subarachnoid trabeculae: a comprehensive review of their

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

INTRODUCTION

In the third century B.C., Herophilus, aGreek physician and the father of anatomy,first described the brain as being enclosedwithin the arachnoid membrane.1 In theseventeenth century, Gerardus Blasius andAndreas Ottomar Goelicke referred to thearachnoid membrane as “tertia cerebrimeninge” or the third cerebral meninge.2-8

The current name of arachnoid mater isattributed to Frederick Ruysch and hisdescription of a spiderlike morphology in1699.9 It is a delicate avascular layer indirect contact with the dura and separatedfrom the pia mater by the cerebrospinalfluid (CSF)-filled subarachnoid space,showing distinctive histology andpathology.1,10

During the late 1960s, Anderson andHayreh along with others describedsubarachnoid trabeculae (SAT), which aresheets or columns of collagen-reinforcedmaterial stretching between the arachnoidand pia membranes11-13 (Figure 1). The

delicate neural tissue of the brain issuspended within the CSF by buoyancy, inaccordance with the Archimedes principle,and also mechanically stabilized by the SATwithin the pia-arachnoid complex (PAC).14

SAT constrain relative movement betweenthe skull and the brain as proposed in theshaken baby syndrome hypothesis.15 TheseSAT, also referred to as arachnoidtrabeculae, subarachnoid space (SAS)trabeculae, or leptomeningeal trabeculae,can be seen with light microscopes but aretoo thin to be detected by ultrasonographyor clinical magnetic resonance imaging.16

Nevertheless, high-resolution magnetic

- INTRODUCTION: Brain is suspended in cerebrospinal fluid (CSF)-filled sub-arachnoid space by subarachnoid trabeculae (SAT), which are collagen-reinforced columns stretching between the arachnoid and pia maters. Muchneuroanatomic research has been focused on the subarachnoid cisterns andarachnoid matter but reported data on the SAT are limited. This study provides acomprehensive review of subarachnoid trabeculae, including their embryology,histology, morphologic variations, and surgical significance.

-METHODS: A literature search was conducted with no date restrictions inPubMed, Medline, EMBASE, Wiley Online Library, Cochrane, and Research Gate.Terms for the search included but were not limited to subarachnoid trabeculae,subarachnoid trabecular membrane, arachnoid mater, subarachnoid trabeculaeembryology, subarachnoid trabeculae histology, and morphology. Articles with ahigh likelihood of bias, any study published in nonpopular journals (not indexedin PubMed or MEDLINE), and studies with conflicting data were excluded.

-RESULTS: A total of 1113 articles were retrieved. Of these, 110 articlesincluding 19 book chapters, 58 original articles, 31 review articles, and 2 casereports met our inclusion criteria.

-CONCLUSIONS: SAT provide mechanical support to neurovascular structuresthrough cell-to-cell interconnections and specific junctions between the pia andarachnoid maters. They vary widely in appearance and configuration amongdifferent parts of the brain. The complex network of SAT is inhomogeneous andmainly located in the vicinity of blood vessels. Microsurgical procedures shouldbe performed with great care, and sharp rather than blunt trabecular dissectionis recommended because of the close relationship to neurovascular structures.The significance of SAT for cerebrospinal fluid flow and hydrocephalus is to bedetermined.

Key words- Arachnoid matter- Liliequist membrane- Microsurgical procedures- Subarachnoid trabeculae- Subarachnoid trabecular membrane- Trabecular cisterns

Abbreviations and AcronymsCSDH: Chronic subdural hematomaCSF: Cerebrospinal fluidDBC: Dural border cellDL: Diencephalic leafGAG: GlycosaminoglycanLM: Liliequist membraneML: Mesencephalic leafPAC: Pia-arachnoid complexPPAS: Potential pia-arachnoid spaceSAH: Subarachnoid hemorrhageSAS: Subarachnoid spaceSAT: Subarachnoid trabeculaeSEM: Scanning electron microscopyTEM: Transmission electron microscopy

From the 1National Skull Base Center, Thousand Oaks,California; 2California Institute of Neuroscience, ThousandOaks, California; 3Advocate BroMenn Medical Center,Normal, Illinois; 4University of Arizona College of Medicine,Tucson, Arizona; 5University of California Irvine MedicalCenter, Irvine, California; 6University of Idaho, Moscow,Idaho; and 7Seattle Science Foundation, Seattle,Washington, USA

To whom correspondence should be addressed:Martin M. Mortazavi, M.D.[E-mail: [email protected]]

Supplementary digital content available online.

