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DOI 10.1007/s00062-015-0383-1
R e v i e w A rt i c l e
Abstract The purpose of this article is to review the temporal resolution. Cine bSSFP MRI uses cardiac gating
physiology of normal brain and spinal cord motion in the to evaluate dynamically the brain and spinal cord with high
subarachnoid space, principles of cine balanced steady- contrast and temporal resolution.
state free precession (bSSFP) magnetic resonance imaging Cine bSSFP can be used in the evaluation of idiopathic
(MRI), clinical applications, and the pitfalls encountered syringomyelia to assess an underlying treatable cause, in-
with this technique. cluding arachnoid bands, which are usually not well vi-
The brain and spinal cord are dynamic structures that sualized with conventional MR sequences due to motion
move with each heartbeat due to transmitted arterial pulse artifact. This MRI technique is also useful in the evaluation
waves. Conventional MRI sequences do not allow ana- of intraspinal and intracranial arachnoid cysts and the de-
tomic evaluation of the pulsatile movement of the neural gree of mass effect on the cord. Other applications include
structures in the subarachnoid space due to limitations in preoperative and postoperative evaluation of Chiari I mal-
formation and the evaluation of lateral ventricular asym-
metry. The major limitation of cine bSSFP is the presence
Electronic supplementary material The online version of this of banding artifacts, which can be reduced by shimming
article (doi: 10.1007/s00062-015-0383-1) contains supplementary
material, which is available to authorized users.
and modifying other scan parameters.
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2 A.E. Li et al.
ing on static techniques for diagnosis ignores the dynamics The Monro–Kellie hypothesis states that the cranium has
of the neural structures within the subarachnoid space: the a fixed volume. The sum of the brain, blood (arteries and
brain and spinal cord move in synchrony with each arterial veins), and CSF volume is constant, and an increase in one
pulse wave. component will cause a decrease in at least one of the other
Cine bSSFP is an MRI technique that uses retrospec- two components [8].
tive cardiac gating to dynamically evaluate the brain and With each cardiac cycle, in early systole, there is an
spinal cord, thereby providing high contrast and tempo- arterial pulsation with expansion of the intracranial arter-
ral resolution. Standard static MRI sequences of the brain ies, leading to capillary dilatation. This causes expansion of
and spinal cord are limited by temporal resolution lead- the brain with caudal displacement of the central structures
ing to motion-related blurring of nonstatic structures. Cine such as the diencephalon, brainstem, and cerebellar tonsils
bSSFP has superior temporal resolution, virtually eliminat- [9]. The normal degree of brain displacement is approxi-
ing movement artifact. At our institution, cine bSSFP has a mately 0.4 mm for the cerebellar tonsils, and 0.1–0.2 mm
temporal resolution of approximately 45 ms compared with for the brainstem and other posterior fossa structures [2, 9]
2500–5000 ms in conventional static T2-weighted (T2W) (Fig. 1). This is balanced by simultaneous cephalic motion
sequences. of the more peripheral structures such as the cerebral hemi-
Cine bSSFP MRI has been used in the diagnosis of arach- spheres and posterior cerebellum [9].
noid membranes in the subarachnoid space, which were not The caudal motion of the brainstem is a rapid piston-like
visible on conventional T2W sequences due to pulsatile motion, causing displacement of CSF from the foramen
motion of the structures in the spinal canal. Gottschalk et al. magnum into the spinal subarachnoid space [10]. The CSF
[1] reported a case of syringomyelia, in which preoperative pulse wave then propagates through the spinal canal [10,
cine bSSFP MRI demonstrated arachnoid membranes in the 11]. The cervical cord also moves caudally with movement
dorsal subarachnoid space, the presence of which was surgi- of the brainstem [9]. This expansion of the brain compresses
cally confirmed when the patient underwent microsurgical the lateral ventricles, promoting CSF flow through the fora-
lysis. Cousins and Haughton [2] used cine bSSFP to study men of Monro and cerebral aqueduct. In diastole, there is
the degree of motion of the cerebellar tonsils in the foramen a gradual return to the brain to its neutral position [7]. The
magnum and found that there was 0.57-mm biphasic ton- overall direction of CSF flow is caudal in systole and cranial
sillar displacement in patients with Chiari I malformation, in diastole [11].
compared with 0.43 mm in controls. The movement of the
pulsatile neural structures including the lamina terminalis
has also been studied with cine bSSFP [3].
Cine bSSFP has been used elsewhere in the body, most
notably in cardiac MRI. The high contrast between blood
and myocardial or vessel wall makes it effective in the
assessment of cardiac wall motion, ventricular function,
and the cardiac valves [4]. Cine bSSFP has also been used
in the dynamic evaluation of the pelvic floor, with images
acquired at rest, during sphincter contraction, straining, and
defecation [5]. Cine SSFP MRI technique has also been
used with MR enterography to identify small bowel stric-
tures and lesions, and evaluate intestinal motility [6].
