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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: is suspended in (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 - 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, , 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: 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 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 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

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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 structures/membranes to which the trabec- opment of the SAS takes place in 2 24 phases. ular structure remains attached. This RESULTS description is generalized from rat fetal The literature search initially yielded tissue. Few data on the embryology of the 1113 articles. One hundred and ten Phase 1: The Development of a Space-Holding SAT are available. of these articles were relevant to SAT, Mesenchymal Layer. Shortly after closure of Concentrations of fibrous material also their embryology, histology, morphology, the neural tube, a mesenchymal layer appear, lining the expanding liquid-filled function, and the significance of moves forward from the future neck region lacunae. Bundles of microfibrils and their microsurgical anatomy for the of the developing spine to invade between collagen are commonly associated with

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Figure 2. The structure of the potential pia-arachnoid space immersed. This layer has no shape, form or any particular consisting of stellate mesenchymal cells linked together by their organization at this point in development and acts as a extended cytoplasmic processes. GS is the extracellular ground space-holding layer between the ectoderm and the substance gel (glycosaminoglycan gel) in which these cells are neuroepithelium for the future pia-arachnoid structures. lacunae in the outer pia-arachnoid layer and Arachnoid Mater. The most superficial layer and the SAT. The current concept of can serve as struts to maintain an open sub- of the arachnoid, referred to as the subdural trabecular columns connecting the arach- arachnoid pathway. As the resulting lacunae mesothelium, subdural neurothelium, or noid to the pia mater is more diverse and approach each other closely, the remaining dural border layer, comprises layers of thin, complex than previously believed.30,36-38 mesenchymal cells and fibers become densely arranged cells that abut the dura The collagen fibers of SAT are enveloped pressed into curtains stretched across the mater and is considered by Schachenmayr by leptomeningeal cells that are connected SAS. These curtains have holes in them andFriedetobeaportionofthedura16,18,26-29 through desmosomes and gap junctions, through which CSF can flow (Figure 3). (Figure 4). Adjacent to this dural border layer without tight junctions29 (Figure 5). These remaining walls are the trabeculae. is the arachnoid barrier layer, which consists Anderson11 and Hayreh12,13 acknowledged Osaka et al.23 described the resultant fluid of tightly packed polygonal cells, round thepresenceofSATintheSASofthehuman space as essentially the cleared-out connec- nuclei coupled with pale cytoplasm, and a without mentioning types or tive tissue space that is formed late in basement lamina that distinguishes it from distribution. Killer et al.40,41 acknowledged embryonic life. The framework of the SAS, the rest of the arachnoid. These cells are differences in the structure and distribution consisting of the outer arachnoidal mem- conjoined by characteristic tight junctions, of SAT among the different segments of the brane, the trabeculae, and the inner pial layer absent in the dural border and optic nerve. Several investigators have used is established by the seventeenth post- desmosomes that form an impermeable different terminologies when describing the conception day. barrier to CSF.30-34 Nabeshima et al.35 morphology of SAT. Parkinson42 used described this portion of the arachnoid in terms such as arachnoid septae, trabeculae, fi Trabecular Attachments humans as similar to, but signi cantly and rough strands to describe spinal SAS 43 Collagen fibers from the trabeculae are thicker than, the barrier layer of other structures. Delmaset et al. used terms attached to the arachnoid mater, which mammals. Both the dural border and the such as stout, columnar, and sheetlike to 29 forms the top surface of the PPAS, rein- arachnoid barrier layers are distinguishable describe cranial SAT. Alcolado et al. also fi fi forcing it with collagen so it can withstand by the lack of collagen brils that can be used the term sheetlike, along with liform 41 relatively powerful forces.16 Below the found in the pia and arachnoid maters. and chordae. Killer et al. chose to use the PPAS, the trabecular collagen passes Deeper to the arachnoid barrier layer, the terms trabeculae, pillar, and septae to through the pia mater, across the subpial arachnoid becomes more loosely packed describe SAS morphology of the human space, and attaches to the basement and is intermittently interlaced with optic nerve. fi membrane, beneath which it is collagen ber bundles. The innermost portion of the arachnoid consists of a embedded in a layer of astrocytes and SAT Variations. Variations in SAT Along the oligodendrocytes.25 narrow layer of leptomeningeal cells that are interconnected by desmosomes and gap Optic Nerve. The arachnoid mater and SAS along with the SAT surrounds the nerve junctions. Histology and Morphology of SAT throughout its course to the orbital cavity, To understand the histology of SAT in where they fuse with the .44 Killer et al. greater detail, the histology of the arach- SAT. It seems that previous literature found the trabeculae to be distributed noid membrane is crucial. oversimplified the morphology of the SAS among the bulbar and intra-canalicular