Citation: World Neurosurg. (2018) 111:279-290.https://doi.org/10.1016/j.wneu.2017.12.041Journal homepage: www.WORLDNEUROSURGERY.org

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resonance imaging has been used to visu-alize arachnoid adhesions and tissue micro-structure within the SAS.17,18

Most anatomic research has focused onthe subarachnoid cisterns and arachnoidmater but few data on SAT have been re-ported. The aim of this study is to detailthe configuration of SAT and provide in-formation on their embryologic origin,histology, and morphologic variation.Their potential role in CSF flow and theirsurgical significance are also discussed.

METHODS

A comprehensive review of the publishedliterature was conducted in PubMed,Medline, EMBASE, Wiley Online Library,Research Gate, Science Direct, Elsevier,Cambridge journals, SAGE journals, andOxford journals. Terms for the searchwere subarachnoid trabeculae, subarach-noid trabecular membrane, arachnoidmater, subarachnoid trabeculae embry-ology, subarachnoid trabeculae histologyand morphology, trabecular cisterns, andLiliequist membrane (LM). No date re-strictions were imposed. The decision toinvolve or eliminate reviews, and dataextraction, were completed by the authors,and any controversies and disagreementswere resolved by discussion.

RESULTS

The literature search initially yielded1113 articles. One hundred and tenof these articles were relevant to SAT,their embryology, histology, morphology,function, and the significance oftheir microsurgical anatomy for the

neurovascular structures within the sub-arachnoid cisterns. To ensure the highstandard of the review, articles with ahigh possibility of bias, and any studypublished in nonpopular journals (notindexed in PubMed MEDLINE), wereexcluded. Animal studies describing theembryologic development and the his-tology of the SAT were included. Thesearticles included 19 book chapters, 58original articles, 31 review articles, and 2case reports containing reviews of theliterature.

Embryologic Development of SATIn 1975, McLone and Bondareff 19 reported adetailed electron microscopic study of theembryonic development of SAT in themouse, which is similar to that inhumans.20 Many of the data available onSAT embryology are based on his work.The pattern of trabecular structure is setduring the first 17 postconceptual days inmice. Embryologically, the trabeculae arethe remnants of the common precursorthat forms both the meningeal arachnoidand pia layers.

FORMATION OF THE POTENTIALPIA-ARACHNOID SPACE

During embryogenesis, the initial devel-opment of the SAS takes place in 2phases.

Phase 1: The Development of a Space-HoldingMesenchymal Layer. Shortly after closure ofthe neural tube, a mesenchymal layermoves forward from the future neck regionof the developing spine to invade between

the embryonic epithelium (ectoderm) andthe developing neuroepithelium of thetelencephalon.16,19,21 At this stage, thereare no arachnoid or pia membranes in thepotential pia-arachnoid space (PPAS). Thisformless layer is composed of a gel-filledmesenchymal network as groundsubstance and acts as a space-holding layerfor 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 throughlong extended interconnecting cytoplasmicprocesses called pseudopodia.16,19,21 Theextensive extracellular space is filled withglycosaminoglycan (GAG) gel throughwhich gases move by diffusion, but there isno bulky movement.22 This stage is referredto as meninx primitive, or primitive SAS, byOsaka et al.23

Phase 2: Origination and Expansion ofFluid-Filled Cavities (Lacunae) CausingCompaction of the Mesenchyme and FibrousMaterial. The trabecular structure origi-nates from the localized withdrawal of thisGAG gel, which occurs at days 10e13 post-conception from arbitrarily positioned cen-ters that start to appear in the gel, resultingin randomly spaced and sized fluid-filledholes. As the cavities enlarge, the remain-ing mesenchymal elements consisting ofcells and fibers are forced to assemble in thetissue that remains in the cavities. As thecavities meet, the mesenchymal materiallining the cavities resists further advance-ment, leaving thin walls of mesenchyme inrandom directions, which become theorigin of the SAT. The loss of GAG gel onthe upper and lower surfaces of the PPASduring days 13e16 allows the mesenchymeto compact to form membranes (Figure 3).The upper and lower surfaces of the

pluripotential placeholder mesenchymalcells start to specialize, becoming fibro-cytes, blood cells, vessels, and other tissues,and reinforce these newmembranes. Thesesurfaces give rise to the arachnoid and pialstructures/membranes to which the trabec-ular structure remains attached.24 Thisdescription is generalized from rat fetaltissue. Few data on the embryology of thespinal cord SAT are available.Concentrations of fibrous material also

appear, lining the expanding liquid-filledlacunae. Bundles of microfibrils andcollagen are commonly associated with

Figure 1. Organization of subarachnoid trabeculae in the subarachnoid space between the pia materand arachnoid mater.

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lacunae in the outer pia-arachnoid layer andcan serve as struts to maintain an open sub-arachnoid pathway. As the resulting lacunaeapproach each other closely, the remainingmesenchymal cells and fibers becomepressed into curtains stretched across theSAS. These curtains have holes in themthrough which CSF can flow (Figure 3).These remaining walls are the trabeculae.

