Quantitative analysis along the pyramidal tract by length-normalized parameterization based on diffusion tensor tractography: Application to patients with relapsing neuromyelitis optica
Introduction
Diffusion tensor tractography is a non-invasive imaging method with the potential to visualize in vivo brain white matter fiber tracts such as the corpus callosum, cingulum and pyramidal tract (PYT), in three-dimensional (3D) space. The streamline method, a popular tractography algorithm, exploits each voxel's principal diffusion direction to follow the trajectories of a fiber tract in 3D space from voxel to voxel (Basser et al., 2000, Conturo et al., 1999, Mori et al., 1999). Tractography is capable of visualizing the shape, location, and topology of a fiber tract and has been applied in a wide range of clinical and scientific studies (Bammer et al., 2003, Berman et al., 2004, Hoon et al., 2002, Lee et al., 2005, Nguyen et al., 2005, Witwer et al., 2002, Zhang et al., 2004).
Compared with tract visualization, tract-based quantitative measurements can provide more information about microstructural changes in brain tissue. Some authors considered a fiber tract as a 3D region of interest (ROI) and then analyzed its diffusion indices (Berman et al., 2005, Glenn et al., 2003, Lin et al., 2005, Pagani et al., 2005, Partridge et al., 2005). This method provides global information for the tract, but it fails to show the regional information along the fiber tract. Thus, Fillard et al. (2003) developed a method for quantitative measurements along fiber tracts. However, because of the lack of anatomical correspondence across subjects, the reliability of this method is weakened during population analysis.
Therefore, in this study, we introduced a length-normalized parameterization method to establish anatomical correspondence of white matter fiber tracts and applied this method to investigate the presence of abnormal diffusion along the PYT between the lowest slice of the cerebral peduncle and the uppermost slice of the lateral ventricle in relapsing neuromyelitis optica (RNMO) patients without visible brain lesions. For this purpose, we followed several steps. First, to establish the anatomical correspondence of PYT across subjects, we selected the lowest slice of the cerebral peduncle as the origin and the uppermost slice of the lateral ventricle as the terminus. Then the PYT between these two anatomical landmarks for each subject was reconstructed on the basis of diffusion tensor tractography. Finally, the part of the PYT was parameterized by normalizing its length and dividing equally the normalized length into a certain number of segments. In this way, the comparability of each segment across subjects along the PYT was established. Tract-specific diffusion indices, including directionally averaged diffusivity (Dav), fractional anisotropy (FA), primary diffusivity (λ1), and transverse diffusivity (λ23), were obtained from each segment. Thus, the distribution maps of these diffusion indices along the PYT were obtained. And then the tract-based statistical analysis was carried out.
Section snippets
Subjects
In this study, sixteen patients (15 females and 1 male) with a relapsing course satisfied the proposed diagnostic criteria of NMO (Wingerchuk et al., 1999). They satisfied all absolute criteria and at least one major supportive criterion or two minor supportive criteria. All these RNMO patients had normal brain MRI scans. Their mean age was 35.4 ± 11.8 years (range, 19.0–55.0 years), and the mean duration of the disease was 4.7 ± 2.4 years (range, 1.0–8.0 years). Their mean Expanded Disability
Results
Friedman test, with the group (patient versus control) as an inter-subject factor and the side (left versus right) as an intrasubject factor, was carried out for each segment. There were no significant differences by side effect or interaction (group-by-side) effect for all segments and for all these four diffusion indices. Therefore, the values derived from the left and right PYT were averaged to obtain the FA, Dav, λ1, and λ23 of the corresponding segment for each subject. Fig. 2 shows the
Discussion
In this study, a length-normalized parameterization method was proposed to establish anatomical correspondence of white matter fiber tracts and was applied to investigate the presence of abnormal diffusion along the PYT of RNMO patients without visible brain lesions. The statistical results indicated that RNMO patients had abnormal diffusion along the PYT, especially in the lower part of it. Our results were obtained without correction for multiple comparisons. With strict Bonferroni
Conclusion
In conclusion, a length-normalized parameterization method was proposed to establish anatomical correspondence for white matter fiber tracts. The main merit of our method is to provide for comparability across subjects along the PYT on the basis of diffusion tensor tractography and to make quantitative analysis along the fiber tract possible. Our method has been applied to investigate abnormal diffusion along the PYT of RNMO patients without visible brain lesions. The proposed method may also
Acknowledgments
The authors are highly grateful to the anonymous reviewers for their significant and constructive remarks and suggestions, which are greatly helpful in improving the paper. The authors also thank Drs. Edmund F. and Rhoda E. Perozzi of Beijing University of Technology for extensive English language assistance. This work was partially supported by the Natural Science Foundation of China, Grant Nos.30570509, 30425004, 60121302 and 30470519, and the National Key Basic Research and Development
References (38)
- et al.
