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Subarachnoid Trabeculae: a Comprehensive Review of Their Embryology, Histology, Morphology, and Surgical Significance Martin M

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Subarachnoid Trabeculae: a Comprehensive Review of Their Embryology, Histology, Morphology, and Surgical Significance Martin M Literature Review Subarachnoid Trabeculae: A Comprehensive Review of Their Embryology, Histology, Morphology, and Surgical Significance Martin M. Mortazavi1,2, Syed A. Quadri1,2, Muhammad A. Khan1,2, Aaron Gustin3, Sajid S. Suriya1,2, Tania Hassanzadeh4, Kian M. Fahimdanesh5, Farzad H. Adl1,2, Salman A. Fard1,2, M. Asif Taqi1,2, Ian Armstrong1,2, Bryn A. Martin1,6, R. Shane Tubbs1,7 Key words - INTRODUCTION: Brain is suspended in cerebrospinal fluid (CSF)-filled sub- - Arachnoid matter arachnoid space by subarachnoid trabeculae (SAT), which are collagen- - Liliequist membrane - Microsurgical procedures reinforced columns stretching between the arachnoid and pia maters. Much - Subarachnoid trabeculae neuroanatomic research has been focused on the subarachnoid cisterns and - Subarachnoid trabecular membrane arachnoid matter but reported data on the SAT are limited. This study provides a - Trabecular cisterns comprehensive review of subarachnoid trabeculae, including their embryology, Abbreviations and Acronyms histology, morphologic variations, and surgical significance. CSDH: Chronic subdural hematoma - CSF: Cerebrospinal fluid METHODS: A literature search was conducted with no date restrictions in DBC: Dural border cell PubMed, Medline, EMBASE, Wiley Online Library, Cochrane, and Research Gate. DL: Diencephalic leaf Terms for the search included but were not limited to subarachnoid trabeculae, GAG: Glycosaminoglycan subarachnoid trabecular membrane, arachnoid mater, subarachnoid trabeculae LM: Liliequist membrane ML: Mesencephalic leaf embryology, subarachnoid trabeculae histology, and morphology. Articles with a PAC: Pia-arachnoid complex high likelihood of bias, any study published in nonpopular journals (not indexed PPAS: Potential pia-arachnoid space in PubMed or MEDLINE), and studies with conflicting data were excluded. SAH: Subarachnoid hemorrhage SAS: Subarachnoid space - RESULTS: A total of 1113 articles were retrieved. Of these, 110 articles SAT: Subarachnoid trabeculae including 19 book chapters, 58 original articles, 31 review articles, and 2 case SEM: Scanning electron microscopy TEM: Transmission electron microscopy reports met our inclusion criteria. - From the 1National Skull Base Center, Thousand Oaks, CONCLUSIONS: SAT provide mechanical support to neurovascular structures California; 2California Institute of Neuroscience, Thousand through cell-to-cell interconnections and specific junctions between the pia and Oaks, California; 3Advocate BroMenn Medical Center, arachnoid maters. They vary widely in appearance and configuration among Normal, Illinois; 4University of Arizona College of Medicine, Tucson, Arizona; 5University of California Irvine Medical different parts of the brain. The complex network of SAT is inhomogeneous and Center, Irvine, California; 6University of Idaho, Moscow, mainly located in the vicinity of blood vessels. Microsurgical procedures should Idaho; and 7Seattle Science Foundation, Seattle, be performed with great care, and sharp rather than blunt trabecular dissection Washington, USA is recommended because of the close relationship to neurovascular structures. To whom correspondence should be addressed: Martin M. Mortazavi, M.D. The significance of SAT for cerebrospinal fluid flow and hydrocephalus is to be [E-mail: [email protected]] determined. Supplementary digital content available online. Citation: World Neurosurg. (2018) 111:279-290. https://doi.org/10.1016/j.wneu.2017.12.041 The current name of arachnoid mater is delicate neural tissue of the brain is Journal homepage: www.WORLDNEUROSURGERY.org attributed to Frederick Ruysch and his suspended within the CSF by buoyancy, in Available online: www.sciencedirect.com description of a spiderlike morphology in accordance with the Archimedes principle, 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All 1699.9 It is a delicate avascular layer in and also mechanically stabilized by the SAT rights reserved. direct contact with the dura and separated within the pia-arachnoid complex (PAC).14 from the pia mater by the cerebrospinal SAT constrain relative movement between INTRODUCTION fluid (CSF)-filled subarachnoid space, the skull and the brain as proposed in the 15 In the third century B.C., Herophilus, a showing distinctive histology and shaken baby syndrome hypothesis. These Greek physician and the father of anatomy, pathology.1,10 SAT, also referred to as arachnoid first described the brain as being enclosed During the late 1960s, Anderson and trabeculae, subarachnoid space (SAS) within the arachnoid membrane.1 In the Hayreh along with others described trabeculae, or