In this article, we review normal brain motion, the physics
of cine bSSFP, clinical applications, artifacts, and pitfalls.
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Clinical Applications of Cine Balanced Steady-State Free Precession MRI for the Evaluation 3
Steady State
Balanced SSFP refers to the use of balanced gradients in Cardiac Gating for Cine Imaging
all three axes (slice selection, phase encoding, and readout)
[4]. Dephasing caused by each applied gradient is compen- Cardiac gating is achieved by the use of an electrocardio-
sated or balanced by applying a gradient of opposite polar- gram (ECG) signal or recording a pulse oximetry trace.
ity, to keep the gradient moment constant, with a net zero Data for a single slice are acquired at multiple points over
area over one TR (Fig. 2) [12]. This results in the sequence the cardiac cycle, which are called cardiac phases [16]. The
being relatively insensitive to motion. Furthermore, phase data for each cardiac phase is set to generate a single image
alternation of the RF pulse flip angle α by 180° (− α) occurs corresponding to that cardiac phase. The images for all the
within a single TR [13]. cardiac phases are viewed sequentially in a cine loop. The
Balanced SSFP uses both free induction decay and spin- number of phases and the heart rate determine the tempo-
echo components for image formation, the former of which ral resolution. For example, an acquisition with 20 cardiac
contains mixed T1 and T2* weighting, and the latter which phases and a heart rate of 72 beats/min results in a temporal
is strongly T2W with little T2*W [4]. Contrast in bSSFP is resolution of 41.7 ms.
determined mainly by the T2/T1 ratio of tissue [12]. Tissues
such as CSF have a high T2/T1 ratio, which results in high
contrast between CSF and the brain and spinal cord [14, 15]. MRI Protocol
Static steady-state precession MRI has been used to obtain
static 3D myelographic-like images of the cervical spine, The MRI protocol at our institution is as follows: 3.0-T scan-
with high SNR and high contrast between CSF and the spi- ner (Siemens Verio) with a 32-channel head coil. Localizer
nal cord. SNR is high, as the transverse magnetization is images, T1W and T2W sequences of the brain, and cervical
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4 A.E. Li et al.
spine are acquired in addition to phase-contrast sequences. Phase-contrast MRI can be utilized to detect the level
These sequences are used to assess the best plane for cine of CSF flow obstruction, which is inferred by the absence
bSSFP, which in most cases is a midline sagittal slice cen- of CSF pulsations [18] or by flow disturbance (Fig. 4d).
tered on the foramen magnum (for Chiari malformation) or The use of phase-contrast MRI alone is limited, as this
at the level of spinal cord pathology. Additional cine bSSFP technique relies on detection of flow abnormalities and
sequences can be obtained in the axial or coronal plane to assumptions about sites of obstruction and does not allow
further delineate pathology. visualization of arachnoid membranes. Phase-contrast MRI
Peripheral pulse oximetry is used for cardiac synchro- can be performed in conjunction with bSSFP to evaluate
nization, with 20 cardiac phases, segments set of 10–12, which arachnoid bands cause CSF flow obstruction. Using
TE of 1.9 ms, TR of 41.7/20 = 2.1 ms, flip angle of 35–55°, both sequences allows the evaluation of the anatomy and
field of view of 158 mm, bandwidth of 916 Hz, and in-plane dynamic significance of these arachnoid bands.
resolution of 0.5 × 0.9 mm with a slice thickness of 3 mm.
A cardiac shim protocol is performed prior to the scan to Spinal Intradural Arachnoid Cyst
reduce banding artifact (see “Pitfalls and Artifacts” section).
For studies of the spinal cord, a body surface coil is used. Spinal arachnoid cysts are usually CSF-containing spaces
Peripheral cardiac synchronization with pulse oximetry is lined by arachnoid mater and can be intradural or extradural
used, as opposed to ECG synchronization, due to its rela- in location. These may be primary lesions that are congenital
tive simplicity and without apparent compromise in diag- or idiopathic. Primary intradural arachnoid cysts are usually
nostic image quality. Total image acquisition time for this located in the midline dorsally, arising from the septum pos-
sequence is approximately 4.5 min. ticum, which is a membranous partition in the dorsal spinal
subarachnoid space in the thoracic region [19]. Secondary
intraspinal arachnoid cysts are thought to arise from dural
Clinical Applications tears or adhesions related to previous trauma, inflammation,
or hemorrhage, although the pathogenesis is debatable [20,
The following clinical applications of cine bSSFP in study- 21]. Secondary arachnoid cysts can arise dorsally, ventrally,
ing the motion of neural structures in the subarachnoid space or laterally. Overall, the most common site for intraspinal
will be discussed: idiopathic syringomyelia, spinal intradu- arachnoid cysts is dorsal to the thoracic cord [21, 22].
ral arachnoid cyst, lateral ventricular asymmetry, Chiari I Intradural arachnoid cysts may communicate with the
malformation preoperative and postoperative evaluation, subarachnoid space via a narrow neck and are then called
and other applications. arachnoid diverticula [21]. These cysts can enlarge due to
a one-way valve effect, and cause spinal cord compression
Idiopathic Syringomyelia [20]. Other arachnoid cysts become walled off and are sepa-
rate from the subarachnoid space.