Osaka et al.23 described the resultant fluidspace as essentially the cleared-out connec-tive tissue space that is formed late inembryonic life. The framework of the SAS,consisting of the outer arachnoidal mem-brane, the trabeculae, and the inner pial layeris established by the seventeenth post-conception day.

Trabecular AttachmentsCollagen fibers from the trabeculae areattached to the arachnoid mater, whichforms the top surface of the PPAS, rein-forcing it with collagen so it can withstandrelatively powerful forces.16 Below thePPAS, the trabecular collagen passesthrough the pia mater, across the subpialspace, and attaches to the basementmembrane, beneath which it isembedded in a layer of astrocytes andoligodendrocytes.25

Histology and Morphology of SATTo understand the histology of SAT ingreater detail, the histology of the arach-noid membrane is crucial.

Arachnoid Mater. The most superficial layerof the arachnoid, referred to as the subduralmesothelium, subdural neurothelium, ordural border layer, comprises layers of thin,densely arranged cells that abut the duramater and is considered by Schachenmayrand Friede to be a portion of the dura16,18,26-29

(Figure 4). Adjacent to this dural border layeris the arachnoid barrier layer, which consistsof tightly packed polygonal cells, roundnuclei coupled with pale cytoplasm, and abasement lamina that distinguishes it fromthe rest of the arachnoid. These cells areconjoined by characteristic tight junctions,absent in the dural border anddesmosomes that form an impermeablebarrier to CSF.30-34 Nabeshima et al.35

described this portion of the arachnoid inhumans as similar to, but significantlythicker than, the barrier layer of othermammals. Both the dural border and thearachnoid barrier layers are distinguishableby the lack of collagen fibrils that can befound in the pia and arachnoid maters.Deeper to the arachnoid barrier layer, thearachnoid becomes more loosely packedand is intermittently interlaced withcollagen fiber bundles. The innermostportion of the arachnoid consists of anarrow layer of leptomeningeal cells thatare interconnected by desmosomes and gapjunctions.

SAT. It seems that previous literatureoversimplified the morphology of the SAS

and the SAT. The current concept oftrabecular columns connecting the arach-noid to the pia mater is more diverse andcomplex than previously believed.30,36-38

The collagen fibers of SAT are envelopedby leptomeningeal cells that are connectedthrough desmosomes and gap junctions,without tight junctions29 (Figure 5).Anderson11 and Hayreh12,13 acknowledged

the presence of SAT in the SAS of the humanoptic nerve without mentioning types ordistribution. Killer et al.40,41 acknowledgeddifferences in the structure and distributionof SAT among the different segments of theoptic nerve. Several investigators have useddifferent terminologies when describing themorphology of SAT. Parkinson42 usedterms such as arachnoid septae, trabeculae,and rough strands to describe spinal SASstructures. Delmaset et al.43 used termssuch as stout, columnar, and sheetlike todescribe cranial SAT. Alcolado et al.29 alsoused the term sheetlike, along with filiformand chordae. Killer et al.41 chose to use theterms trabeculae, pillar, and septae todescribe SAS morphology of the humanoptic nerve.

SAT Variations. Variations in SAT Along theOptic Nerve. The arachnoid mater and SASalong with the SAT surrounds the nervethroughout its course to the orbital cavity,where they fusewith the sclera.44Killer et al.found the trabeculae to be distributedamong the bulbar and intra-canalicular

Figure 2. The structure of the potential pia-arachnoid spaceconsisting of stellate mesenchymal cells linked together by theirextended cytoplasmic processes. GS is the extracellular groundsubstance gel (glycosaminoglycan gel) in which these cells are

immersed. This layer has no shape, form or any particularorganization at this point in development and acts as aspace-holding layer between the ectoderm and theneuroepithelium for the future pia-arachnoid structures.


LITERATURE REVIEW



portions, but contrary to the observations byHayreh12,13 and Liu and Kahn,45 thetrabeculae were most dense in the bulbarsegment of the optic nerve. Septae werelocated in the midorbital portion, andpillars were found in the intracanalicularand midorbital portions of the optic nerveSAS.Bulbar Segment of the Orbital OpticNerve. Scanning electron microscopy(SEM) of the bulbar segment showed thatthe SAS were widest at this segment andcontained numerous round SAT withoutbroadening at the arachnoid and pialayers.40,41 (Figure 6). They were found tohave branches that formed a complex anddelicate network. The measured width ofthe trabeculae ranged from 5 to 7 mm.40,41

