Characterising and Modelling Susceptibility Artifacts in the Mouse Brain at 9.4 T
Rosie Goodburn1, Nicholas Powell2,3, James O’Callaghan2, Simon Walker-Samuel2, and Karin Shmueli1

1Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom, 2UCL Centre for Advanced Biomedical Imaging, Division of Medicine, London, United Kingdom, 3UCL Centre for Medical Imaging Computing, London, United Kingdom

Synopsis

Susceptibility artifacts hamper gradient-echo MRI of the mouse brain at 9.4 Tesla. Here, we characterised and modelled magnetic field maps aiming to improve preclinical mouse MRI. To characterise field perturbations, we measured and coregistered field maps in 7 mice to create a group-average field map. Next, a Fourier forward model was used to simulate a field map based on a susceptibility distribution constructed from the group-average magnitude image. The measured and modelled field maps showed similar qualitative field patterns, especially around the aural air cavities, but had quantitative differences. Work is ongoing to improve the accuracy of the model.

Background and Purpose

Susceptibility artifacts, including geometric distortion and signal dropout, result from spatial mismapping due to field perturbations, ΔB, and their spatial gradients, G = ∇B. They are most severe at high field strengths, particularly surrounding air spaces in tissue. We aimed to improve understanding of these artifacts by characterising and modelling field maps of the mouse brain at 9.4 T because susceptibility artifacts hamper high-resolution preclinical MRI at this field strength. Here, we characterised the field maps by calculating an average field map measured in several mice. In addition, a forward susceptibility model was used to simulate a modelled field map, and the measured and modelled field maps were compared.

Data Acquisition

An Agilent 9.4 T VNMRS 20 cm horizontal-bore system was used to image 7 C57BL/6 ten-week-old male mice in vivo1. Prior to imaging, the mice were secured in a cradle under anaesthesia with 1-2% isoflurane in 100% oxygen. A 72-mm-diameter birdcage radiofrequency (RF) coil was used for RF transmission and a mouse brain surface coil array (RAPID, Germany) was used for signal detection. A Multi-Echo Gradient Echo sequence was used with 12 echoes at TE1 = 1.38 ms and ΔTE = 2.64 ms, with isotropic 150 μm voxels and 110×100×100 matrix size. The phase data from the two receive coils were combined by finding the weighted mean of the single coil phase as in Robinson et al2.

Methods

We tested several methods for field map calculation. The best approach, with the least noise and no residual wraps, was to use a nonlinear fit3 of the complex (magnitude and phase) data over time in each voxel, followed by 3D spatial unwrapping (FSL Prelude)4 to unwrap any residual wraps.

Calculating the Average Measured Field Map: This approach was used to calculate field maps for each mouse and global field offset corrections were made by referencing to the mean value in a central region of each mouse field map. Coregistration was then performed using NiftyReg5: Magnitude image volumes were corrected for bias fields using N4ITK6. They were then coregistered using 12 degrees-of-freedom affine transformations (Figure 1). The net transformations, saved as 4x4 matrices, were applied to each corresponding field map. The voxelwise group-average of the 7 offset-corrected and coregistered field maps was then calculated.

Simulating the Modelled Field Map: A model of the underlying susceptibilities was constructed by thresholding the average magnitude image volume and assigning values7 for tissue (-9 ppm) and air (0.36 ppm) susceptibilities. The model was zero-padded by 100 voxels in each dimension. In an attempt to correctly model the mouse tissue susceptibility outside the imaged region, tissue susceptibility values at the edge of the imaged region were replicated along the B0 direction to the edge of the padded field of view. This padded susceptibility model was used to compute the field map using a Fourier forward model8.

Comparing the Measured and Modelled Field Maps: The difference of the measured and modelled field maps was calculated. A mask of the brain region was drawn manually on the average magnitude image (1st echo). Using this mask, histograms of ΔB/B0 were computed in the brains of the measured, modelled and difference field maps. Gradient magnitude maps were also calculated by scaling ΔB/B0 voxelwise difference maps to give gradient maps for each direction, Gx, Gy, and Gz. The gradient magnitude was found for each voxel using: $$$|G|=\sqrt{G_x+G_y+G_z}$$$9.

