High-quality MRS detects metabolic changes in mice at different stages of prion disease
Eleni Demetriou1, Mohamed Tachrount2, Karin Shmueli3, Mark Farrow4, and Xavier Golay1

1Brain Repair and Rehabilitation, Institute of Neurology, London, United Kingdom, 2Brain repair and rehabilitation, Institute of Neurology, London, United Kingdom, 3Medical Physics and Biomedical Engineering, University College of London, London, United Kingdom, 4MRC prion unit, University College of London, London, United Kingdom

Synopsis

The neurochemical profile of prion disease in mice at different disease stages was evaluated using high-quality MR spectra obtained in thalamus. Seven metabolites were measured in vivo and longitudinally providing substantial metabolic information. Metabolic changes were obtained throughout the disease course, however only glutamate and myo-inositol were significantly different at all stages of the disease. We conclude that MR spectroscopy provides additional information over previous histological studies [1].

Introduction

Prion diseases are fatal neurodegenerative disorders that have prolonged asymptomatic incubation periods. The mechanism by which prions cause brain damage remains unclear and therefore characterization of early pathology would be of benefit for the diagnosis and treatment of this chronic neurodegenerative disorder. In-vivo proton spectroscopy allows quantitative measures of metabolite concentrations. Moreover, there are few MRS studies in murine models of prion disease and the data were acquired with relatively long-TE spectroscopic sequences [2,3]. To gain a better insight into metabolic alterations associated with prion disease in mice we performed MRS at short TE in the thalamus of prion-infected mice at different stages of prion disease.

Methods

Two groups of 7-week-old FVB mice were intracerebrally inoculated with 30μl of 1% brain homogenate from Rocky Mountain Laboratory prion-infected mice (n=19) or brain homogenate from uninfected mice as controls (n=11). The prion-infected group was separated into three groups of mice scanned at different stages of prion disease: 80 days post injection (dpi) – asymptomatic-stage (n=6), 130 dpi – early-stage (n=6), and 160 dpi – late-stage (n=7). Control mice were separated into two groups: 80 dpi (n=5) and 160 dpi (n=6). All mice were anaesthetized (1.5-1.8% isoflurane in 1.5% oxygen with balance in air) and scanned on a 9.4 T Agilent system using a 33-mm-diameter transmit/receive coil (Rapid Biomedical). Anatomical scans were acquired in an axial slice (thickness = 2mm) using a fast spin-echo sequence (data matrix: 256x128, TR=3000ms, TE=20ms, FOV=20x20mm). In vivo proton spectra were acquired using a PRESS sequence (TR = 5000msec, TE = 7.5msec and TE = 144 mec, 128 averages, total acquisition time=10 min) with a voxel centered on the thalamus (1.7 x 4.3 x 1.8 mmᶾ). After first and second order shimming, the typical linewidth of the water resonance was 20-23Hz.

Data analysis: Metabolite concentrations were estimated using TARQUIN [4]. Experimental data were modelled as a linear combination of modified simulated basis signals. The Cramer-Rao lower bounds were used as a reliability measure of the metabolite concentration estimates. All metabolite concentrations are presented as mean ± standard deviation. Statistical analysis was performed using a two-tailed test. Significant changes in metabolite concentrations are indicated by p<0.05.

Results

The metabolite concentrations were evaluated for age dependence between the two control groups scanned at 80 dpi and 160 dpi. The only change with age was an increase in N-acetylaspartate (NAA ) (p=0.009) and creatine (Cr) (p=0.005 ). Therefore, the control groups were merged into one group when compared with prion-infected mice for all the metabolites except NAA and Cr. Significant changes were detected in glutamate (Glu) and myo-inositol (Ins) at all stages of prion disease (80 dpi, 130 dpi, 160 dpi) when compared with the control group. However, there was no significant change in Choline (Cho). NAA, Cr, Lactate and Lipids were only found to be significantly different at 130 dpi and 160 dpi compared with the control group. Moreover, Taurine (Tau) was only significantly increased at 80 dpi without any significant change at 130 dpi and 160 dpi (fig 1). Figure 2 shows representative MRS spectra in thalamus from a control and a prion-infected mouse at 160 dpi.

Discussion and Conclusion

In this study, we evaluated the neurochemical profile of prion-infected mice at different stages of prion disease. There are very few In-vivo MRS studies in mice infected with scrapie/prions and these have reported changes including a decrease in the ratio of NAA to both Cho and Cr and an increase of Ins in prion-infected mice [2,3]. Our experiments showed additional results compared with previous studies in prion-infected mice including a significant increase in lactate and lipids at 130 dpi and 160 dpi. Increased Ins most likely reflects neuronal loss and microglial activation as shown in previous histological studies [1], while a reduction in Glu might be secondary to reduced brain function. We conclude that high-quality/short-TE MR spectroscopy provides additional information about characteristic changes occurring in thalamus of prion-infected mice in line with previous histological studies [1].

Acknowledgements

No acknowledgement found.

References

[1] Sandberg M, Al-Doujaily H, Sharps B et al. Prion neuropathology follows the accumulation of alternate prion protein isoforms after infective titre has peaked.Nat Commun. 2014;5:4347;

[2]Broom K, Daniel A, Lowe J et al. MRI and MRS alterations in the preclinical phase of murine prion disease:Association with neuropathological and behavioural changes. Neurobiol Dis 2007; 26(3):707-717;

[3] Bell J, Cox J, Williams S et al. In vivo detection of metabolic changes in a mouse model of scrapie using nuclear magnetic spectroscopy. J Gen Virol 1991; 72:2419-2423.

[4] Wilson M, Reynolds G, Kauppinen RA et al. A constrained least-squares approach to the automated quantitation of in vivo ¹H magnetic resonance spectroscopy data. Magn Reson Med. 2011; 65:1-12.

Figures

Figure 1 Comparison of the concentration of metabolites in thalamus between prion-infected mice at different stages of prion disease and control mice. Data are expressed as mean ± standard deviation (* p<0.05, ** p<0.005, *** p<0.0005).

Figure 2 Representative ¹H MRS spectra acquired in thalamus of a prion-infected mouse (b) and a control mouse (a) at 160 dpi. The arrows indicate metabolites that showed significant differences in concentration between the prion-infected and control groups. The PRESS voxel in the thalamus is shown overlaid on a representative anatomical image.



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