They were enveloped in a sheath of flat,smooth leptomeningeal cells that onoccasion contained fenestrations 0.2e1.0 mm wide, probably because of thetransmission electron microscopy (TEM)preparation and perhaps were not realholes. TEM showed these leptomeningealcells forming single or multiple layers; themultiple layers were attached bydesmosomes.41,45 It also showed that an

extracellular matrix supported these cells.The center of the trabeculae consisted ofdensely packed collagen fibrils organizedinto small bundles. Slim cytoplasmicbridges were seen connecting onetrabecula to an adjacent one. Occasionally,the trabecular networks were noted tocontain a blood vessel or 2, as alsoreported by Alcolado et al.29

Midorbital Segment of the Orbital OpticNerve Portion. The SAS of the midorbitalsegment was smaller than that of thebulbar segment and consisted of anabundance of broad septae and roundpillars but contained no trabeculae.40,41,45

Measurements were not provided for theseptae, which were described as dividingthe SAS into chambers and containinglarge perforations that connected adjacentchambers. However, the pillars weremeasured at a diameter ranging from 10 to30 mm and possessed broadened ends atboth terminations.40,41,45 The largerdiameter and broadened ends of the pil-lars differentiated them from the trabec-ulae, which were smaller in diameter andlacked broadened ends. However, thehistology of the leptomeningeal cells and

the central components of the septa andpillars was comparable to that of thetrabeculae.Intracanalicular Portion of the OpticNerve. The SAS of the intracanalicularsegment was extremely narrow and con-sisted of pillars and trabeculae as previ-ously described. The center of the canalestablished 1 or 2 large pillars approxi-mately 0.5 mm in size and encompassing 1or 2 blood vessels.41,45 The other parts ofthe intracanalicular segment showedeither delicate round and slightly curvedtrabeculae of approximately 5 mm diameteror single pillars with a diameter ofapproximately 25 mm, which expanded atthe dural and pial attachment of thearachnoidal layer.45 At the orbital openingof the canal, the trabeculae were moreabundant, running in parallel andbridging the SAS obliquely.Variations in SAT Along Blood Vessels andNerves. SAT enclose the small blood vesselsand adhere to the surface of larger bloodvessels in the SAS and cisterns.1

Furthermore, fine capillaries have beenfound in the trabeculae of rats.46 At thesites of attachment, the trabeculae cells

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


LITERATURE REVIEW




become continuous with the cells on thesurface of the pia or the blood vessels.1

According to Yasargil,46 SAT also adhereto the nerves within the SAS. SAT tend tobe thicker where the arteries and nervespass through the trabeculated wall fromone cisternal compartment to another. Inmost individuals, the 3 cisterns in whichthe arachnoid trabeculae and membranesare condensed and present the greatestimpediments during operations are theinterpeduncular cistern, the quadrigeminalcistern, and the cisterna magna.47,48

Neural elements including nerve endingsin the arachnoid and SAT, mainly in thecisterna magna, have been described; theycould contribute to conveying informationabout CSF pressure gradients and also incerebral vasospasm.46

In 2015, Saboori and Sadegh20 usedSprague-Dawley rats to investigate the his-tology and morphology of SAT more fullysince it had been shown that the trabeculaein rats and humans were morphologicallysimilar.49-51 SEM showed tree-shaped SATthat consisted of branches from thearachnoid mater converging into a singletrunk attached to the pia mater. Other

shapes of trabeculae were also mentionedand described as “plates,” “veillike,” “pil-lars,” and “rods.”20 The veillikemorphology was reported in regionswhere there was a greater density of SAT,usually associated with the closeness ofblood vessels. SEM also established thatthere are holes in the trabeculae rangingin size from approximately 0.5 to 3.0 mm,making them permeable.TEM was performed and the general

appearance of the collagen fibril bundles,the thickness of the individual collagen fi-bers, and the periodicity seen with alter-nating light and dark periods confirmedwhat Kierszenbaum and van der Rest andGarrone52 had claimed: that the SAT werecomposed of type I collagen.53 TEM alsoshowed the collagen fibril groups to havea lateral and a transverse orientation,which confirmed the rodlike morphologyof the SAT seen on SEM. Fibroblastic cellssurrounded the collagen fibril groups thatmake up the SAT. Also, the SAT weresurrounded by 50e200 nm of extracellularmatrix that consisted not only of collagenfibrils but also of fibronectins, laminins,and proteoglycans. The collagen fibril

