Microstructural Characterization of the Pia-Arachnoid Complex Using Optical Coherence Tomography

Traumatic brain injury (TBI) is one of the leading causes of death and disability in the world, and is often identified by the presence of subdural and/or subarachnoid hemorrhages that develop from ruptured cortical vessels during brain-skull displacement. The pia-arachnoid complex (PAC), also known as the leptomeninges, is the major mechanical connection between the brain and skull, and influences cortical vessel deformation and rupture following brain trauma. This complex consists of cerebrospinal fluid, arachnoid trabeculae, and subarachnoid vasculature sandwiched between the arachnoid and pia mater membranes. Remarkably, studies of the tissues in the PAC are largely qualitative and do not provide numerical metrics of population density and variability of the arachnoid trabeculae and subarachnoid vasculature. In this study, microstructural imaging was performed on the PAC to numerically quantify these metrics. Five porcine brains were perfusion-fixed and imaged in situ using optical coherence tomography with micrometer resolution. Image processing was performed to estimate the volume fraction (VF) of the arachnoid trabeculae and subarachnoid vasculature in 12 regions of the brain. High regional variability was found within each brain, with individual brains exhibiting up to a 38.4 percentage-point range in VF. Regions with high VF were often next to regions with low VF. This suggests that some areas of the brain may be mechanically weaker, increasing their susceptibility to hemorrhage during TBI events. This study provides the first quantifiable data of arachnoid trabeculae and subarachnoid vasculature distribution within the PAC and will be valuable to understanding brain biomechanics during head trauma.

[1]  Mathias Fink,et al.  From supersonic shear wave imaging to full-field optical coherence shear wave elastography , 2013, Journal of biomedical optics.

[2]  David A Boas,et al.  Rapid volumetric angiography of cortical microvasculature with optical coherence tomography. , 2010, Optics letters.

[3]  Jeffrey A. Golden,et al.  Maturation-dependent response of the piglet brain to scaled cortical impact. , 2000, Journal of neurosurgery.

[4]  Joseph T. Gwin,et al.  HEAD IMPACT SEVERITY MEASURES FOR EVALUATING MILD TRAUMATIC BRAIN INJURY RISK EXPOSURE , 2008, Neurosurgery.

[5]  S. Margulies,et al.  Physiological and pathological responses to head rotations in toddler piglets. , 2010, Journal of neurotrauma.

[6]  M. King,et al.  Measurement of viscoelastic properties in multiple anatomical regions of acute rat brain tissue slices. , 2014, Journal of the mechanical behavior of biomedical materials.

[7]  J. Fujimoto,et al.  Optical Coherence Tomography , 1991, LEOS '92 Conference Proceedings.

[8]  J. Dobbing,et al.  Comparative aspects of the brain growth spurt. , 1979, Early human development.

[9]  Guillermo Aguilar,et al.  Transparent nanocrystalline yttria-stabilized-zirconia calvarium prosthesis. , 2013, Nanomedicine : nanotechnology, biology, and medicine.

[10]  Angelika Unterhuber,et al.  Imaging ex vivo healthy and pathological human brain tissue with ultra-high-resolution optical coherence tomography. , 2005, Journal of biomedical optics.

[11]  A. Cowey,et al.  Imaging ex vivo and in vitro brain morphology in animal models with ultrahigh resolution optical coherence tomography. , 2004, Journal of biomedical optics.

[12]  J M Schmitt,et al.  Subsurface imaging of living skin with optical coherence microscopy. , 1995, Dermatology.

[13]  R O Weller,et al.  The Cranial Arachnoid and Pia Mater in Man: Anatomical and Ultrastructural Observations , 1988, Neuropathology and applied neurobiology.

[14]  David A Boas,et al.  Optical coherence tomography for the quantitative study of cerebrovascular physiology , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[15]  B. Devaux,et al.  Imaging of non-tumorous and tumorous human brain tissues with full-field optical coherence tomography☆ , 2013, NeuroImage: Clinical.

