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Premature white matter aging in patients with right mesial temporal lobe epilepsy: A machine learning approach based on diffusion MRI data.

ABSTRACT: Brain age prediction based on machine learning has been applied to various neurological diseases to discover its clinical values. By this innovative approach, it has been reported that the patients with refractory epilepsy had premature brain aging. Of refractory epilepsy, right and left subtypes of mesial temporal lobe epilepsy (MTLE) are the most common forms and exhibit distinct patterns in white matter alterations. So far, it is unclear whether these two subtypes of MTLE would have difference in white matter aging due to distinct white matter alterations. To address this issue, a machine learning based brain age model using diffusion MRI data was established to investigate biological age of white matter tracts. All diffusion MRI datasets were obtained from the same 3-Tesla MRI scanner. To build the brain age prediction model, diffusion MRI datasets of 300 healthy participants were processed to extract age-relevant diffusion indices from 76 major white matter tracts. The extracted diffusion indices underwent Gaussian process regression to build the prediction model for white matter brain age. The model was validated in an independent testing set (N = 40) to ensure no overfitting of the model. The model was then applied to patients with right and left MTLE and matched controls (right MTLE: N = 17, left MTLE: N = 18, controls: N = 37), and predicted age difference (PAD) was obtained by calculating the difference between each individual's predicted brain age and chronological age. The higher PAD score indicated older brain age. The results showed that right MTLE exhibited older predicted brain age than the other two groups (PAD of right MTLE = 10.9 years [p < 0.05 against left MTLE; p < 0.001 against control]; PAD of left MTLE = 2.2 years [p > 0.1 against control]; PAD of controls = 0.82 years). Patients with right and left MTLE showed strong correlations of the PAD scores with age of onset and duration of illness, but both groups showed opposite directions of correlations. In right MTLE, positive correlation of PAD with seizure frequency was found, and the right uncinate fasciculus was the most attributable tract to the increase in PAD. In conclusion, the present study found that patients with right MTLE exhibited premature white matter brain aging and their PAD scores were correlated with seizure frequency. Therefore, PAD is a potentially useful indicator of white matter impairment and disease severity in patients with right MTLE.

SUBMITTER: Chen CL

PROVIDER: S-EPMC6978225 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:ObjectivesTo explore the dynamic changes of white matters following anterior temporal lobectomy (ATL) in mesial temporal lobe epilepsy (MTLE) patients who achieved seizure-free at two-year follow-up.MethodsDiffusion tensor imaging (DTI) was obtained in ten MTLE patients at five serial time points: before surgery, three months, six months, 12 months and 24 months after surgery, as well as in 11 age- and sex-matched healthy controls at one time point. Regions with significant postoperative fractional anisotropy (FA) changes and their dynamic changes were confirmed by comparing all preoperative and postoperative data using Tract-Based Spatial Statistics (TBSS).ResultsAfter successful ATL, significant FA changes were found in widespread ipsilateral and contralateral white matter regions (P <.05, FWE correction). Ipsilateral external capsule, cingulum, superior corona radiate, body of corpus callosum, inferior longitudinal fasciculus, optic radiation and contralateral inferior cerebellar peduncle, inferior longitudinal fasciculus showed significant FA decrease at three months after surgery, without further changes. Ipsilateral superior cerebellar peduncle and contralateral corpus callosum, anterior corona radiate, external capsule, optic radiation showed significant FA decrease at three months follow up but increase later. Ipsilateral cerebral peduncle and contralateral middle cerebellar peduncle showed significant FA decrease at three months follow up, with further decrease after that. While ipsilateral posterior limb of internal capsule, retrolenticular part of internal capsule and contralateral posterior corona radiate showed significant FA increase after surgery.ConclusionsFA changes after successful ATL presented as four distinct patterns, reflecting different structural adaptions following epilepsy surgery. Some FA increases indicated the reversibility of preoperative diffusion abnormalities and the possibility of structural reorganization, especially in the contralateral hemisphere.

Project description:Background: We hypothesized that right and left temporal lobe epilepsy (RTLE and LTLE, respectively) have distinctive spatial patterns of white matter (WM) changes that can be differentiated and interpreted with the use of multiple diffusion parameters. We compared the global microstructure of fiber bundles with regard to WM alterations in both RTLE and LTLE, addressing some of the methodological issues of previous studies. Methods: Diffusion tensor imaging data from 17 patients with RTLE (age: 40.7 ± 10.4), 15 patients with LTLE (age: 37.3 ± 10.4), and 15 controls (age: 34.8 ± 11.2) were used in the study. WM integrity was quantified by fractional anisotropy (FA), mean diffusivity (MD), longitudinal diffusivity (LD), and radial diffusivity (RD). The diffusion parameters were compared between the groups in tracts representing the core of the fiber bundles. The volumes of hippocampi and amygdala were subsequently compared across the groups, while the data were adjusted for the effect of hippocampal sclerosis. Results: Significantly reduced FA and increased MD, LD, and RD were found bilaterally over widespread brain regions in RTLE. An increase in MD and RD values was observed in widespread WM fiber bundles ipsilaterally in LTLE, largely overlapping with regions where FA was lower, while no increase in LD was observed. We also found a difference between the LTLE and RTLE groups for the right hippocampal volume (with and without adjustment for HS), whereas no significant volume differences were found between patients and controls. Conclusions: It appears that patients with RTLE exhibit a more widespread pattern of WM alterations that extend far beyond the temporal lobe in both ipsilateral and contralateral hemisphere; furthermore, these changes seem to reflect more severe damage related to chronic degeneration. Conversely, more restrained changes in the LTLE may imply a pattern of less severe axonal damage, more restricted to ipsilateral hemisphere. Comprehensive finding of more prominent hippocampal atrophy in the RTLE raises an interesting issue of seizure-induced implications on gray matter and WM microstructure that may not necessarily mean a straightforward causal relationship. Further correlations of diffusion-derived metrics with neuropsychological and functional imaging measures may provide complementary information on underlying WM abnormalities with regard to functional hemispheric specialization.

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Premature white matter aging in patients with right mesial temporal lobe epilepsy: A machine learning approach based on diffusion MRI data.

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