groups had fluctuating densities of fibrils;some were very densely packed, whereasothers were less dense. Fluid was alsofound in deeper layers of the arachnoidbetween cells, which indicated that thearachnoid layer must have some degree ofpermeability.LM: An Anatomic Variant. According toFroelich et al.,54 the LM is a complex andvariable arachnoidal structure that is eithera single-layered, 2-layered, or 3-layeredmembrane. It is formed by a group ofanatomically distinct arachnoid sheets: adiencephalic leaf (DL), amesencephalic leaf(ML), and a pair of diencephalicemesen-cephalic leaves.55 According to Wanget al.,47 it consists of 3 layers:mesencephalic, diencephalic, and a pair ofhypothalamic membranes.Spinal SAT. The literature on spinal SAT issparse and knowledge about them islimited. Nauta et al.56 were the first to reviewthe anatomy of the spinal subarachnoid withreference to the cadaver dissection work ofKey and Retzius and based on their ownoperative experiences.57 Nauta et al.56

found that despite some variations, therewere consistent features in the spinalarachnoid anatomy. To resolve theconfusion in the standard texts andliterature from a diversity of names,descriptions, and drawings of the humanspinal subarachnoid septa and trabeculae,Parkinson in 199142 carried out a study byexamining 62 complete human cordsunder the dissecting microscope. He foundthat anteriorly there were essentially noconnecting septa or trabeculae between thecord and the arachnoid membrane.Posteriorly, there is a scanty series ofconnecting fibers and fenestrated sheets 1or 2 mm on either side of the midline(dorsolateral septa) in the upper cervicalregion. These fibers become increasinglymore widespread in the lower cervicalregion and remain extensive in the lumbarenlargement, beyond which theyprogressively dwindle to end abruptly atthe filum terminale origin.According to Rickenbacher et al.,58 only

in the upper cervical region are there fewtrabeculae in the midline both ventrallyand dorsally. In the lower cervicalregion, only the dorsal trabeculae fibersshow membranous expansion, firstforming an incomplete and thencaudally a complete membrane called thedorsal subarachnoid septum (septum

Figure 4. A nonstained pia-arachnoid complex from a sheep under a lightmicroscope. The subarachnoid trabeculae (SAT) fibers (arrows), bloodvessels (BV), and arachnoid membrane tissue are visible.


LITERATURE REVIEW



posticum).58 This septum extends as fardown as the conus medullaris dividingthe dorsal SAS into left and rightcompartments. Throughout the length,there are many unexplained, redundant,nonbranching, beaded, thicker roguestrands. All of these strands differ incharacter from the right-angle fiberarrangement of the denticulate ligament,the 2 leaves of which are often separatedto form segmental longitudinal tunnels.42

Intermittently, they become tangentiallyadherent to the arachnoid membrane. Inthe thoracic region, these trabeculaeform relatively fenestrated membranesrunning obliquely anteroinferiorly incorrespondence to the nerve roots,forming slanting compartments.58 In thelumbar region, these root septa divideinto trabeculae that become progressivelyscant toward the cauda equina and alongits course. Throughout the cauda equina,strands are haphazardly arrangedconnecting the roots and supportingblood vessels.42,58 Parkinson42 found noevidence of change in the number ortype of connection with age.The spinal SAT give shape to tubular

arachnoid sheaths for each nerve root andfor the spinal cord.59 Fila radicularia, thenerve rootlets for each dermatome, are

joined to each other by strands andwebs. The trabecular arachnoid of thespine restricts nerve root movement to adefinite extent, holding each root in itsposition within the dural sac and inrelation to other nerve roots.59 As theventral roots of the spinal nerves traversethe ventral part of the SAS, theirfilaments are hinged to each other andto the ligamentum denticulatum by thedelicate trabecular connective tissue.58

Functions of SATMechanical Properties. According to Killeret al.,40 SAT could play more of a filler rolerather than a support role. Otherreports40,60-64 state that SAT seem to beimportant as mechanical pillars betweenthe pia and arachnoid membranes,damping and constraining the movementof the brain relative to the skull, andthereby possibly affecting traumatic braininjuries. The random three-dimensionalredundant structure of the walls is resil-ient and can lose a few elements withoutfailure under severe conditions such astrauma. In such conditions, the stress isredistributed among the remainingelements of its structure.15,60

A model described by Scott et al.64

suggests that the PAC, which includes the

arachnoid membrane, arachnoidtrabeculae, subarachnoid vasculature, andpia membrane, has a significant effect onbrain biomechanics and increases thelocal variability of stress along the brain.This study, carried out using complexfinite element models of the immaturepiglet brain to identify changes in corticalstress distribution, showed thatincorporating the regional variability ofPAC substructures substantially alteredthe distribution of the main stress on thecortical surface of the brain. This findingshows that despite the small volumetriccontribution of the PAC to the intracranialspace, the microstructural variability has aconsiderable effect on brain mechanicsduring head rotation, thereby contributingsignificantly to brain deformation. Thedata suggested that this regionalvariability of PAC substructures could alsoinfluence localized predictions ofintracranial hemorrhage.64