In vivo MR tractography using diffusion imaging
Eur. J. Radiol.
(2003) - et al.
Microstructural and physiological features of tissues elucidated by quantitative diffusion tensor MRI
J. Magn. Reson., Ser. B
(1996) - et al.
Estimation of the effective self-diffusion tensor from the NMR spin echo
J. Magn. Reson., Ser. B
(1994) - et al.
Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants
NeuroImage
(2005) - et al.
Diffusion tensor MRI as a diagnostic tool of upper motor neuron involvement in amyotrophic lateral sclerosis
J. Neurol. Sci.
(2004) - et al.
Fiber tracking by diffusion tensor imaging in corticospinal tract stroke: topographical correlation with clinical symptoms
NeuroImage
(2005) - et al.
‘Importance sampling’ in MS: use of diffusion tensor tractography to quantify pathology related to specific impairment
J. Neurol. Sci.
(2005) - et al.
A method for obtaining tract-specific diffusion tensor MRI measurements in the presence of disease: application to patients with clinically isolated syndromes suggestive of multiple sclerosis
NeuroImage
(2005) - et al.
Parametric and non-parametric statistical analysis of DT-MRI data
J. Magn. Reson.
(2003) - et al.
Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture
NeuroImage
(2001)
Diffusion tensor imaging and axonal tracking in the human brainstem
NeuroImage
Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke
NeuroImage
Visualizing and characterizing white matter fiber structure and architecture in the human pyramidal tract using diffusion tensor MRI
Magn. Reson. Imaging
Anisotropy of water diffusion in corona radiate and cerebral peduncle in patients with hemiparesis
NeuroImage
Dealing with uncertainty in diffusion tensor MR data
Isr. J. Chem.
In vivo fiber tractography using DT-MRI data
Magn. Reson. Med.
Changes in water diffusion due to Wallerian degeneration in peripheral nerve
Magn. Reson. Med.
Diffusion-tensor imaging guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas
J. Neurosurg.
Tracking neuronal fiber pathways in the living human brain
Proc. Natl. Acad. Sci.
Cited by (40)
Tract-Based Spatial Statistics and Other Approaches for Cross-Subject Comparison of Local Diffusion MRI Parameters
2015, Brain Mapping: An Encyclopedic ReferenceCross-Subject Comparison of Local Diffusion MRI Parameters
2013, Diffusion MRI: From Quantitative Measurement to In vivo Neuroanatomy: Second EditionAutomated approaches for analysis of multimodal MRI acquisitions in a study of cognitive aging
2012, Computer Methods and Programs in BiomedicineCitation Excerpt :However, this approach is not sensitive to local changes of FA along specific fiber tracts. Therefore, methods have been introduced that can provide estimated FA variation along white matter fiber tracts [28–33], giving additional information to global estimates. Gong et al. [30] used a scale-invariant polar parametrization of the arc to study the circular-like shaped cingulum.
Signal-to-noise ratio of diffusion weighted magnetic resonance imaging: Estimation methods and in vivo application to spinal cord
2012, Biomedical Signal Processing and ControlA Monte Carlo simulation of image misalignment effects in diffusion tensor imaging
2010, Magnetic Resonance ImagingCitation Excerpt :Furthermore, a recent MR spectroscopy study suggested that axonal damage of normal-appearing brain parenchyma is associated with the earliest stages of MS [39]. Significant mean diffusivity increase [38,40,41] and mean FA decrease by 0.03 [40,41] in the pyramidal tracts of the MS patients were also reported. With respect to the present data, the mean FAFACT changed comparably with respect to the motion-corrected reference at RMSd=2.75 mm (Fig. 3), respectively.
- 1
These authors contributed equally to this work.