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Figure 3. Stages in the embryologic development of . GAG, glycosaminoglycan; SAT, subarachnoid trabeculae.

portions, but contrary to the observations by extracellular matrix supported these cells. the central components of the septa and Hayreh12,13 and Liu and Kahn,45 the The center of the trabeculae consisted of pillars was comparable to that of the trabeculae were most dense in the bulbar densely packed collagen fibrils organized trabeculae. segment of the optic nerve. Septae were into small bundles. Slim cytoplasmic Intracanalicular Portion of the Optic located in the midorbital portion, and bridges were seen connecting one Nerve. The SAS of the intracanalicular pillars were found in the intracanalicular trabecula to an adjacent one. Occasionally, segment was extremely narrow and con- and midorbital portions of the optic nerve the trabecular networks were noted to sisted of pillars and trabeculae as previ- SAS. contain a blood vessel or 2, as also ously described. The center of the canal Bulbar Segment of the Orbital Optic reported by Alcolado et al.29 established 1 or 2 large pillars approxi- Nerve. Scanning electron microscopy Midorbital Segment of the Orbital Optic mately 0.5 mm in size and encompassing 1 (SEM) of the bulbar segment showed that Nerve Portion. The SAS of the midorbital or 2 blood vessels.41,45 The other parts of the SAS were widest at this segment and segment was smaller than that of the the intracanalicular segment showed contained numerous round SAT without bulbar segment and consisted of an either delicate round and slightly curved broadening at the arachnoid and pia abundance of broad septae and round trabeculae of approximately 5 mm diameter layers.40,41 (Figure 6). They were found to pillars but contained no trabeculae.40,41,45 or single pillars with a diameter of have branches that formed a complex and Measurements were not provided for the approximately 25 mm, which expanded at delicate network. The measured width of septae, which were described as dividing the dural and pial attachment of the the trabeculae ranged from 5 to 7 mm.40,41 the SAS into chambers and containing arachnoidal layer.45 At the orbital opening They were enveloped in a sheath of flat, large perforations that connected adjacent of the canal, the trabeculae were more smooth leptomeningeal cells that on chambers. However, the pillars were abundant, running in parallel and occasion contained fenestrations 0.2e1. measured at a diameter ranging from 10 to bridging the SAS obliquely. 0 mm wide, probably because of the 30 mm and possessed broadened ends at Variations in SAT Along Blood Vessels and transmission electron microscopy (TEM) both terminations.40,41,45 The larger Nerves. SAT enclose the small blood vessels preparation and perhaps were not real diameter and broadened ends of the pil- and adhere to the surface of larger blood holes. TEM showed these leptomeningeal lars differentiated them from the trabec- vessels in the SAS and cisterns.1 cells forming single or multiple layers; the ulae, which were smaller in diameter and Furthermore, fine capillaries have been multiple layers were attached by lacked broadened ends. However, the found in the trabeculae of rats.46 At the desmosomes.41,45 It also showed that an histology of the leptomeningeal cells and sites of attachment, the trabeculae cells