Role in CSF Flow. The curtainlike structureof the SAT stretched across the SAS hasholes through which CSF flows (Figure 7).This feature could play a part in the CSFdynamics between the SAS of the opticnerve and the chiasmal cistern andcontribute to understanding of thepathophysiology of asymmetric andunilateral papilledema.40,41 Changes intheir structure after trauma or hemorrhagecould in principle contribute toposttraumatic and posthemorrhagichydrocephalus. Alterations in CSF flowvelocities have been noted in the spinalSAS near arachnoid adhesions.18,65 Severalcomputational fluid dynamicsebasedstudies have indicated the possibleimportance of SAT in CSF solute transportand pressures. Stockman66 found that SASmicroanatomy increased CSF flow mixingbut had a relatively small effect on overallCSF velocity profiles. Tangen et al.67 foundthat SAT drastically affected solutetransport within the SAS. Gupta et al.68,69

implemented a computational fluiddynamics model that included anisotropicpermeability within the cortical SAS causedby pillar-shaped SAT.

Role After Hemorrhage. In subarachnoidhemorrhage (SAH), SAT as collagenbundles in the SAS are considered tohave a role in activating the Hagemanfactor in the coagulation system.70,71

Figure 5. Spinal meninges and subarachnoid space. A view of the cut end ofthe spinal cord from dog (SPC) shows the pia mater (PM) lying directly uponthe surface of the cord. The arachnoid trabeculae (AT), continuous with thepia, extend to the arachnoid mater (AM) and to an artery (A) above. Theseparation of the arachnoid mater from the thick dura mater (DM) is anartifact of preparation. The subarachnoid space (SAS) separates thearachnoid from the pia. Original magnification �140.39


LITERATURE REVIEW




Platelets are also believed to be activatedby trabeculae, as well as by thrombinduring SAH.70,71

Role in Formation of Chronic SubduralHematomas. Chronic subdural hematomas(CSDHs) usually occur after a head traumain children, and without trauma in thealcoholic population and in the elderly (>65years) as a result of cerebral atrophy anddegeneration when there is adequate sub-dural space.72,73 SAT may contribute toposttraumatic CSDH or hygromas possiblyby tears in minor vessels supplying thearachnoid, as well as tears in the arachnoidcaused by traction of the trabeculae.74-77 Thetrabeculae in the SAS are more condensedcompared with the subdural space,contributing more to the delicate nature ofbridging veins. In trauma, the tinny fragilewalls of these bridging veins, the

organization of collagen fibers, and theabsence of strengthening trabeculae lead toseparation of the dural border cell (DBC)layer and tearing of bridging veins, resultingin bleeding and hematoma formation.74,78

In elderly patients with age-adequate ce-rebral atrophy, a negative pressure is pro-duced within the cranium as well, as thedistance from the skull to the cerebral cortexbecomes longer.74 The bridging veins arestretched on the atrophied hemisphere andmay become torn even by a minorunnoticed nontraumatic acceleration-deacceleration injury.74,75 If the distancesurpasses the length of SAT, it causes theseparation of the DBC layer, forming a hy-pothetical subdural space inwhich the bloodfrom the bleeding bridging veins is accu-mulated.75 Cranial morphology and thedegree of cerebral atrophy are the 2 actorsthat determine the force pulling the SAT

that leads to the separation of the DBClayer.75 Intracranial hypotension caused byCSF leakage and coagulopathies can alsolead to CSDH in the same manner.74,75,79

Surgical Significance of SATArachnoid membranes, including LM, areof paramount surgical importance and arekey landmarks in microsurgical proced-ures.80-82 These structures help to delin-eate the contour of the lesions, henceprotecting nearby brain structures. Never-theless, neurosurgeons should always payparticular attention to the topography ofthe cisterns and associated arachnoidaladhesions and trabeculae in microsurgicalapproaches to preclude injury to thesurrounding neurovascular structures.Furthermore, the trabecular membranesare structured in a compartmental formthat can limit the spread of blood (e.g.,from a ruptured aneurysm) to other cis-terns by allowing the injury to remainlocalized by observing the blood-filledcistern.80,83-85

Although Yasargil46,86,87 provided adetailed description of the subarachnoidcistern, the compartmental trabecularmembranes remain to be described. Vinaset al.88-90 were the first to describe themicrosurgical anatomy of the compart-mental SAT and their surgical significancein detail. These investigators noted thatthe SAS is lined by trabecular membranes,extending from the arachnoid mater to thepia mater.88-90 They also noticed that incertain areas, trabecular membranes formdense networks that resemble an authentictrue membrane.88-90 Yasargil (1984) andVinas (1994) also reported that these SATdivide the SAS into compartments calledcisterns.46,89 According to Yasargilet al.,46,86,87 these SAT networks hold asignificant microsurgical importancebecause they provide physical support tothe arteries, veins, and nerves that passwithin and through them. However, thewalls of the cisterns direct the flow of CSFthrough openings of various sizes.88-90

