Brain parenchyma deformation and strain in patients with spontaneous intracranial hypotension

Abstract Background Spontaneous intracranial hypotension (SIH) is mainly associated with orthostatic headache but can also cause cognitive impairment, with symptoms mimicking behavioral-type frontotemporal dementia in severe cases. SIH is caused by a spinal cerebrospinal fluid (CSF) leak and can lead to brain sagging. The specific brain regions affected by this motion, their deformation, and the magnitude of the associated mechanical strain have not been quantitatively characterized. We investigated whether brain MRI in patients with SIH shows quantifiable strain, expansion, and compression of brain structures by comparing images before and after surgical occlusion of a spinal leak. Methods We performed a retrospective analysis of 96 patients with SIH who underwent surgical closure of a spinal CSF leak. We performed AI-assisted diffeomorphic registration of pre- and postoperative MRI. From the resulting displacement maps, we calculated the Jacobian determinant as an indicator of expansion and contraction, and the von Mises equivalent deviatoric strain as an indicator of distortion and shearing in brain regions. Results were compared with 61 healthy adults scanned twice over a comparable interval, and correlated with perioperative headache, quality-of-life and cognitive scores. Results Ventricles and transverse sinuses showed relevant perioperative expansion and contraction, respectively. Beyond these expected volumetric changes, significant deviatoric strain was observed in temporomesial and frontal structures, including the temporal poles (right/ left: 8.6/ 8.7%), hippocampus (9.0/ 9.8%), and basal forebrain (9.9/ 9.8%) ( p < 0.001 for all), despite only moderate volumetric change in these regions. Deformation substantially exceeded that of healthy controls. Whole-brain strain showed a modest positive association with perioperative improvement in headache burden, whereas analyses of cognitive outcome were underpowered. Conclusion SIH is associated with quantifiable regional brain deformation resulting in region-specific mechanical strain. Elevated strain in fronto-limbic and temporomesial regions, implicated in behavioral and cognitive regulation, suggests a network-level mechanical effect that may contribute to the clinical presentation observed in severe SIH.