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groups had fluctuating densities of fibrils; some were very densely packed, whereas others were less dense. Fluid was also found in deeper layers of the arachnoid between cells, which indicated that the arachnoid layer must have some degree of permeability. LM: An Anatomic Variant. According to Froelich et al.,54 the LM is a complex and variable arachnoidal structure that is either a single-layered, 2-layered, or 3-layered membrane. It is formed by a group of anatomically distinct arachnoid sheets: a diencephalic leaf (DL), a mesencephalic leaf (ML), and a pair of diencephalicemesen- cephalic leaves.55 According to Wang et al.,47 it consists of 3 layers: mesencephalic, diencephalic, and a pair of hypothalamic membranes. Spinal SAT. The literature on spinal SAT is sparse and knowledge about them is limited. Nauta et al.56 were the first to review the anatomy of the spinal subarachnoid with reference to the cadaver dissection work of Key and Retzius and based on their own operative experiences.57 Nauta et al.56 Figure 4. A nonstained pia-arachnoid complex from a sheep under a light microscope. The subarachnoid trabeculae (SAT) fibers (arrows), blood found that despite some variations, there vessels (BV), and arachnoid membrane tissue are visible. were consistent features in the spinal arachnoid anatomy. To resolve the confusion in the standard texts and become continuous with the cells on the shapes of trabeculae were also mentioned literature from a diversity of names, surface of the pia or the blood vessels.1 and described as “plates,”“veillike,”“pil- descriptions, and drawings of the human According to Yas¸argil,46 SAT also adhere lars,” and “rods.”20 The veillike spinal subarachnoid septa and trabeculae, to the nerves within the SAS. SAT tend to morphology was reported in regions Parkinson in 199142 carried out a study by be thicker where the and nerves where there was a greater density of SAT, examining 62 complete human cords pass through the trabeculated wall from usually associated with the closeness of under the dissecting microscope. He found one cisternal compartment to another. In blood vessels. SEM also established that that anteriorly there were essentially no most individuals, the 3 cisterns in which there are holes in the trabeculae ranging connecting septa or trabeculae between the the arachnoid trabeculae and membranes in size from approximately 0.5 to 3.0 mm, cord and the arachnoid membrane. are condensed and present the greatest making them permeable. Posteriorly, there is a scanty series of impediments during operations are the TEM was performed and the general connecting fibers and fenestrated sheets 1 , the quadrigeminal appearance of the collagen fibril bundles, or 2 mm on either side of the midline cistern, and the .47,48 the thickness of the individual collagen fi- (dorsolateral septa) in the upper cervical Neural elements including nerve endings bers, and the periodicity seen with alter- region. These fibers become increasingly in the arachnoid and SAT, mainly in the nating light and dark periods confirmed more widespread in the lower cervical cisterna magna, have been described; they what Kierszenbaum and van der Rest and region and remain extensive in the lumbar could contribute to conveying information Garrone52 had claimed: that the SAT were enlargement, beyond which they about CSF pressure gradients and also in composed of type I collagen.53 TEM also progressively dwindle to end abruptly at cerebral vasospasm.46 showed the collagen fibril groups to have the filum terminale origin. In 2015, Saboori and Sadegh20 used a lateral and a transverse orientation, According to Rickenbacher et al.,58 only Sprague-Dawley rats to investigate the his- which confirmed the rodlike morphology in the upper cervical region are there few tology and morphology of SAT more fully of the SAT seen on SEM. Fibroblastic cells trabeculae in the midline both ventrally since it had been shown that the trabeculae surrounded the collagen fibril groups that and dorsally. In the lower cervical in rats and humans were morphologically make up the SAT. Also, the SAT were region, only the dorsal trabeculae fibers similar.49-51 SEM showed tree-shaped SAT surrounded by 50e200 nm of extracellular show membranous expansion, first that consisted of branches from the matrix that consisted not only of collagen forming an incomplete and then arachnoid mater converging into a single fibrils but also of fibronectins, laminins, caudally a complete membrane called the trunk attached to the pia mater. Other and proteoglycans. The collagen fibril dorsal subarachnoid septum (septum

