Assessing the effects of pediatric subject motion on T2 relaxation under spin tagging (TRUST) cerebral oxygenation measurements using volume navigators (vNavs)
Jeffrey N Stout1, M. Dylan Tisdall2, Patrick McDaniel3, Borjan Gagoski4, Divya S Bolar2,5, Patricia Ellen Grant4, and Elfar Adalsteinsson1,3,6

1Harvard-MIT Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA, United States, 2Martinos Center for Biomedical Imaging, MGH/Harvard Medical School, Boston, MA, United States, 3Department of Electrical Engineering and Computer Science, Massachusetts Institute of Technology, Cambridge, MA, United States, 4Fetal-Neonatal Neuroimaging and Developmental Science Center, Boston Children’s Hospital, Boston, MA, United States, 5Department of Radiology, Massachusetts General Hospital, Boston, MA, United States, 6Institute for Medical Engineering and Science, Cambridge, MA, United States

Synopsis

When using the T2-relaxation under spin tagging (TRUST) technique on non-compliant subjects, motion has an unknown effect on estimations of cerebral oxygenation that are derived from an empirical mapping between T2 and blood oxygen saturation. Incorporating low resolution 3D-EPI volume navigators into the TRUST pulse sequence permits independent measurements of motion during scanning. We show that for static scans vNav modules have only small effects on resulting venous blood T2 estimates, that poor exponential goodness of fit is not a sufficient indicator of motion, and that T2 is biased upwards with increasing motion.

Introduction

Using T2-relaxation under spin tagging (TRUST)1–3 to measure cerebral oxygenation in neonates has shown that subject motion affects blood signal isolation and has unknown impact on venous oxygen saturation (SvO2) quantification. In TRUST, the venous blood signal in the superior sagittal sinus (SSS) is isolated using a spin tagging approach, an exponential fit is used to estimate T2 from the resulting signal, and an empirical calibration is used to map T2 to venous oxygen saturation. To quantify subject motion during TRUST scans, we incorporated volume navigators (vNav)4 into the TRUST sequence to retrospectively determine the movements that occurred during the scan. We show that for static scans vNav modules have only small effects on resulting venous blood T2 estimates, that poor exponential goodness of fit is not a sufficient indicator of motion, and that blood T2 is biased upwards with increasing motion.

Methods

vNav acquisition modules4 were inserted into the TRUST sequence (Figure 1). For offline registration not including the label shadow we used the methods of McDaniel, et al:5 volumes were co-registered and motion parameters measured using the FSL FLIRT tool (cost function=correlation ratio, DOF=6)6 and custom Matlab scripts. Translations were determined for a voxel centered on the SSS and motion score calculated.4 For this pilot study with compliant subjects, three adults (2 male, 1 female, mean age=21) were scanned with IRB approval on a Siemens Tim Trio scanner. The TRUST image was positioned 25 mm above the confluence of the sinuses perpendicular to the SSS with scan parameters: TE/TR=12/5000ms, T2 effective echo times (TEeff)=0,18,36,72,144ms, resolution=3.4x3.4x5mm, inversion time=1200ms, tagging width=100mm, tagging gap=25mm, 3 averages, total acquisition=2:30. The subject was then instructed to move or remain still for alternating TRUST+vNav scans. The three brightest voxels near the SSS were averaged to give a signal intensity (S(TEeff)) value for one TEeff. Fitting to S(TEeff)=S0exp(TEeff*C) was performed by taking ln(S(TEeff)) and then performing a linear least squares fit. T2,blood=1/(R1,blood-C), R1,blood=0.62 [s-1].1 Goodness of fit was evaluated based on the standard deviation of the residuals (SDR) of the fit.

Results

Simulations of the TRUST+vNav sequence using Bloch simulation and TRUST signal equations1 show that vNav modules cause changes in T2 smaller than same subject T2 variance and SDR changes were smaller than for typical in vivo fits. T2 estimates from TRUST and TRUST+vNav sequences demonstrate no significant difference in T2 values (Table 1). vNavs track head motion, with example motion trajectories for a quiescent and moving subject shown in Figure 2. Figure 3 shows maximum motion score during the scan plotted against SDR. Figure 4 shows the significant positive correlation between the difference of estimated T2 and mean baseline T2 per subject, and maximum motion score.

