CSF flow imaging in Chiari 1
malformation
Wende Gibbs, MD, Department of Neuroradiology
Gabriel Zada, MD, Department of Neurosurgery
John Liu, MD, Department of Neurosurgery
Patrick Hsieh, MD, Department of Neurosurgery
Meng Law, MD, MBBS, Department of Neuroradiology
University of Southern California, Keck School of Medicine
Control # 1775
eEdE-227
Disclosures

Wende Gibbs: none

Gabriel Zada: none

John Liu: none

Patrick Hsieh: none

Meng Law: Toshiba Grant Speakers Bureau; Bracco
speaker and consultant; Guerbet Medical Advisory
Board; Prism Stock; Fuji speaker and consultant
Purpose

Chiari 1 malformation (CM1) has traditionally been
defined by morphologic criteria: cerebellar tonsil
herniation 3-6mm below the foramen magnum

It is increasingly clear that CM1 is a complex disorder
resulting from not only abnormal anatomy, but
disordered CSF flow

This 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
Approach

Review theories of pathogenesis of CM1, focusing on
the interplay of anatomy and CSF flow dynamics

Describe 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 treatment
Introduction

CM1 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 images1-3

However, 30 - 50% of individuals with tonsillar herniation
greater than 5mm are asymptomatic4

In those individuals with symptoms, the degree of
herniation does not correlate well with symptom severity5

Further, 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 age
Introduction
Both abnormal anatomy and aberrant CSF flow dynamics
contribute to the pathophysiology of CM1
Anatomy/Morphology
Posterior fossa anatomy
Tonsillar herniation
Spinal canal geometry
CSF dynamics
Complex CSF flow patterns
Resistance to flow
Abnormal flow velocity
Pressure gradients
Craniospinal compliance
Pathology/Symptoms
Syrinx
Suboccipital headache
Motor or sensory dysfunction
Fatigue
Pain
Introduction

Suboccipital decompressive surgery is a standard
treatment for CM1

35-45% of patients have minimal or no relief years
after surgery7,8

The 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 fields
CM1 Imaging

The observation of cerebellar tonsillar ectopia in the absence of
syrinx, hydrocephalus, or suggestive signs and symptoms has
uncertain clinical significance

When signs and symptoms are present, neuroimaging is vital to
diagnosis and management
Symptoms

Headache (typically suboccipital)

Neck, back, face pain

“Cape” pain: neck, upper back, shoulders

Nonradicular limb pain

Weakness

Dizziness

Vertigo

Slurred speech

Syncope

Difficulty swallowing

Tinnitus
Signs
Cranial nerve:
 Dysphagia
 Dysarthria
 Hoarseness
 Cough
 Nystagmus
Cerebellar
 Ataxia
 Dysmetria
Brainstem
 Nystagmus
 Sleep apnea
Sensorineural
hearing loss
 Hypertension
 Sinus
bradycardia/tachy
cardia
 Syncope
Spinal cord
 Hyperactive
reflexes
 Babinski,
Hoffman reflex




Spastic gait
Urinary
incontinence,
frequency
Extremity
weakness
CM1 Imaging

Routine imaging sequences
are obtained to evaluate for
hydrocephalus, syrinx, or other
craniocervical junction (CCJ)
pathology

The midline sagittal image is
used to quantify cerebellar
tonsillar ectopia in relation to a
line connecting the basion and
opisthion (McRae’s line,
foramen magnum)
CM1 Imaging: Classification



Chiari 0:
 Tonsils descend 3mm or less below the foramen magnum
 Syrinx
 +/- crowding at foramen magnum
Chiari 1:
 Greater than 5mm tonsillar descent in age >15 year
 Greater than 6mm tonsillar descent in age < 15 years
 3-5 mm is borderline, and abnormal if syrinx or symptoms
 4th ventricle remains in normal position
Chiari 1.5:
 Herniation of tonsils
 Elongation and displacement of 4th ventricle and brainstem
Chiari 0 and Chiari 1.5 are controversial classifications
CM1 Imaging
Static features of CM1 - anatomy and morphology – are studied with
traditional MRI and CT sequences
Degree of tonsillar herniation
Tonsillar shape
Posterior fossa volume
Posterior fossa crowdedness
Linear Posterior Fossa Measures:
 Clivus
 Supraocciut
 Twining line
 McRae Line
Dynamic aspects of CM1 are
evaluated with CSF flow
techniques and computational
fluid dynamic simulations
CSF velocity
CSF stroke volume
Tonsil and cord movement
Pressure
Resistance to flow
Craniospinal compliance
CM1 Imaging: Morphology

The morphologic abnormality in CM1 is diverse

In general, CM1 is characterized by:


Pointed configuration of the tonsils

More vertically oriented cerebellar folia

Crowded foramen magnum

Narrowed retrocerebellar and premedullary
subarachnoid space

Lower limits of normal or small posterior fossa

Short clivus

Inferior 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
CM1 Imaging: Morphology

Posterior cranial fossa (PCF) volumetry is a potential
predictor of surgical outcome9,10

Alpern et. al. studied 20 morphologic and physiologic
measures, of which 10 were found to discriminate CM1
from healthy controls better than tonsillar herniation alone

The three parameters that best characerized CM1:
 Cord displacement
 Posterior cranial fossa crowdedness
 Normalized posterior cranial fossa volume

Using these three parameters, 37 healthy subjects and
35/36 CM1 subjects were correctly classified10
CM1 Imaging: Morphology

Complex CMI (cCMI) has recently been
described in the neurosurgical literature as a CMI
variant with more severe clinical phenotype

Recognition by the radiologist is useful as cCMI
may require more extensive or repeat
neurosurgical procedures

Moore and Moore evaluated a number of
morphologic measures and found that obex level
was the most important differentiating factor
between CMI and cCMI11