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arachnoid membrane, arachnoid trabeculae, subarachnoid vasculature, and pia membrane, has a significant effect on brain biomechanics and increases the local variability of stress along the brain. This study, carried out using complex finite element models of the immature piglet brain to identify changes in cortical stress distribution, showed that incorporating the regional variability of PAC substructures substantially altered the distribution of the main stress on the cortical surface of the brain. This finding shows that despite the small volumetric contribution of the PAC to the intracranial space, the microstructural variability has a considerable effect on brain mechanics during head rotation, thereby contributing significantly to brain deformation. The Figure 5. Spinal and subarachnoid space. A view of the cut end of data suggested that this regional the spinal cord from dog (SPC) shows the pia mater (PM) lying directly upon the surface of the cord. The arachnoid trabeculae (AT), continuous with the variability of PAC substructures could also pia, extend to the arachnoid mater (AM) and to an (A) above. The influence localized predictions of separation of the arachnoid mater from the thick (DM) is an .64 artifact of preparation. The subarachnoid space (SAS) separates the arachnoid from the pia. Original magnification 140.39 Role in CSF Flow. The curtainlike structure of the SAT stretched across the SAS has holes through which CSF flows (Figure 7). posticum).58 This septum extends as far joined to each other by strands and This feature could play a part in the CSF down as the dividing webs. The trabecular arachnoid of the dynamics between the SAS of the optic the dorsal SAS into left and right spine restricts nerve root movement to a nerve and the chiasmal cistern and compartments. Throughout the length, definite extent, holding each root in its contribute to understanding of the there are many unexplained, redundant, position within the dural sac and in pathophysiology of asymmetric and nonbranching, beaded, thicker rogue relation to other nerve roots.59 As the unilateral papilledema.40,41 Changes in strands. All of these strands differ in ventral roots of the spinal nerves traverse their structure after trauma or hemorrhage character from the right-angle fiber the ventral part of the SAS, their could in principle contribute to arrangement of the denticulate ligament, filaments are hinged to each other and posttraumatic and posthemorrhagic the 2 leaves of which are often separated to the ligamentum denticulatum by the hydrocephalus. Alterations in CSF flow to form segmental longitudinal tunnels.42 delicate trabecular connective tissue.58 velocities have been noted in the spinal Intermittently, they become tangentially SAS near arachnoid adhesions.18,65 Several adherent to the arachnoid membrane. In Functions of SAT computational fluid dynamicsebased the thoracic region, these trabeculae Mechanical Properties. According to Killer studies have indicated the possible form relatively fenestrated membranes et al.,40 SAT could play more of a filler role importance of SAT in CSF solute transport running obliquely anteroinferiorly in rather than a support role. Other and pressures. Stockman66 found that SAS correspondence to the nerve roots, reports40,60-64 state that SAT seem to be microanatomy increased CSF flow mixing forming slanting compartments.58 In the important as mechanical pillars between but had a relatively small effect on overall lumbar region, these root septa divide the pia and arachnoid membranes, CSF velocity profiles. Tangen et al.67 found into trabeculae that become progressively damping and constraining the movement that SAT drastically affected solute scant toward the and along of the brain relative to the skull, and transport within the SAS. Gupta et al.68,69 its course. Throughout the cauda equina, thereby possibly affecting traumatic brain implemented a computational fluid strands are haphazardly arranged injuries. The random three-dimensional dynamics model that included anisotropic connecting the roots and supporting redundant structure of the walls is resil- permeability within the cortical SAS caused blood vessels.42,58 Parkinson42 found no ient and can lose a few elements without by pillar-shaped SAT. evidence of change in the number or failure under severe conditions such as type of connection with age. trauma. In such conditions, the stress is Role After Hemorrhage. In subarachnoid The spinal SAT give shape to tubular redistributed among the remaining hemorrhage (SAH), SAT as collagen arachnoid sheaths for each nerve root and elements of its structure.15,60 bundles in the SAS are considered to for the spinal cord.59 Fila radicularia, the A model described by Scott et al.64 have a role in activating the Hageman nerve rootlets for each dermatome, are suggests that the PAC, which includes the factor in the coagulation system.70,71