Discussion

vNavs have been well characterized and are suitable for resolving translations of less than 0.5mm.4 Due to the differences between control and label acquisitions in TRUST, a small (<0.5 mm translation at the SSS) jitter results from the registration between these states for still subjects. Figure 2 shows the registration across all label acquisitions, and future work will consider the motion during control and label states in parallel since the venous blood signal isolation is affected by either. Figure 2 suggests good motion tracking using the vNavs. Previous work established that the failed signal isolation resulting from movement between control and tag acquisitions partly manifests itself as poor goodness of exponential fit.1 Figure 3 suggests that though this is largely true, goodness of fit as assessed by SDR cannot be used to determine whether or not motion occurred. This is important both because of the upward bias in T2 estimates that results from motion (Figure 4) and the estimation error in T2 that grows larger with increased motion. We hypothesize that the larger T2 values with motion result from poor venous blood signal isolation, meaning that tissue compartments with higher intrinsic T2 values (grey matter and cerebral spinal fluid) are included in the assumed pure blood signal. Future work will use the motion parameters—measured independently from the T2-fitting process—to perform retrospective motion correction by rejecting or weighting S(TEeff) values before performing the fit. We will also explore the possibility that brain state changes contribute to the upward bias in T2 when a subject is instructed to move.

Conclusion

Motion causes an upward bias of venous blood T2 estimates in the TRUST technique. During scans with poor subject compliance, specifically during pediatric scans, independent motion monitoring, here performed with vNavs, may be necessary.

Acknowledgements

Mark Vangel, Department of Radiology, MGH, for his help with statistical methods.

This publication was made possible by NIBIB-NIH grants 5T32EB1680, R01EB017337, U01HD087211, and by NIH-NICHD grants 4R00HD074649-03, R21HD072505.

References

1. Lu, H.; Ge, Y. Quantitative Evaluation of Oxygenation in Venous Vessels Using T2-Relaxation-Under-Spin-Tagging MRI. Magnetic resonance in medicine?: official journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 2008, 60, 357–63.

2. Xu, F.; Ge, Y.; Lu, H. Noninvasive Quantification of Whole-Brain Cerebral Metabolic Rate of Oxygen (CMRO2) by MRI. Magnetic resonance in medicine?: official journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 2009, 62, 141–8.

3. Liu, P.; Huang, H.; Rollins, N.; Chalak, L. F.; Jeon, T.; Halovanic, C.; Lu, H. Quantitative Assessment of Global Cerebral Metabolic Rate of Oxygen (CMRO2 ) in Neonates Using MRI. NMR in biomedicine 2014.

4. Tisdall, M. D.; Hess, A. T.; Reuter, M.; Meintjes, E. M.; Fischl, B.; Kouwe, A. J. W. van der Volumetric Navigators for Prospective Motion Correction and Selective Reacquisition in Neuroanatomical MRI. Magnetic resonance in medicine?: official journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine 2012, 68, 389–99.

5. McDaniel, P.; Gagoski, B.; Tisdall, M. D.; Kouwe, A. J. W. van der; Grant, P. E.; Wald, L. L.; Adalsteinsson, E. Quantification of Fetal Motion Tracked with Volumetric Navigator MRI Acquisitions. In Proc. Intl. Soc. Mag. Reson.; 2015.

6. Jenkinson, M.; Bannister, P.; Brady, M.; Smith, S. Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images. NeuroImage 2002, 17, 825–841.

Figures

Figure 1: TRUST+vNav pulse sequence, with example midsagittal vNav image showing labeling and pre-saturation (arrow) shadows.

Figure 2: Label image motion trajectories for a quiescent subject and subject asked to make small intermittent movements.

Figure 3: Max motion score versus goodness of fit assessed by the standard deviation of the natural log of the residual signal intensities (SDR) for both scans with and without motion.

Figure 4: Difference between T2 and mean T2 without motion for each subject, versus maximum motion score during the 2:30 TRUST scan. (a) for all scans, N=28, R2=0.37, p=0.001. (b) for scans where subject was asked to move voluntarily, N=12, R2=0.30, p=0.064.

Table 1: Descriptive statistics for the T2 estimates from each scan. No significant difference between TRUST and TRUST+vNAV sequences.



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