leptomeningeal trabeculae, seventeenth century, Gerardus Blasius and subarachnoid trabeculae (SAT), which are can be seen with light microscopes but are Andreas Ottomar Goelicke referred to the sheets or columns of collagen-reinforced too thin to be detected by ultrasonography arachnoid membrane as “tertia cerebri material stretching between the arachnoid or clinical magnetic resonance imaging.16 meninge” or the third cerebral meninge.2-8 and pia membranes11-13 (Figure 1). The Nevertheless, high-resolution magnetic WORLD NEUROSURGERY 111: 279-290, MARCH 2018 www.WORLDNEUROSURGERY.org 279 LITERATURE REVIEW MARTIN M. MORTAZAVI ET AL. SUBARACHNOID TRABECULAE ANATOMY AND SURGICAL SIGNIFICANCE the embryonic epithelium (ectoderm) and the developing neuroepithelium of the telencephalon.16,19,21 At this stage, there are no arachnoid or pia membranes in the potential pia-arachnoid space (PPAS). This formless layer is composed of a gel-filled mesenchymal network as ground substance and acts as a space-holding layer for the future pia-arachnoid structures (Figure 2). The space-holding mesenchymal layer is made up of widely spaced, stellate mesen- chymal cells linked to each other through Figure 1. Organization of subarachnoid trabeculae in the subarachnoid space between the pia mater long extended interconnecting cytoplasmic and arachnoid mater. processes called pseudopodia.16,19,21 The extensive extracellular space is filled with glycosaminoglycan (GAG) gel through which gases move by diffusion, but there is resonance imaging has been used to visu- neurovascular structures within the sub- no bulky movement.22 This stage is referred alize arachnoid adhesions and tissue micro- arachnoid cisterns. To ensure the high to as meninx primitive, or primitive SAS, by structure within the SAS.17,18 standard of the review, articles with a Osaka et al.23 Most anatomic research has focused on high possibility of bias, and any study the subarachnoid cisterns and arachnoid published in nonpopular journals (not Phase 2: Origination and Expansion of mater but few data on SAT have been re- indexed in PubMed MEDLINE), were Fluid-Filled Cavities (Lacunae) Causing ported. The aim of this study is to detail excluded. Animal studies describing the Compaction of the Mesenchyme and Fibrous the configuration of SAT and provide in- embryologic development and the his- Material. The trabecular structure origi- formation on their embryologic origin, tology of the SAT were included. These nates from the localized withdrawal of this histology, and morphologic variation. articles included 19 book chapters, 58 GAG gel, which occurs at days 10e13 post- Their potential role in CSF flow and their original articles, 31 review articles, and 2 conception from arbitrarily positioned cen- surgical significance are also discussed. case reports containing reviews of the ters that start to appear in the gel, resulting literature. in randomly spaced and sized fluid-filled METHODS holes. As the cavities enlarge, the remain- Embryologic Development of SAT ing mesenchymal elements consisting of A comprehensive review of the published In 1975, McLone and Bondareff 19 reported a cells and fibers are forced to assemble in the literature was conducted in PubMed, detailed electron microscopic study of the tissue that remains in the cavities. As the Medline, EMBASE, Wiley Online Library, embryonic development of SAT in the cavities meet, the mesenchymal material Research Gate, Science Direct, Elsevier, mouse, which is similar to that in lining the cavities resists further advance- Cambridge journals, SAGE journals, and humans.20 Many of the data available on ment, leaving thin walls of mesenchyme in Oxford journals. Terms for the search SAT embryology are based on his work. random directions, which become the were subarachnoid trabeculae, subarach- The pattern of trabecular structure is set origin of the SAT. The loss of GAG gel on noid trabecular membrane, arachnoid during the first 17 postconceptual days in the upper and lower surfaces of the PPAS mater, subarachnoid trabeculae embry- mice. Embryologically, the trabeculae are during days 13e16 allows the mesenchyme ology, subarachnoid trabeculae histology the remnants of the common precursor to compact to form membranes (Figure 3). and morphology, trabecular cisterns, and that forms both the meningeal arachnoid The upper and lower surfaces of the Liliequist membrane (LM). No date re- and pia layers. strictions were imposed. The decision to pluripotential placeholder mesenchymal involve or eliminate reviews, and data cells start to specialize, becoming fibro- extraction, were completed by the authors, FORMATION OF THE POTENTIAL cytes, blood cells, vessels, and other tissues, and any controversies and disagreements PIA-ARACHNOID SPACE and reinforce these new membranes. These were resolved by discussion. During embryogenesis, the initial devel- surfaces give rise to the arachnoid and pial
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