[16]  A. Rezai,et al.  A feasibility study of optical coherence tomography for guiding deep brain probes , 2006, Journal of Neuroscience Methods.

[17]  A L Rhoton,et al.  Microsurgical anatomy of the superficial veins of the cerebrum. , 1985, Neurosurgery.

[18]  Christian M. Oh,et al.  Thinned-skull cortical window technique for in vivo optical coherence tomography imaging. , 2012, Journal of visualized experiments : JoVE.

[19]  J. G. Fujimoto,et al.  Assessing atherosclerotic plaque morphology: comparison of optical coherence tomography and high frequency intravascular ultrasound. , 1997, Heart.

[20]  Stefan M. Duma,et al.  Brain Injury Prediction: Assessing the Combined Probability of Concussion Using Linear and Rotational Head Acceleration , 2013, Annals of Biomedical Engineering.

[21]  R. Weller Microscopic morphology and histology of the human meninges. , 2005, Morphologie : bulletin de l'Association des anatomistes.

[22]  G. Ripandelli,et al.  Optical coherence tomography. , 1998, Seminars in ophthalmology.

[23]  C Ross Ethier,et al.  Shadow removal and contrast enhancement in optical coherence tomography images of the human optic nerve head. , 2011, Investigative ophthalmology & visual science.

[24]  Susan S. Margulies,et al.  Finite element model predictions of intracranial hemorrhage from non-impact, rapid head rotations in the piglet , 2012, International Journal of Developmental Neuroscience.

[25]  T. Flynn Developmental changes of myelin-related lipids in brain of miniature swine , 1984, Neurochemical Research.

[26]  J. C. Soares,et al.  Mesoscopy and Scanning Electron Microscopy of the Trabecular Projections in the Superior Sagittal Sinus , 2003, Cells Tissues Organs.

[27]  R. Ichord,et al.  Repeated traumatic brain injury affects composite cognitive function in piglets. , 2009, Journal of neurotrauma.

[28]  R. Weller,et al.  The fine anatomy of the human spinal meninges. A light and scanning electron microscopy study. , 1988, Journal of neurosurgery.

[29]  J. Golden,et al.  Magnetic resonance imaging studies of age-dependent responses to scaled focal brain injury in the piglet. , 2003, Journal of neurosurgery.

[30]  J. Izatt,et al.  Optical coherence microscopy in gastrointestinal tissues , 1996, Summaries of papers presented at the Conference on Lasers and Electro-Optics.

[31]  C. Kurth,et al.  Different cerebral hemodynamic responses following fluid percussion brain injury in the newborn and juvenile pig. , 1994, Journal of neurotrauma.

[32]  Junfeng Zhu,et al.  Reconstructing micrometer-scale fiber pathways in the brain: Multi-contrast optical coherence tomography based tractography , 2011, NeuroImage.

[33]  Joseph J Crisco,et al.  Spectrum of acute clinical characteristics of diagnosed concussions in college athletes wearing instrumented helmets: clinical article. , 2012, Journal of neurosurgery.

[34]  J Flammer,et al.  Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations , 2003, The British journal of ophthalmology.

[35]  Steven Rowson,et al.  Linear and angular head acceleration measurements in collegiate football. , 2009, Journal of biomechanical engineering.

[36]  S. Boppart Optical coherence tomography: technology and applications for neuroimaging. , 2003, Psychophysiology.

[37]  A Schweikard,et al.  Automatic scanning of large tissue areas in neurosurgery using optical coherence tomography , 2012, The international journal of medical robotics + computer assisted surgery : MRCAS.

[38]  J. Dobbing,et al.  Prenatal and postnatal growth and development of the central nervous system of the pig , 1967, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[39]  A. Duhaime,et al.  Experimental acute subdural hematoma in infant piglets. , 1996, Pediatric neurosurgery.