Syringomyelia refers to the formation of a cavity in the spi- These have been traditionally diagnosed by myelogra-
nal cord. The syrinx may be associated with Chiari malfor- phy, computed tomography myelography, or conventional
mation, tumor, trauma, infection, or be “idiopathic,” where MRI sequences [22, 23]. With myelographic techniques,
no underlying cause has been demonstrated. A proportion of the arachnoid cyst can be seen to fill with contrast medium
presumed idiopathic syringomyelia cases are thought to be if there is a communication between the cyst and the sub-
due to the obstruction of CSF flow around the spinal cord, arachnoid space. The drawback of myelography is the inva-
which may be due to underlying arachnopathies including sive nature of the technique. The presence of arachnoid
arachnoid membranes or arachnoid cysts [17]. cysts can be diagnosed on conventional MRI sequences if
Microsurgical lysis is the treatment of choice for patients the cyst walls are visible, or may be inferred by the mass
with symptomatic syringomyelia due to arachnoid adhe- effect on the spinal cord. Phase-contrast MRI may dem-
sions. Identification of arachnoid membranes or adhesions onstrate abnormal flow around the cyst, or dynamic spinal
is essential in the process of selecting patients for surgery. cord compression by the cyst, although anatomical details
Arachnoid membranes are usually not well seen on of the cyst are not delineated [24].
standard static T2 sequences due to motion blur with each Intradural arachnoid cysts can be diagnosed with cine
CSF pulsation. High-resolution cine bSSFP allows visual- bSSFP, by visualization of the cyst walls, which appear as
ization of arachnoid membranes and adhesions. Arachnoid fine septa moving in synchrony with the spinal cord or with
adhesions appear as a thin transverse or obliquely oriented the transmitted CSF pulse wave (Figs. 4, 5, and 6; Movies
hypointense band between the spinal cord and dura. These 4–8). In addition, this technique provides high-resolution,
bands generally move in synchrony with the spinal cord dynamic assessment of the associated mass effect of intra-
(Fig. 3; Movies 2 and 3). dural cystic structures on the spinal cord (Fig. 7; Movie 9).
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Clinical Applications of Cine Balanced Steady-State Free Precession MRI for the Evaluation 5
Fig. 4 An 80-year-old woman with sensory symptoms. The provision- noid cyst (white arrow), excluding the diagnosis of idiopathic cord
al diagnosis was thoracic cord herniation or an arachnoid cyst based on herniation. d Phase-contrast MRI demonstrates prominent flow signal
static MRI imaging. Sagittal (a) and axial (b) static T2W image shows inferior to the arachnoid cyst wall at the T3 level, with disruption of
focal anterior displacement of the spinal cord at T2/3 (black arrow). flow at the level of the cyst wall (black arrowhead). Prominent flow
There is flattening of the spinal cord, with cord signal hyperintensity signal within the cyst suggests communication with the CSF space.
(open arrow). No arachnoid membrane is seen. c Still image frame See Movie 4 for corresponding cine bSSFP sequence.
from cine bSSFP MRI demonstrates the superior wall of an arach-
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6 A.E. Li et al.
Fig. 6 Subtle case of intradural arachnoid cyst in a 35-year-old man. are visible. Still images from sagittal (b) and coronal (c) cine bSSFP
a Sagittal static T2W image shows focal anterior displacement of the sequence demonstrate a small arachnoid cyst dorsal to the spinal cord.
spinal cord at T6/7 (white arrowhead). The differential diagnosis was The superior and inferior cyst walls (white arrows) are visible. See
initially idiopathic cord herniation or an arachnoid cyst. No cyst walls Movies 7 and 8 for corresponding cine bSSFP sequence.
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Clinical Applications of Cine Balanced Steady-State Free Precession MRI for the Evaluation 7
Fig. 7 A 52-year-old man with a neurenteric cyst. Sagittal (a) and and flattening of the spinal cord. An associated syrinx is seen from T1
axial (b) T2W image show a vertebral fusion anomaly at T3/T4 (ar- to T10 (open arrow). c Phase-contrast MRI demonstrates interrupted
rowhead). An intradural extramedullary cystic lesion (white arrow) is flow signal at the level of the cystic lesion (black arrows). See Movie
seen ventral to the spinal cord at T2/3, causing marked compression 9 for corresponding cine bSSFP sequence.