Inferior herniation of the obex below the foramen
magnum (FM) and a prominent dorsal bump was
observed in all patients with cCMI in their study

Typical CMI is characterized by obex above or at
the FM
Complex CMI: The
obex lies just below the
FM (arrow).
CM1 Imaging: Dynamic

CSF dynamics in the cranial and spinal subarachnoid
space may be equally important to morphology in the
pathophysiology of CM1

CSF velocity, resistance to flow, pressure, and
craniospinal compliance cannot be measured with
static MR techniques

Dynamic evaluation of CSF flow has primarily been
studied with 2D phase contrast MRI

New techniques developed to study flow include 4D
PC MRI and Time inversion recovery pulse (TimeSLIP)
Morphology
Abnormal morphology of
cerebellar tonsils at the FM:
-crowding of neural structures
-narrowed subarachnoid space
Obstruction of CSF pulsations
Cranial arterial driving pressure
forces same volume of CSF
against obstruction
Increased pressure: may
further displace or damage
neural structures
Hydrodynamics
Increased pressure gradient
Elevated CSF velocity
Altered craniospinal
compliance
Increased resistance to CSF
flow
Increased pressure: over time
may alter neural elasticity,
permeability, water content
Surgical decompression alleviates crowding, results in decreased peak CSF velocity,
and alters craniocervical CSF compliance
CM1 Imaging: Phase Contrast

2D PC MRI in axial and/or sagittal orientation has been
used to quantitatively and qualitatively evaluate dynamic
CSF features such as:

Direction of flow
 Peak CSF velocity
 Pulse wave velocity in the subarachnoid space
 Relative timing of CSF and arterial pulsations

Before 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 venc
 Velocities above the Venc produce aliasing artifact
 Velocities significantly below the Venc have weak signal
CM1 Imaging: Phase Contrast

Magnitude and phase images provide information about anatomy
and velocity

The phase image, reflecting spin phase shifts, is the most sensitive
to flow

Quantitative information is acquired with images in the axial plane
with through-plane velocity encoding in the craniocaudal direction

Qualitative features of flow are observed in the sagittal plane with
in-plane velocity encoding

Peripheral cardiac gating allows for collection of 12-24 phases
during the repetition interval, depending on HR

By convention, bright signal reflects caudal motion during systole
and dark signal represents cranial motion during diastole
CM1 Imaging: Phase Contrast
Phase 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 Contrast

The 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 decompression

However, there is not an established correlation
between change in velocity and the degree of clinical
improvement

CM1 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 models5,12,13
CM1 Imaging: Phase Contrast

McGirt 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 syrinx8

Abnormal ventral and dorsal flow was associated with
a 2.6-fold reduction in risk of symptom recurrence
after surgery

These findings support the role of inhomogeneous
flow patterns in CM1 pathophysiology
CM1 Imaging: Phase Contrast

Time-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 field

Using 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 SAS

This results in flow jets with
elevated velocities and flow
vortices14
A
B
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.
CM1 Imaging: Phase Contrast

Peak 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 technique

The volumetric measurement facilitated by the 4D
technique demonstrated variability among patients as to
the level where peak systolic flow was found

Inconsistent results in prior studies may relate to the
inability of the 2D technique to capture the correct level
for peak flow measurement
CM1 Imaging: Time-SLIP

Another 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 concept

In this case, instead of flowing blood, CSF is used as an
endogenous tracer

Advantages over phase contrast include:

Superior anatomic detail

Shorter acquisition time

Improved evaluation of non periodic or turbulent flow
CM1 Imaging: Time-SLIP

First 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 flow

When images are acquired, the labeled CSF flows
into regions of suppressed background with high
conspicuity

CSF bulk flow can be observed for up to 5 seconds
before contrast between tagged and non tagged CSF
is lost
Time-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 nontagged
background
(red arrow)
CM1 Imaging: Time-SLIP
A
B
Time-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.
CM1 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) CSF
 Notice 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 aqueduct
 Turbulent flow is seen in the 4th ventricle
(moving dark lines in the midst of bright
CSF)
 CSF moves within the cervical syrinx
 At the end of 5 seconds, contrast between
Click to play cine clip.
tagged and untagged CSF is lost
CM1 Imaging: Time-SLIP
Click to play cine clip.
2D Phase Contrast
Click to play cine clip.
Time-SLIP
2D PC demonstrates the presence and direction of flow. Time-SLIP
allows better visualization of location of flow, as well as periodic
and turbulent flow.
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.
A. Initial imaging. Sagittal T1-W image shows
ectopic, pointed cerebellar tonsils and crowding
at the foramen magnum (FM).
A
B
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.
C
D
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 2: 43-year-old man with 10 year history of upper and lower extremity weakness
and numbness, ataxia, increasing difficulty with fine motor control.
Click to play cine clip.
A
The 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.
Click to play cine clip.
B
The 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.
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.15
Case 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 preexisting tonsillar ectopia. He underwent posterior fossa decompression, C1 laminectomy,
and duraplasty.
A
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.
B
Click to play cine clip.
C
Click to play cine clip.
D
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.
Case 4. 49-year-old woman with history of suboccipital headaches.
Click to play cine clip.
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?)
Click to play cine clip.
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.
Time-SLIP

Investigators are currently devising methods to quantify
flow velocity on Time-SLIP16

PC MR and Time-SLIP provide complementary information
for the characterization of pathologies with aberrant CSF
flow dynamics

CSF 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 interventions
Summary

Historically and currently, neuroimaging is vital to
diagnosis and management of CM1

The 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 fields

Emerging techniques such as 4D PC MRI and TimeSLIP are providing unique insights into CSF flow
dynamics in CM1 and other pathologies resulting
from disordered CSF flow dynamics
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