnumIt is increasingly clear that CM1 is a complex disorder
resulting from not only abnormal anatomy, but disordered CSF
flowThis exhibit will review static and dynamic imaging tools
applied to the study of CM1, including new techniques that may
improve diagnostic accuracy, patient management and surgical
outcome
3ApproachReview theories of pathogenesis of CM1, focusing on the
interplay of anatomy and CSF flow dynamicsDescribe established and
recently developed neuroimaging tools used to study CM1:
traditional MRI sequences and dynamic techniques including phase
contrast MR and Time-spatial labeling inversion pulse technique
(Time-SLIP) Demonstrate the utility of Time-SLIP in providing a
rapid, individualized assessment of CSF flow before and after
surgical treatment4IntroductionCM1 has historically been described
as a change in hindbrain morphology characterized by cerebellar
tonsil herniation 3-6mm* below the foramen magnum on sagittal MRI
or CT images1-3However, 30 - 50% of individuals with tonsillar
herniation greater than 5mm are asymptomatic4In those individuals
with symptoms, the degree of herniation does not correlate well
with symptom severity5Further, a subset of patients with CM1
symptoms have no tonsillar herniation, suggesting abnormal
morphology alone cannot explain CM1 symptomatology6*The degree of
herniation is not universally agreed upon, and depends upon
age5IntroductionBoth abnormal anatomy and aberrant CSF flow
dynamics contribute to the pathophysiology of
CM16IntroductionSuboccipital decompressive surgery is a standard
treatment for CM135-45% of patients have minimal or no relief years
after surgery7,8The search for a noninvasive method of selecting
patients with CM1 symptoms who will benefit from surgical
intervention is an active area of research across many fields7CM1
ImagingHeadache (typically suboccipital)Neck, back, face painCape
pain: neck, upper back, shouldersNonradicular limb
painWeaknessDizzinessVertigoSlurred speechSyncopeDifficulty
swallowingTinnitusCranial
nerve:DysphagiaDysarthriaHoarsenessCoughNystagmusCerebellarAtaxiaDysmetriaBrainstemNystagmusSleep
apneaSensorineural hearing lossHypertensionSinus
bradycardia/tachycardiaSyncopeSpinal cordHyperactive
reflexesBabinski, Hoffman reflexSpastic gaitUrinary incontinence,
frequencyExtremity weakness
SymptomsSignsThe observation of cerebellar tonsillar ectopia in
the absence of syrinx, hydrocephalus, or suggestive signs and
symptoms has uncertain clinical significanceWhen signs and symptoms
are present, neuroimaging is vital to diagnosis and management8CM1
ImagingRoutine imaging sequences are obtained to evaluate for
hydrocephalus, syrinx, or other craniocervical junction (CCJ)
pathologyThe midline sagittal image is used to quantify cerebellar
tonsillar ectopia in relation to a line connecting the basion and
opisthion (McRaes line, foramen magnum)
Menick Neurosurg focus 20019CM1 Imaging: ClassificationChiari 0:
Tonsils descend 3mm or less below the foramen magnumSyrinx+/-
crowding at foramen magnumChiari 1:Greater than 5mm tonsillar
descent in age >15 yearGreater than 6mm tonsillar descent in age
< 15 years3-5 mm is borderline, and abnormal if syrinx or
symptoms4th ventricle remains in normal positionChiari
1.5:Herniation of tonsils Elongation and displacement of 4th
ventricle and brainstemChiari 0 and Chiari 1.5 are controversial
classifications
10CM1 ImagingDegree of tonsillar herniationTonsillar
shapePosterior fossa volumePosterior fossa crowdednessLinear
Posterior Fossa Measures:ClivusSupraocciutTwining lineMcRae
Line
CSF velocityCSF stroke volumeTonsil and cord
movementPressureResistance to flowCraniospinal compliance
Static features of CM1 - anatomy and morphology are studied with
traditional MRI and CT sequencesDynamic aspects of CM1 are
evaluated with CSF flow techniques and computational fluid dynamic
simulations11CM1 Imaging: MorphologyThe morphologic abnormality in
CM1 is diverseIn general, CM1 is characterized by:Pointed
configuration of the tonsilsMore vertically oriented cerebellar
foliaCrowded foramen magnumNarrowed retrocerebellar and
premedullary subarachnoid spaceLower limits of normal or small
posterior fossaShort clivusInferior elongation of the 4th ventricle
with mildly low-lying nucleus gracilis (the demarcation of obex and
central canal)40-80% of symptomatic CM1 have a syrinx4
Menick Neurosurg focus 200112CM1 Imaging: MorphologyPosterior
cranial fossa (PCF) volumetry is a potential predictor of surgical
outcome9,10Alpern et. al. studied 20 morphologic and physiologic
measures, of which 10 were found to discriminate CM1 from healthy
controls better than tonsillar herniation aloneThe three parameters
that best characerized CM1:Cord displacementPosterior cranial fossa
crowdednessNormalized posterior cranial fossa volumeUsing these
three parameters, 37 healthy subjects and 35/36 CM1 subjects were
correctly classified10
Alpern 201413CM1 Imaging: MorphologyComplex CMI (cCMI) has