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8 A.E. Li et al.
The goals of decompression surgery for Chiari I malfor- evaluation of third ventriculostomy and anatomic studies of
mations are to enlarge the volume of the posterior fossa, arachnoid membranes such as the Liliequist membrane [3].
decompress the inferior cerebellum, and re-establish CSF Cine bSSFP can also delineate the septations in a syrinx,
flow through the foramen magnum [38]. Various surgical which are often too fine to resolve on conventional T2W
techniques have been used to achieve this. Commonly used sequences (Fig. 11; Movie 15). Another potential application
approaches include osseous decompression, with or without of cine bSSFP is the diagnosis of tethered cord syndrome,
dural grafting, intradural dissection of adhesions, and resec- allowing comparison of spinal cord motion in pre- and post-
tion of the cerebellar tonsils [39]. surgical settings. Constructive interference in steady-state
Postoperatively, cine bSSFP allows dynamic visualiza- (CISS) MRI techniques have been reported to allow visual-
tion of the movement of the posterior fossa structures, rather ization of the tethered filum terminale [40]. CISS MRI has
than relying on assumptions based on CSF flow as in phase- also been used to demonstrate the cyst wall and scolex in
contrast MRI. Postsurgical complications such as adhesions cases of intraventricular neurocysticercosis [41], and this
can be diagnosed on bSSFP by detection of a fine hypoin- may be another potential application of cine bSSFP MRI.
tense arachnoid band tethering the cerebellum or cervical
cord to the cranium or the duraplasty or tethering of the dor-
sal cerebellar surface to the overlying dural graft (Fig. 10; Pitfalls and Artifacts
Movies 13 and 14).
The main artifact with cine bSSFP is the presence of band-
Miscellaneous ing artifact, which commonly occurs in the thoracic spine
[1]. This occurs as bSSFP is susceptible to artifacts from
Other proposed clinical applications for bSSFP include the magnetic field inhomogeneities. Banding artifacts appear
evaluation of cerebral aqueduct stenosis and postoperative as thick linear hypointensities that are usually fixed during
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Clinical Applications of Cine Balanced Steady-State Free Precession MRI for the Evaluation 9
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10 A.E. Li et al.
the evaluation of the dynamic movement of the neural struc- Movie 6 Cine bSSFP shows the superior and inferior cyst
tures in the subarachnoid space with each heartbeat. This walls. Further compression of the spinal cord is seen with
technique facilitates the diagnosis of intraspinal or intracra- each heartbeat
nial arachnoid cysts, evaluation of idiopathic syringomy-
elia, lateral ventricular asymmetry, and in the preoperative Movie 7 Sagittal cine bSSFP: the cyst walls are more clearly
and postoperative assessment of Chiari I malformation, appreciated with dynamic imaging
particularly as an adjunct to the more widely used phase-
contrast cine MRI. The main limitation of cine bSSFP MRI Movie 8 Coronal cine bSSFP: the cyst walls are more
is the presence of banding artifacts, which can be minimized clearly appreciated with dynamic imaging
with various techniques.
Movie 9 Sagittal cine bSSFP shows more clearly the cyst
Conflict of Interest No grant funding or financial support was re- walls, with exaggeration of the mass effect on the spinal
ceived by any author for the creation of this work. The authors have no
conflict of interest with the material presented in this article. cord seen each heartbeat
Movie 3 Intraoperative video demonstrates the presence of Movie 13 Sagittal cine bSSFP sequence demonstrates dor-
an arachnoid band dorsal to the spinal cord. Microneurosur- sal tethering of the medulla, inferior cerebellar vermis, and
gical lysis of the arachnoid band is performed upper cervical cord due to adhesions. There is loss of nor-
mal pulsatile motion at the cervicomedullary junction
Movie 4 Sagittal cine bSSFP sequence clearly demonstrates
superior wall of arachnoid cyst and associated mass effect Movie 14 Cine bSSFP following repeat posterior fossa
on the spinal cord decompression and adhesiolysis. Subtle motion of the upper
spinal cord is now seen
Movie 5 Cine phase-contrast scan demonstrates turbulent
flow at the superior margin of the arachnoid cyst Movie 15 Corresponding cine bSSFP shows fine septations
within syrinx
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Clinical Applications of Cine Balanced Steady-State Free Precession MRI for the Evaluation 11
Movie 16 Sagittal cine bSSFP sequence shows several thick 18. Mauer UM, Freude G, Danz B, Kunz U. Cardiac-gated phase-
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