These membranes help to protect theentire SAS from collapse during rupture ora surgical approach to a cistern with theconsequent loss of CSF.85,87,89 However, incertain situations such as SAH or bacterialmeningitis, the flow of fluid throughvarious cisterns can be retarded orprevented.88-90

Figure 6. Scanning electron microscopy appearance of the subarachnoid space in the bulbar segment.(A) Overview of the subarachnoid space showing the complex network of trabeculae. The arrowspoint to veillike cytoplasmic extensions between adjacent trabeculae (bar ¼ 150 mm). (B, C) Delicatesubarachnoid space network formed by branching trabeculae (bar ¼ 50 mm). The arrow points to atrabeculum with a blood vessel. Note again the veillike cytoplasmic extensions connecting adjacenttrabeculae (bar ¼ 2 mm). Surface of trabeculae covered by flattened cells with distinct intercellularclefts and fenestrations (bar ¼ 0.2 mm).41


LITERATURE REVIEW



Microsurgical procedures should be per-formed with great care and the trabeculaepulled as lightly as possible because of theirrelationship to neurovascular structures88-90

(see Video 1). Vinas et al.88-90 examinedthe relationship between SAT found insupratentorial and infratentorial levels andat the levels of tentorium to theircorresponding blood vesselsand cranial nerves. Accordingto the data available in theliterature, the variations ofthe subarachnoid trabecularmembrane and subarachnoidcisterns are summarized inTables 1 and 2.88-94

LM is an important anatomic landmarkin the approach to the parasellar andpremesencephalic and prepontineareas.80,88-90,95-97 Understanding oftrabecular membranes, including the LMand its relation to the surroundingsstructures, which can be determined bypreoperative imaging, can help surgeonsto plan the route of access, improveexposure, and minimize injuries.The DL of this membrane has significant

importance in surgical approaches to thesellar and parasellar region and divides thecisterns of the skull base into pre-Liliequistand post-Liliequist groups.54,55,96,98 TheML has less surgical importance than doesthe DL.54,95 The ML separates the supra-tentorial from infratentorial cisterns.54,87,97

In perimesencephalic lesions, such asdiaphragm sellae meningiomas, andtrigeminal neuromas, the ML can be pre-served by displacing upward and can

provide a safe and clear surgical plane foroperating on these tumors, if it is followedclearly.54,55,96,98

DISCUSSION

Previous studies have sought to describe themeninges and their roles in brain and spinalcord function and stability. Comparatively

little attention has been given tothe SAT and their role. Yasargilmade ground-breaking efforts indescribing the topographicanatomy of subarachnoid cis-terns and their importance incerebrovascular and skull base

surgery.46,86,89 SAT were also mentioned aspart of these subarachnoid cisterns but theirstructure and role have not been furtherdelineated. In recent years, researchers havedescribed SAT anatomy and variations in thecentral nervous system.11-13,20,29-38,40-81,99

SAT have mostly been seen as part of thePAC. In recent years, they have attractedincreasing interest. Their role has evolvedfrom being a filler of the SAS into support-ing pillars. This role immediately puts themat the center for balancing intracranial andintraspinal biomechanics, stabilizing neuro-vascular structures such as cranial nerves,arteries, and veins in the arachnoid cisternsand also affecting CSF flow, thereby givingthem surgical significance.

The Role of SAT as Supporting Structuresand Interaction with Intracranial PressureDuring microsurgery, SAT maintainthe SAS as a firm open CSF-filled

compartment. Dissection within the sub-arachnoid cisterns depends on sectioningof the SAT. An interesting model devel-oped by Scott et al.64 implied that changesin the density of SAT could affect the localbiomechanical properties of the brain,making specific regions prone totraumatic bleeding. Studies are underway measuring the biomechanicalproperties of the SAT and their potentialalterations during different CNS diseases.Although the SAT and arachnoid mem-

brane act as a support structure, they arealso held in place by intracranial pressurewithin the CSF system. Alterations inintracranial CSF pressure can affect theSAT, arachnoid membranes, and CSFspace geometries. For example, post mor-tem, the arachnoid membrane quickly de-laminates from the dura and collapses ontop of the cortical surface as a result of lossof intracranial pressure concomitant withCSF absorption into the dural venous si-nuses as venous pressure decreases. Thus,postmortem visualization of SAT is difficultbecause the layers of tissue and fibersbecome relatively tightly cupped around thebrain. The cortical SAS changes sodramatically that the cortical CSF normallyenveloping the brain is nearly nonexistent.This situation can make anatomic dissec-tion and study of the SAT and relatedstructures challenging and drastically altersstudy of the normal CSF compartmentalvolumes and geometry. Similarly, duringsurgical opening of the arachnoid mem-brane, CSF pressures are altered and canthereby also affect the normal CSF spacegeometry and volumes. Delamination ofthe arachnoid membrane from the duraand leakage of CSF into this region canresult in formation of arachnoid cysts andother cavities. The interaction of CSF flowand pressures can lead to alterations inarachnoid cyst volume.