recently been described in the neurosurgical literature as a CMI
variant with more severe clinical phenotypeRecognition by the
radiologist is useful as cCMI may require more extensive or repeat
neurosurgical proceduresMoore and Moore evaluated a number of
morphologic measures and found that obex level was the most
important differentiating factor between CMI and cCMI11Inferior
herniation of the obex below the foramen magnum (FM) and a
prominent dorsal bump was observed in all patients with cCMI in
their studyTypical CMI is characterized by obex above or at the
FM
Complex CMI: The obex lies just below the FM (arrow).
Alpern 201414CM1 Imaging: DynamicCSF dynamics in the cranial and
spinal subarachnoid space may be equally important to morphology in
the pathophysiology of CM1CSF velocity, resistance to flow,
pressure, and craniospinal compliance cannot be measured with
static MR techniquesDynamic evaluation of CSF flow has primarily
been studied with 2D phase contrast MRINew techniques developed to
study flow include 4D PC MRI and Time inversion recovery pulse
(Time-SLIP)
Alpern 201415Abnormal morphology of cerebellar tonsils at the
FM:-crowding of neural structures-narrowed subarachnoid
spaceObstruction of CSF pulsationsElevated CSF velocityIncreased
resistance to CSF flowAltered craniospinal complianceCranial
arterial driving pressure forces same volume of CSF against
obstructionIncreased pressure: over time may alter neural
elasticity, permeability, water contentIncreased pressure: may
further displace or damage neural
structuresMorphologyHydrodynamicsIncreased pressure
gradientSurgical decompression alleviates crowding, results in
decreased peak CSF velocity, and alters craniocervical CSF
complianceCM1 Imaging: Phase Contrast2D PC MRI in axial and/or
sagittal orientation has been used to quantitatively and
qualitatively evaluate dynamic CSF features such as:Direction of
flowPeak CSF velocityPulse wave velocity in the subarachnoid
spaceRelative timing of CSF and arterial pulsationsBefore PC MR
images are acquired, maximum CSF velocity must be anticipated in
order to set the Venc (velocity encoding)To optimize signal, CSF
velocity should be the same or slightly below the vencVelocities
above the Venc produce aliasing artifactVelocities significantly
below the Venc have weak signal17CM1 Imaging: Phase
ContrastMagnitude and phase images provide information about
anatomy and velocityThe phase image, reflecting spin phase shifts,
is the most sensitive to flowQuantitative information is acquired
with images in the axial plane with through-plane velocity encoding
in the craniocaudal directionQualitative features of flow are
observed in the sagittal plane with in-plane velocity
encodingPeripheral cardiac gating allows for collection of 12-24
phases during the repetition interval, depending on HRBy
convention, bright signal reflects caudal motion during systole and
dark signal represents cranial motion during diastole18
CM1 Imaging: Phase ContrastPhase images in sagittal orientation
in cine mode
White flow is moving caudally during systole
Black flow is moving cranially during diastole
In this patient with CMI, there is craniocaudal flow ventral to
the brainstem and upper cervical cord Craniocaudal flow dorsal to
the tonsils and cord is minimal.Click to play cine clip.CM1
Imaging: Phase ContrastThe majority of studies utilizing 2D PC MRI
show that CM1 is characterized by elevated peak CSF flow velocity
at the foramen magnum, and that peak velocity decreases after
decompressionHowever, there is not an established correlation
between change in velocity and the degree of clinical
improvementCM1 is characterized by inhomogeneous flow patterns and
simultaneous bidirectional flow: important findings confirmed in
subsequent studies using different techniques, including 4D PC MRI
and computation flow models5,12,1320CM1 Imaging: Phase
ContrastMcGirt et al. found that pediatric CM1 patients with normal
CSF flow at the FM as assessed by PC MR were 4.8-fold more likely
to experience symptom recurrence following surgery regardless of
the degree of tonsillar herniation or presence of syrinx8Abnormal
ventral and dorsal flow was associated with a 2.6-fold reduction in
risk of symptom recurrence after surgeryThese findings support the
role of inhomogeneous flow patterns in CM1 pathophysiology21CM1
Imaging: Phase ContrastTime-resolved three directional velocity
encoded phase contrast MRI (4D PC MRI) is a recent advance that can
better assess the three dimensional complexities of the CSF flow
fieldUsing 4D PC MRI, Bunck et al. showed that in CM1, the anterior
subarachnoid space (SAS) is markedly narrowed, with CSF flow
diversion to the anterolateral SASThis results in flow jets with
elevated velocities and flow vortices14
Coronal 4D PC MRI images in control (A) and CM1 (B). Compare
uniform, homogeneous flow in A, with lateral flow diversion and
left sided flow jet in B.