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that leads to the separation of the DBC layer.75 Intracranial hypotension caused by CSF leakage and coagulopathies can also lead to CSDH in the same manner.74,75,79

Surgical Significance of SAT Arachnoid membranes, including LM, are of paramount surgical importance and are key landmarks in microsurgical proced- ures.80-82 These structures help to delin- eate the contour of the lesions, hence protecting nearby brain structures. Never- theless, neurosurgeons should always pay particular attention to the topography of the cisterns and associated arachnoidal adhesions and trabeculae in microsurgical approaches to preclude injury to the surrounding neurovascular structures. Furthermore, the trabecular membranes are structured in a compartmental form that can limit the spread of blood (e.g., from a ruptured aneurysm) to other cis- terns by allowing the injury to remain localized by observing the blood-filled cistern.80,83-85 Although Yas¸argil46,86,87 provided a detailed description of the subarachnoid

Figure 6. Scanning electron microscopy appearance of the subarachnoid space in the bulbar segment. cistern, the compartmental trabecular (A) Overview of the subarachnoid space showing the complex network of trabeculae. The arrows membranes remain to be described. Vinas point to veillike cytoplasmic extensions between adjacent trabeculae (bar ¼ 150 mm). (B, C) Delicate et al.88-90 were the first to describe the m arrow subarachnoid space network formed by branching trabeculae (bar ¼ 50 m). The points to a microsurgical anatomy of the compart- trabeculum with a blood vessel. Note again the veillike cytoplasmic extensions connecting adjacent fi trabeculae (bar ¼ 2 mm). Surface of trabeculae covered by flattened cells with distinct intercellular mental SAT and their surgical signi cance clefts and fenestrations (bar ¼ 0.2 mm).41 in detail. These investigators noted that the SAS is lined by trabecular membranes, extending from the arachnoid mater to the pia mater.88-90 They also noticed that in Platelets are also believed to be activated organization of collagen fibers, and the certain areas, trabecular membranes form by trabeculae, as well as by thrombin absence of strengthening trabeculae lead to dense networks that resemble an authentic during SAH.70,71 separation of the dural border cell (DBC) true membrane.88-90 Yas¸argil (1984) and layer and tearing of bridging veins, resulting Vinas (1994) also reported that these SAT Role in Formation of Chronic Subdural in bleeding and hematoma formation.74,78 divide the SAS into compartments called . Chronic subdural hematomas In elderly patients with age-adequate ce- cisterns.46,89 According to Yas¸argil (CSDHs) usually occur after a head trauma rebral atrophy, a negative pressure is pro- et al.,46,86,87 these SAT networks hold a in children, and without trauma in the duced within the cranium as well, as the significant microsurgical importance alcoholic population and in the elderly (>65 distance from the skull to the cerebral cortex because they provide physical support to years) as a result of cerebral atrophy and becomes longer.74 The bridging veins are the arteries, veins, and nerves that pass degeneration when there is adequate sub- stretched on the atrophied hemisphere and within and through them. However, the dural space.72,73 SAT may contribute to may become torn even by a minor walls of the cisterns direct the flow of CSF posttraumatic CSDH or hygromas possibly unnoticed nontraumatic acceleration- through openings of various sizes.88-90 by tears in minor vessels supplying the deacceleration injury.74,75 If the distance These membranes help to protect the arachnoid, as well as tears in the arachnoid surpasses the length of SAT, it causes the entire SAS from collapse during rupture or caused by traction of the trabeculae.74-77 The separation of the DBC layer, forming a hy- a surgical approach to a cistern with the trabeculae in the SAS are more condensed pothetical in which the blood consequent loss of CSF.85,87,89 However, in compared with the subdural space, from the bleeding bridging veins is accu- certain situations such as SAH or bacterial contributing more to the delicate nature of mulated.75 Cranial morphology and the , the flow of fluid through bridging veins. In trauma, the tinny fragile degree of cerebral atrophy are the 2 actors various cisterns can be retarded or walls of these bridging veins, the that determine the force pulling the SAT prevented.88-90

