Aaron E Rusheen1,2, Elise M Berning1, Dane T Bothun1, Ben T Gifford1, Stephan J Goerss1, Kirk M Welker3, John Huston3, Kevin E Bennet1,4, Yoonbae Oh1,5, Charles D Blaha1, Kendall H Lee1,5, and Fagan J Andrew3
1Department of Neurosurgery, Mayo Clinic, Rochester, MN, United States, 2Medical Scientist Training Program, Mayo Clinic, Rochester, MN, United States, 3Department of Radiology, Mayo Clinic, Rochester, MN, United States, 4Department of Engineering, Mayo Clinic, Rochester, MN, United States, 5Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, United States
Synopsis
7.0T MRI provides
precise visualization and targeting of brain structures for image-guided stereotactic
neurosurgery. However, image localizers used by stereotactic systems do not
exist for 7.0T scanners. Challenges in their development include: the small
bore creates geometric constraints that disallow use of conventional localizers,
and the increased B0 increases geometric distortion, affecting
registration accuracy. Here, a skull-contoured localizer utilizing point
fiducials was designed to attach to a novel stereotactic frame. Extracranial
distortion was thoroughly mapped using several optimized imaging sequences.
This data was used to optimally place fiducials on the localizer, improving
registration accuracy.
Introduction
MRI is critical
to functional neurosurgery for navigation and accurate targeting of specific
neurologic structures and pathologies.1 This is especially important
in the approach for deep brain stimulation (DBS).2 3.0T MRI does not
afford the necessary signal/contrast-noise ratios (SNR/CNR) to resolve small neural
targets, and hence indirect targeting methods (human brain atlases) and
intra-operative microelectrode recordings (target verification) are required for
placement of DBS electrodes. 7.0T MRI offers the potential to parcellate brain
structures for direct targeting and identify unseen neural connections through
diffusion tensor imaging.3 Thus, 7.0T MRI offers safer, more
effective, and more individualized surgery.
For high
quality 7.0T imaging to be applicable to stereotactic targeting, the stereotactic
image localizer must fit within the narrow head coil. Presently, conventional
N-bar designs are much too large. Another major problem is the increased
geometric distortion with 7.0T which, for stereotactic surgery, can lead to
inaccuracies in intervention and sub-optimal outcomes. Image geometric distortions
cause shifts in true fiducial locations which impacts registration and
ultimately targeting accuracy.4 Sources of distortion include gradient
nonlinearities, imperfect B0 shimming, B1 inhomogeneity, chemical
shift artifacts, and susceptibility-induced distortions. Optimal sequence
design can mitigate these distortions, while maintaining the required image spatial
and contrast resolution for target visualization.
The aim of this
study was to design a head localizer frame with fiducial placements at
extracranial locations exhibiting minimal geometric distortions when imaged
with optimized imaging sequences at 7.0T. Sequences were refined in phantom
and human experiments, with extracranial distortions thoroughly mapped with
high spatial resolution in the 3D space.Methods
A prototype skull-contoured
localizer was designed to fit within the reduced diameter of the FDA-approved head
coil (1Tx/32Rx, Nova Medical). The localizer integrated with a novel “D1” stereotactic system previously developed in
our laboratory (Figure 1).
This system utilizes a small skull-secured device platform that permits rigid
attachment of the image localizer to the skull. The localizer had 8 custom-made 4mm spherical fiducials placed in a unique geometric pattern on the localizer to allow for proper right/left,
anterior/posterior, and superior/inferior image registration. The localizer was affixed to imaging phantoms with targetable points and filled with oil (Marcol
82); this set-up was used to determine fiducial and target registration errors
(FRE/TRE), and for protocol optimization (Figure 2a). Human imaging (n=3) was performed
with approval from the local IRB (IRB#19-002599), at 7.0T (Terra, Siemens). MPRAGE,
FGATIR, T2-w, and SWI imaging sequences were optimized (Table 1). The receiver
bandwidth was varied, commensurate with adequate SNR, to minimize geometric
distortions. A trained neurosurgeon evaluated the images to ensure good
visualization of the target nuclei
(subthalamic nucleus, globus pallidus, ventrointermedial thalamus).