Bunck et al, Eur Radiology (2012) 22:1860-1870.AB22CM1 Imaging:
Phase ContrastPeak CSF velocities were significantly greater at the
craniocervical junction in CM1 patients than in controls, a finding
in most, but not all prior studies using the 2D PC MR techniqueThe
volumetric measurement facilitated by the 4D technique demonstrated
variability among patients as to the level where peak systolic flow
was foundInconsistent results in prior studies may relate to the
inability of the 2D technique to capture the correct level for peak
flow measurement23CM1 Imaging: Time-SLIPAnother recently developed
MR technique applied to the study of CSF flow dynamics is
Time-spatial labeling inversion pulse (Time-SLIP)Time-SLIP is based
upon the arterial spin labeling conceptIn this case, instead of
flowing blood, CSF is used as an endogenous tracerAdvantages over
phase contrast include:Superior anatomic detail Shorter acquisition
timeImproved evaluation of non periodic or turbulent flow
24CM1 Imaging: Time-SLIPFirst the background signal is
suppressed with a non selective inversion recovery pulse This is
followed by a second, spatially selective pulse perpendicular to
the direction of flowWhen images are acquired, the labeled CSF
flows into regions of suppressed background with high
conspicuityCSF bulk flow can be observed for up to 5 seconds before
contrast between tagged and non tagged CSF is lost25Time-SLIP
A nonselective IR pulse is applied, inverting all signal in the
field of view
A second, spatially selective inversion pulse is applied to the
region of interest
After a short period of time, tagged CSF is seen moving into the
non-tagged background (red arrow)26CM1 Imaging: Time-SLIPTime-SLIP
in CM1 after surgical decompression. The initial image (A) shows
the location of the selective pulse (gold lines). Tagged CSF is
bright in this slice. All other CSF is suppressed (dark). After
several seconds (B) tagged CSF is seen above and below the slice
(gold lines), ventral to the brainstem and cord and dorsal to the
cerebellum and cord (orange arrows). *Note the exquisite anatomic
detail of the images allowing precise localization of CSF flow, a
significant advantage over PC MR images.
AB27CM1 imaging: Time-SLIP
In this cine clip, we watch the movement of CSF over 5 seconds.
Gold lines mark the selective pulse with tagged (bright) CSFNotice
the movement of CSF above and below the slice with time We observe
features of flow not possible by any other technique:CSF moves from
the 4th ventricle superiorly into the aqueductTurbulent flow is
seen in the 4th ventricle (moving dark lines in the midst of bright
CSF)CSF moves within the cervical syrinxAt the end of 5 seconds,
contrast between tagged and untagged CSF is lost
Click to play cine clip.28CM1 Imaging: Time-SLIP
2D Phase ContrastTime-SLIP2D PC demonstrates the presence and
direction of flow. Time-SLIP allows better visualization of
location of flow, as well as periodic and turbulent flow.Click to
play cine clip.Click to play cine clip.Walker 9/5 and 9/1229A.