The Relationship Between the Number ofSAT and Propensity for Cerebral TraumaAs Scott et al. suggested in their numericmodeling studies discussed in detailearlier, more numerous SAT could in-crease the likelihood of injury to the brain.Increased SAT can increase surfacestresses on the brain, leading to a greaterpropensity for injury to the delicate braintissue and cortical draining veins. Here,there is a huge gap of knowledge thatneeds to be addressed in future research.

Figure 7. A closer look at the three-dimensional redundant structure of the subarachnoid trabeculae.The curtainlike walls have holes in them through which cerebrospinal fluid (CSF) can flow.

Video available atWORLDNEUROSURGERY.org


LITERATURE REVIEW




Potential Role of SAT in Hydrocephalusand Related DisordersUnderstanding their anatomy, along withfurther understanding of CSF dynamics,sheds new light on potential functions ofthe SAT. It is not unrealistic to assumethat thickening of the SAT after trauma orespecially SAH could be a cofactor in thedevelopment of communicating hydro-cephalus. For example, a local increase inSAT distribution could alter the pulse-damping characteristics of the intracra-nial cavity and/or flow dynamics,21,24,100

thereby affecting interstitial fluid trans-port within the CNS tissues.69,101-103 If thisprocess could be shown then the surgicalliterature would need to reform its termi-nology of communicating hydrocephalusto micro-obstructive hydrocephalus if hy-pertrophied SAH proved to be the cause.Other recent work has indicated a possible

role of CSF pulse-timing along the spinein syringomyelia.104-107 The elongated SATstructure and integral fluid-solid connec-tion to the delicate tissue surface couldalso contribute via the cellular mechano-sensitivity of CNS tissues.108-110

Surgical Importance of SATThe role of SAT in maintaining the neu-rovascular structures within the SAS hasbeen extensively outlined in this study.Retractorless microneurosurgery hasemerged as an important aspect of mod-ern safe neurosurgery. Cautious sectioningof the SAT within the SAS during surgeryallows the neurosurgeon not only tomobilize the cranial nerves, arteries, andveins within the subarachnoid cisterns andto protect them but also to mobilize thebrain easily with no need for retraction.Hence, access to areas that previously

needed retraction would be facilitated bycareful sharp dissection of the SAT, andwithout retraction. The emergence ofretractionless microneurosurgery, and theimportance of neurovascular structureswithin the subarachnoid cisterns and thepotential role of SAT, are all reasonsenough to extend much-needed basic andclinical research to these previously over-looked but important structures.

CONCLUSIONS

SAT are delicate thin mesenchymal col-umns of collagen-reinforced materialstretching between the arachnoid and piamembranes and appear to be significant forthe stability of the SAS, the protection of thecranial nerves, arteries and vessels withinthe subarachnoid cisterns, the stability ofthe brain within the SAS, and potentially

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

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 Chiasmatic cistern Basilar cistern Interpeduncular cistern

Lamina terminalis cistern Cisterna magna Quadrigeminal cistern

Pericallosal cistern Supra-cerebellar cistern Superior cerebellar cistern

Velum interpositum cistern


LITERATURE REVIEW



CSF flow, because of their redundant three-dimensional structure. Understanding theiranatomy and function could be crucial forestablishing a new understanding of theevolution of hydrocephalus. Carefuldissection seems to be a crucial aspect ofmodern surgical techniques for safe retrac-torless neurosurgery. Specific biomechan-ical studies are needed to understand theirphysiologic significance and their potentialcausative or reactive role in different con-ditions of the brain and spinal cord.

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Conflict of interest statement: M.M.M.: Haag-Streitconsultant, Depuy Synthes, American Surgical Company;S.A.F.: SBMT-Haag-Streit Skull Base fellowship grant;M.A.T.: Stryker Neurovascular consultant; B.A.M.: ResearchFunding from Alcyone Lifesciences and VoyagerTherapeutics.

Received 6 October 2017; accepted 8 December 2017

Citation: World Neurosurg. (2018) 111:279-290.https://doi.org/10.1016/j.wneu.2017.12.041

Journal homepage: www.WORLDNEUROSURGERY.org

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https://doi.org/10.1115/1.4034657

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subarachnoid trabeculae: a comprehensive review of their

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