Regional mechanical and biochemical properties of the porcine cortical meninges

Abstract

The meninges are pivotal in protecting the brain against traumatic brain injury (TBI), an ongoing issue in most mainstream sports. Improved understanding of TBI biomechanics and pathophysiology is desirable to improve preventative measures, such as protective helmets, and advance our TBI diagnostic/prognostic capabilities. This study mechanically characterised the porcine meninges by performing uniaxial tensile testing on the dura mater (DM) tissue adjacent to the frontal, parietal, temporal, and occipital lobes of the cerebellum and superior sagittal sinus region of the DM. Mechanical characterisation revealed a significantly higher elastic modulus for the superior sagittal sinus region when compared to other regions in the DM. The superior sagittal sinus and parietal regions of the DM also displayed local mechanical anisotropy. Further, fatigue was noted in the DM following ten preconditioning cycles, which could have important implications in the context of repetitive TBI. To further understand differences in regional mechanical properties, regional variations in protein content (collagen I, collagen III, fibronectin and elastin) were examined by immunoblot analysis. The superior sagittal sinus was found to have significantly higher collagen I, elastin, and fibronectin content. The frontal region was also identified to have significantly higher collagen I and fibronectin content while the temporal region had increased elastin and fibronectin content. Regional differences in the mechanical and biochemical properties along with regional tissue thickness differences within the DM reveal that the tissue is a non-homogeneous structure. In particular, the potentially influential role of the superior sagittal sinus in TBI biomechanics warrants further investigation. STATEMENT OF SIGNIFICANCE: This study addresses the lack of regional mechanical analysis of the cortical meninges, particularly the dura mater (DM), with accompanying biochemical analysis. To mechanically characterise the stiffness of the DM by region, uniaxial tensile testing was carried out on the DM tissue adjacent to the frontal, parietal, temporal and occipital lobes along with the DM tissue associated with the superior sagittal sinus. To the best of the authors' knowledge, the work presented here identifies, for the first time, the heterogeneous nature of the DM's mechanical stiffness by region. In particular, this study identifies the significant difference in the stiffness of the DM tissue associated with the superior sagittal sinus when compared to the other DM regions. Constitutive modelling was carried out on the regional mechanical testing data for implementation in Finite Element models with improved biofidelity. This work also presents the first biochemical analysis of the collagen I and III, elastin, and fibronectin content within DM tissue by region, providing useful insights into the accompanying macro-scale biomechanical data.

Mechanical Properties of the Cranial Meninges: A Systematic Review

“…Thus, it is not surprising that significant inter and intra-subject variability has been observed for the dura mater. 37,69 The large variability of dural mechanics is also evident in the relatively large standard deviations of the data presented in Fig. 4 (A).…”

“…37 Interestingly, the authors observed significant regional differences in collagen I content, the main structural element of the extracellular matrix, 35 and regions with high collagen I content generally had higher mechanical stiffness than other regions. 37 Numerous investigations have found that collagen fibres within the dura mater show signs of local alignment, but this alignment occurs over short spatial distances and thus it has generally been accepted that the dura is structurally isotropic in bulk. 27,[38][39][40]…”

“…Numerous investigations on the anisotropy of bulk dura mater tissue have confirmed that the tissue exhibits bulk isotropic mechanical behaviour. 37,38,69…”

Mechanical Characterization and Modeling of the Porcine Cerebral Meninges

“…Currently, not all FE head models include a description of the meninges: of those that do (Horgan and Gilchrist, 2003 ; King et al, 2006 ; Kleiven, 2006 ; Chafi et al, 2009 ; Li et al, 2011 ), they often include a simplified linear response based on uniaxial tests performed by Galford and McElhaney ( 1970 ). There is a relative dearth of primary data on the mechanical properties of the meninges, and with the exception of Walsh et al ( 2018 ); De Kegal et al ( 2017 ) and MacManus et al ( 2017a ), all other studies have been conducted over 30 years ago (Galford and McElhaney, 1970 ; Van Noort et al, 1981a ; McGarvey et al, 1984 ; Bylski et al, 1986 ). Of these previous investigations, there are large variations in results which could be attributed to the nature of the testing protocol, the source of the meninges samples, storage of samples and insufficient sample sizes.…”

Assessment of head injury risk caused by impact using finite element models

“…In fact, the upper limit of this dural fold is the superior sagittal sinus (SSS), whereas the lower limit is a free edge [85]. A recent study by Walsh et al (2018) [86] of uniaxial testing on porcine dura mater samples found a significantly greater stiffness of the dural layer in the SSS region (increase of almost a 100% with respect to the frontal, parietal, occipital and temporal regions). This finding is relevant for the development of head models as it is likely to constrain the deformation and displacement of the SSS-falx complex during brain movement.…”