Extracranial
distortion was analyzed via a custom distortion analysis device that fit around
the subject’s head within the head coil, comprising 46 fiducial locations with
known ‘ground truth’ positions (Figure 2b). Following rigid image registration, the
global and local distortions were determined for each image sequence using
custom python software. This was used to refine the initial prototype design of
the localizer for fiducial placement in areas of low distortion. The finalized optimized localizer was used in
phantom studies to investigate the improvement in registration errors (both TRE
and FRE).Results
Phantom testing
with the prototype localizer revealed an FRE/TRE of 3.69-6.43mm/ >10mm, respectively.
Initial parameterization revealed that increased receiver bandwidth significantly
reduced this degree of error.
Human tests
were then conducted using the distortion analysis device. Low bandwidth
sequences demonstrated an overall higher geometric distortion (FRE: 1.61mm) compared
to high bandwidth sequences (FRE: 1.37mm) (n=3 for each unique sequence). For
high bandwidth sequences, registration errors of 1.5±0.09mm, 1.49±0.14mm, 1.47±0.03mm,
and 1.02±0.04mm were found for MPRAGE, FGATIR, T2, and SWI, respectively. For
low bandwidth sequences, registration errors of 2.01±0.15mm, 1.74±0.2mm, 1.53±0.09mm,
and 1.15±0.05mm were found for MPRAGE, FGATIR, T2, and SWI, respectively. Statistically
significant increases in fiducial registration error were found between high
and low bandwidths in MPRAGE and FGATIR sequences (paired t-test, Figure 3, 4).
In addition,
individual displacement of fiducials after registration compared with their
known ground truth locations permitted the creation of 3D distortion maps. These
maps were used to modify the image localizer for placement of fiducials in
areas that demonstrated reduced distortion (image not shown, patent pending). Overall,
this new localizer demonstrated a FRE of 1.2-1.4mm and a TRE of 0.72-2.4mm.Discussion
7.0T imaging
enhanced visualization of neural targets. Detailed mapping of extracranial
distortion among a number of clinical sequences demonstrated nonuniform
magnitudes of distortion, with lower distortion for the high bandwidth
sequences. Relatively increased distortion was observed at the base of the
skull and above the apex of the head, with lower distortion near the center of
the head. These data helped guide the precise fiducial placement on the finalized
localizer design, in extracranial locations that demonstrated the least amount
of distortion. The registration errors (1-2mm) found with this new localizer are
in the clinically acceptable range and will be used in further experiments to
determine its accuracy for stereotactic targeting. Furthermore, the distortion
data generated here is generalizable to other applications, such as placement
of skin fiducials or eventual 7.0T intra-MRI surgery. Acknowledgements
We would like to acknowledge the Mayo Clinic Department of Radiology for their support of our imaging experiments. We would also like to acknowledge our sources of support: the Grainger Foundation, NIH MSTP T32 (GM065841) and NRSA TL1 (TR002380) training grants. References
1. Kelly, P.
J., Sharbrough, F. W., Kall, B. A. & Goerss, S. J. Magnetic resonance
imaging-based computer-assisted stereotactic resection of the hippocampus and
amygdala in patients with temporal lobe epilepsy. Mayo Clin Proc 62, 103-108,
doi:10.1016/s0025-6196(12)61877-1 (1987).
2. Cho, Z. H.
et al. Direct visualization of deep brain stimulation targets in Parkinson
disease with the use of 7-tesla magnetic resonance imaging. J Neurosurg 113,
639-647, doi:10.3171/2010.3.JNS091385 (2010).
3. Lenglet, C.
et al. Comprehensive in vivo mapping of the human basal ganglia and thalamic
connectome in individuals using 7T MRI. PLoS One 7, e29153,
doi:10.1371/journal.pone.0029153 (2012).
4. Voormolen et al. Implications of
Extracranial Distortion in Ultra-High-Field Magnetic Resonance Imaging for
Image-Guided Cranial Neurosurgery. World Neurosurgery 26:e250-e258, doi:
0.1016/j.wneu.2019.02.028