Novel diffusion tractography methodology using Kalman filter prediction to improve preoperative benefit-risk analysis in pediatric epilepsy surgery

OBJECTIVE In this study the authors investigated the clinical reliability of diffusion weighted imaging maximum a posteriori probability (DWI-MAP) analysis with Kalman filter prediction in pediatric epilepsy surgery. This approach can yield a suggested resection margin as a dynamic variable based on preoperative DWI-MAP pathways. The authors sought to determine how well the suggested margin would have maximized occurrence of postoperative seizure freedom (benefit) and minimized occurrence of postoperative neurological deficits (risk). METHODS The study included 77 pediatric patients with drug-resistant focal epilepsy (age 10.0 +/- 4.9 years) who underwent resection of their presumed epileptogenic zone. In preoperative DWI tractography from the resected hemisphere, 9 axonal pathways, C-i=(1-9), were identified using DWI-MAP as follows: C1-3 supporting face, hand, and leg motor areas; C-4 connecting Broca's and Wernicke's areas; C5-8 connecting Broca's, Wernicke's, parietal, and premotor areas; and C-9 connecting the occipital lobe and lateral geniculate nucleus. For each C-i, the resection margin, d(i), was measured by the minimal Euclidean distance between the voxels of C-i and the resection boundary determined by spatially coregistered postoperative MRI. If C-i was resected, d(i) was assumed to be negative (calculated as -1 x average Euclidean distance between every voxel inside the resected C-i volume, r(i)). Kalman filter prediction was then used to estimate an optimal resection margin, d(i)*, to balance benefit and risk by approximating the relationship between d(i) and r(i). Finally, the authors defined the preservation zone of C-i that can balance the probability of benefit and risk by expanding the cortical area of C-i up to d(i)* on the 3D cortical surface. RESULTS In the whole group (n = 77), nonresection of the preoperative preservation zone (i.e., actual resection margin d(i) greater than the Kalman filter-defined d(i)*) accurately predicted the absence of postoperative motor (d(1-3)*: 0.93 at seizure-free probability of 0.80), language (d(4-8)*: 0.91 at seizure-free probability of 0.81), and visual deficits (d(9)*: 0.90 at seizure-free probability of 0.75), suggesting that the preservation of preoperative C-i within d(i)*supports a balance between postoperative functional deficit and seizure freedom. The subsequent subgroup analyses found that preservation of preoperative C-i (=1-4,9) within d(i =1-4,9)* may provide accurate deficit predictions independent of age and seizure frequency, suggesting that the DWI-based surgical margin can be effective for surgical planning even in young children and across a range of epilepsy severity. CONCLUSIONS Integrating DWI-MAP analysis with Kalman filter prediction may help guide epilepsy surgery by visualizing the margins of the eloquent white matter pathways to be preserved.