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compartment. Dissection within the sub- arachnoid cisterns depends on sectioning of the SAT. An interesting model devel- oped by Scott et al.64 implied that changes in the density of SAT could affect the local biomechanical properties of the brain, making specific regions prone to traumatic bleeding. Studies are under way measuring the biomechanical properties of the SAT and their potential alterations during different CNS diseases. Although the SAT and arachnoid mem- brane act as a support structure, they are also held in place by within the CSF system. Alterations in intracranial CSF pressure can affect the Figure 7. A closer look at the three-dimensional redundant structure of the subarachnoid trabeculae. SAT, arachnoid membranes, and CSF The curtainlike walls have holes in them through which cerebrospinal fluid (CSF) can flow. space geometries. For example, post mor- tem, the arachnoid membrane quickly de- laminates from the dura and collapses on Microsurgical procedures should be per- provide a safe and clear surgical plane for top of the cortical surface as a result of loss formed with great care and the trabeculae operating on these tumors, if it is followed of intracranial pressure concomitant with pulled as lightly as possible because of their clearly.54,55,96,98 CSF absorption into the dural venous si- relationship to neurovascular structures88-90 nuses as venous pressure decreases. Thus, (see Video 1). Vinas et al.88-90 examined postmortem visualization of SAT is difficult DISCUSSION the relationship between SAT found in because the layers of tissue and fibers supratentorial and infratentorial levels and Previous studies have sought to describe the become relatively tightly cupped around the at the levels of tentorium to their meninges and their roles in brain and spinal brain. The cortical SAS changes so corresponding blood vessels cord function and stability. Comparatively dramatically that the cortical CSF normally and . According little attention has been given to enveloping the brain is nearly nonexistent. tothedataavailableinthe the SAT and their role. Yas¸argil This situation can make anatomic dissec- literature, the variations of made ground-breaking efforts in tion and study of the SAT and related the subarachnoid trabecular describing the topographic structures challenging and drastically alters membrane and subarachnoid Video available at anatomy of subarachnoid cis- study of the normal CSF compartmental cisterns are summarized in WORLDNEUROSURGERY.org terns and their importance in volumes and geometry. Similarly, during Tables 1 and 2.88-94 cerebrovascular and skull base surgical opening of the arachnoid mem- 46,86,89 LM is an important anatomic landmark . SAT were also mentioned as brane, CSF pressures are altered and can in the approach to the parasellar and part of these subarachnoid cisterns but their thereby also affect the normal CSF space premesencephalic and prepontine structure and role have not been further geometry and volumes. Delamination of areas.80,88-90,95-97 Understanding of delineated. In recent years, researchers have the arachnoid membrane from the dura trabecular membranes, including the LM described SAT anatomy and variations in the and leakage of CSF into this region can 11-13,20,29-38,40-81,99 and its relation to the surroundings central . result in formation of arachnoid cysts and structures, which can be determined by SAT have mostly been seen as part of the other cavities. The interaction of CSF flow preoperative imaging, can help surgeons PAC. In recent years, they have attracted and pressures can lead to alterations in to plan the route of access, improve increasing interest. Their role has evolved volume. exposure, and minimize injuries. from being a filler of the SAS into support- The DL of this membrane has significant ing pillars. This role immediately puts them The Relationship Between the Number of importance in surgical approaches to the at the center for balancing intracranial and SAT and Propensity for Cerebral Trauma sellar and parasellar region and divides the intraspinal biomechanics, stabilizing neuro- As Scott et al. suggested in their numeric cisterns of the skull base into pre-Liliequist vascular structures such as cranial nerves, modeling studies discussed in detail and post-Liliequist groups.54,55,96,98 The arteries, and veins in the arachnoid cisterns earlier, more numerous SAT could in- ML has less surgical importance than does and also affecting CSF flow, thereby giving crease the likelihood of injury to the brain. the DL.54,95 The ML separates the supra- them surgical significance. Increased SAT can increase surface tentorial from infratentorial cisterns.54,87,97 stresses on the brain, leading to a greater In perimesencephalic lesions, such as The Role of SAT as Supporting Structures propensity for injury to the delicate brain diaphragm sellae , and and Interaction with Intracranial Pressure tissue and cortical draining veins. Here, trigeminal neuromas, the ML can be pre- During microsurgery, SAT maintain there is a huge gap of knowledge that served by displacing upward and can the SAS as a firm open CSF-filled needs to be addressed in future research.