Initial imaging. Sagittal T1-W image shows ectopic, pointed
cerebellar tonsils and crowding at the foramen magnum (FM).B. The
preoperative Time-SLIP image demonstrates flow ventral the cervical
cord (blue arrow). No flow is seen dorsal to the cord below the FM
(gold arrow). Yellow lines indicate the tagged slice. All bright
CSF above and below the lines has flowed from the tagged slice.C.
Post decompression sagittal T2-W image reveals relief of crowding
at the FM. More CSF is seen dorsal and inferior to the tonsils. A
small amount of fluid is seen posterior to the duraplasty.D. Post
operative Time-SLIP image again shows CSF flow ventral to cervical
cord (blue arrow). There is now flow dorsal to the cord at this
level (gold arrow).Case 1: 35 year-old man with 2 years of
worsening headache, facial pain, and developing slurred speech. MRI
demonstrated tonsillar herniation 16mm below the foramen magnum.
After decompression with C1 and partial C2 laminectomies and
duraplasty, the patient had marked improvement of his headaches and
resolution of his facial pain.
ABCD30The pre-operative Time-SLIP image demonstrates flow
ventral to the cord, but only trace flow dorsal to the cord at the
tagged level (level marked by gold dots). A small amount of flow is
also seen within the syrinx.
AClick to play cine clip.
BClick to play cine clip.The high intrinsic signal to noise and
temporal resolution of Time-SLIP in comparison to 2D PC MRI allows
visualization of CSF movement in response to respiration.
Respiratory motion may have a greater effect on CSF flow than
cardiac pulsation.15The post-decompression study reveals increased
flow dorsal to the cord. Craniocaudal flow within the syrinx has
also increased. Interestingly, there is a small amount of cranial
flow of fluid within the pseudomeningocele. This may relate to
respiration. Case 2: 43-year-old man with 10 year history of upper
and lower extremity weakness and numbness, ataxia, increasing
difficulty with fine motor control.31Case 3: 58-year-old man with
complicated history of cervical stenosis with myelopathy post C6-T1
laminectomy and fusion one year ago. Increasing difficulty with
gait, balance, and left leg weakness prompted imaging. He was found
to have an increase in his pre-existing tonsillar ectopia. He
underwent posterior fossa decompression, C1 laminectomy, and
duraplasty.8/2014 and 12/2014. The patient had only partial
improvement in symptoms. Time-SLIP shows that there is no flow
dorsally at the FM. The brisk ventral flow is already apparent on
the first image. 4 months later, the pseudomeningocele is noted to
be larger. There is no change in CSF flow pattern. There is no
cranial flow in the fourth ventricle, an abnormal finding.5/2014.
The preoperative image shows crowding at the FM, increased from
prior studies. The focus of abnormal T2 signal in the cord at C7/T1
reflects myelomalacia. The post decompression image shows relief of
crowding. There is a large pseudomeningocele.
Click to play cine clip.ABCDClick to play cine clip.32
Case 4. 49-year-old woman with history of suboccipital
headaches.Note the short clivus, small posterior fossa, and
superiorly oriented straight sinus, typical of CM1. Crowding at the
FM is minimal but there is a large cervical syrinx (Chiari 0?)
Note the change in shape of the syrinx in relation to the flow
in the ventral and dorsal SAS at that level. No flow is seen
dorsally at the FM. Note the cranially-directed flow through the
aquaduct into the third ventricle, a normal finding.
Selective tagging pulses can be performed at multiple levels and
in different orientations, as long as the slice is perpendicular to
the flow direction of interest. A coronal orientation can evaluate
flow between the lateral and third ventricles.Click to play cine
clip.Click to play cine clip.33Time-SLIP
Investigators are currently devising methods to quantify flow
velocity on Time-SLIP16PC MR and Time-SLIP provide complementary
information for the characterization of pathologies with aberrant
CSF flow dynamicsCSF dynamics visualized with Time-SLIP differ from
classic CSF circulation theories, and the development of this
method has advanced knowledge of CSF physiology A better
understanding of CSF dynamics in health and disease may lead to
increased diagnostic accuracy and better patient selection for
surgical interventionsyamada34SummaryHistorically and currently,
neuroimaging is vital to diagnosis and management of CM1The search
for a noninvasive method of selecting patients with CM1 symptoms
who will benefit from surgical intervention is an active area of
research across many fieldsEmerging techniques such as 4D PC MRI
and Time-SLIP are providing unique insights into CSF flow dynamics
in CM1 and other pathologies resulting from disordered CSF flow
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