Results and Discussion

The measured and modelled field maps (Figure 2) appear qualitatively similar, with characteristic dipoles surrounding the aural air cavities. The difference image highlights the fact that the modelled field map seems to have slightly more field perturbation immediately surrounding the aural cavities. This may reflect the additional effect of bone which was not included in the model. Histograms for the measured and modelled field maps (Figure 3) show a difference in the spread and symmetry of field values inside the brain region, possibly due to residual shimming differences. Figure 4 shows the large |G| around the aural cavities where susceptibility artifacts will be worst.

Conclusions and Future Work

The measured and modelled field and gradient maps have qualitatively similar patterns, but differ quantitatively. This is likely to be due to inaccuracies in the susceptibility model such as neglecting the susceptibility of bone and an imprecise representation of the mouse anatomy outside the imaged field of view. Work is ongoing to accurately incorporate these effects into the model. This approach could be used in future to evaluate artifact reduction techniques such as automated10, passive11 or active12 shimming and tailored RF pulses13 in mouse brain studies at 9.4 T.

Acknowledgements

SWS is supported by a Wellcome Trust Senior Research Fellowship (grant WT100247MA).

References

1. O’Callaghan J, Wells J, Shmueli K, and Lythgoe M. In vivo quantitative susceptibility mapping of the mouse brain at 9.4 T: A new contrast mechanism to investigate genetic models of neurodegeneration. Proc Intl Soc Mag Reson Med. 2014;22:349.

2. Robinson S, Grabner G, Witoszynskyj S, and Trattnig S. Combining phase images from multi-channel RF coils using 3D phase offset maps derived from a dual-echo scan. Magn Reson Med. 2011;65(6):1638-1648.

3. Liu T, Wisnieff C, Lou M, et al. Nonlinear formulation of the magnetic field to source relationship for robust quantitative susceptibility mapping. Magn Reson Med. 2013;69(2):467-476.

4. Jenkinson M. Fast, automated, N-D phase-unwrapping algorithm. Magn Reson Med. 2003;49(1):193-197.

5. Modat M. Efficient dense non-rigid registration using the free-form deformation framework. PhD Thesis. London: University College London; 2012.

6. Tustison N, Avants B, Cook P, et al. N4ITK: Improved N3 bias correction. IEEE Trans Med Imaging. 2010;29(6):1310-1320.

7. Schenck J. The role of magnetic susceptibility in magnetic resonance imaging: MRI magnetic compatibility of the first and second kinds. Med Phys. 1996;23(6):815-850.

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9. Wilson J, Jenkinson M, de Araujo I, et al. Fast, fully automated global and local magnetic field optimisation for fMRI of the human brain. NeuroImage. 2002;17(2):967–976.

10. Miyasaka N, Takahashi K, and Hetherington H. Fully automated shim mapping method for spectroscopic imaging of the mouse brain at 9.4 T. Mag Reson Med. 2006;55(1):198-202.

11. Koch K, Brown P, Rothman D, and de Graaf R. Sample-specific diamagnetic and paramagnetic passive shimming. J Magn Reson. 2006;182(1):66-74.

12. Juchem C, Brown P, Nixon T, et al. Multicoil shimming of the mouse brain. Magn Reson Med. 2011;66(3):893-900.

13. Wastling S and Barker G. Designing hyperbolic secant excitation pulses to reduce signal dropout in gradient-echo echo-planar imaging Mag Reson Med. 2015;74(3):661-672.

Figures

Figure 1: The NiftyReg Reg Aladin algorithm was used to coregister the 7 mouse magnitude image volumes by performing these affine transformations5.

Figure 2: Average measured (a-c), modelled (d-f) and difference: measured - modelled (g-i) field maps for 7 mice. Matching horizontal, sagittal and coronal slices are shown centered around a dipolar field pattern (yellow circle) surrounding each aural air cavity. The brain region is shown by the dotted line.

Figure 3: Histograms of field values, ΔB/B0, in the masked brain region (dotted line in Figure 1) of the measured and modelled field maps. Histogram of the difference: measured - modelled field map in the brain region.

Figure 4: Average field gradient magnitude maps for the measured (a-c) and modelled (d-f) field maps. Slices matching those in Figure 1 are shown. Note the region of high |G| around the aural air cavity (yellow circle).



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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