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Table 1. Paired and Unpaired Trabecular Membranes

Subarachnoid Trabecular Membrane Supratentorial Level Infratentorial Level At the Level of Tentorium

Paired Anterior cerebral membrane Superior cerebellar membrane Cerebellar precentral Posterior communicating membrane Basilar membrane Superior cerebellar Anterior choroidal membrane Anterior inferior cerebral membrane Lateral oculomotor Lateral oculomotor membrane Posterior inferior cerebral membrane Caudal oculomotor Caudal oculomotor membrane Perforated membrane Olfactory membrane Carotid membrane Unpaired Liliequist membrane Liliequist membrane Liliequist membrane Top basilar Chiasmatic Top basilar

Potential Role of SAT in Hydrocephalus role of CSF pulse-timing along the spine needed retraction would be facilitated by and Related Disorders in syringomyelia.104-107 The elongated SAT careful sharp dissection of the SAT, and Understanding their anatomy, along with structure and integral fluid-solid connec- without retraction. The emergence of further understanding of CSF dynamics, tion to the delicate tissue surface could retractionless microneurosurgery, and the sheds new light on potential functions of also contribute via the cellular mechano- importance of neurovascular structures the SAT. It is not unrealistic to assume sensitivity of CNS tissues.108-110 within the subarachnoid cisterns and the that thickening of the SAT after trauma or potential role of SAT, are all reasons especially SAH could be a cofactor in the Surgical Importance of SAT enough to extend much-needed basic and development of communicating hydro- The role of SAT in maintaining the neu- clinical research to these previously over- cephalus. For example, a local increase in rovascular structures within the SAS has looked but important structures. SAT distribution could alter the pulse- been extensively outlined in this study. damping characteristics of the intracra- Retractorless microneurosurgery has nial cavity and/or flow dynamics,21,24,100 emerged as an important aspect of mod- CONCLUSIONS thereby affecting interstitial fluid trans- ern safe neurosurgery. Cautious sectioning SAT are delicate thin mesenchymal col- port within the CNS tissues.69,101-103 If this of the SAT within the SAS during surgery umns of collagen-reinforced material process could be shown then the surgical allows the neurosurgeon not only to stretching between the arachnoid and pia literature would need to reform its termi- mobilize the cranial nerves, arteries, and membranes and appear to be significant for nology of communicating hydrocephalus veins within the subarachnoid cisterns and the stability of the SAS, the protection of the to micro-obstructive hydrocephalus if hy- to protect them but also to mobilize the cranial nerves, arteries and vessels within pertrophied SAH proved to be the cause. brain easily with no need for retraction. the subarachnoid cisterns, the stability of Other recent work has indicated a possible Hence, access to areas that previously the brain within the SAS, and potentially

Table 2. Paired and Unpaired Subarachnoid Cisterns

Subarachnoid Cisterns Supratentorial Level Infratentorial Level At the Level of Tentorium

Paired Olfactory cistern Pontocerebellar cistern Ambient cistern Carotid cistern Cerebellomedullar cistern Sylvius cistern Ambient cistern Crural cistern Posterior communicating cistern Oculomotor cistern Unpaired Basilar cistern Interpeduncular cistern cistern Cisterna magna Quadrigeminal cistern Supra-cerebellar cistern Superior cerebellar cistern Velum interpositum cistern

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