The collagenic architecture of human dura mater

Laboratory investigation

Restricted access


Human dura mater is the most external meningeal sheet surrounding the CNS. It provides an efficient protection to intracranial structures and represents the most important site for CSF turnover. Its intrinsic architecture is made up of fibrous tissue including collagenic and elastic fibers that guarantee the maintenance of its biophysical features. The recent technical advances in the repair of dural defects have allowed for the creation of many synthetic and biological grafts. However, no detailed studies on the 3D microscopic disposition of collagenic fibers in dura mater are available. The authors report on the collagenic 3D architecture of normal dura mater highlighting the orientation, disposition in 3 dimensions, and shape of the collagen fibers with respect to the observed layer.


Thirty-two dura mater specimens were collected during cranial decompressive surgical procedures, fixed in 2.5% Karnovsky solution, and digested in 1 N NaOH solution. After a routine procedure, the specimens were observed using a scanning electron microscope.


The authors distinguished the following 5 layers in the fibrous dura mater of varying thicknesses, orientation, and structures: bone surface, external median, vascular, internal median, and arachnoid layers.


The description of the ultrastructural 3D organization of the different layers of dura mater will give us more information for the creation of synthetic grafts that are as similar as possible to normal dura mater. This description will be also related to the study of the neoplastic invasion.

Article Information

Address correspondence to: Marina Protasoni, M.D., Ph.D., Department of Human Morphology, University of Insubria, Via Monte Generoso 71, 21100 Varese, Italy. email:

Please include this information when citing this paper: published online February 4, 2011; DOI: 10.3171/2010.12.JNS101732.

© AANS, except where prohibited by US copyright law.



  • View in gallery

    Upper: Transverse section of the dura mater seen by scanning electron microscopy. At low magnification, it is possible to distinguish 5 different layers depending on the orientation with respect to the bone. The most external is in direct contact with the bone and is called the bone surface layer (α). The fibrous dura recognized by the anatomists as the median layer comprises the external median layer (β), the vascular layer (γ), and the internal median layer (δ). The most internal layer in direct contact with dural border cells and facing the arachnoid mater is called the arachnoid layer (ε). Lower: The scheme is divided into 2 parts. The first (a) represents each layer described in the upper panel and is examined in the study as follows: the bone surface layer (α), the external median layer (β), the vascular layer (γ), the internal median layer (δ), and the arachnoid layer (ε). The bone of the calvaria (x), the arachnoid membrane (y), and the brain cortex (k) are also shown. The second part (b) represents a single specimen divided into 3 lesser specimens for the study: the first (1) is the specimen used to study the bone surface layer, the second (2) to study the arachnoid layer, and the third (3) to study the thickness of the dura mater.

  • View in gallery

    A: Bone surface layer. At low magnification, it is possible to observe a continuous sheet of collagen fibers with few ridges on the surface. Among these, the deepest correspond to the meningeal vessel imprint (asterisk). B: At a higher magnification, the bone surface layer is clearly distinguished in its thickness. C: At high magnification, the distribution of collagen fibers of the bone surface layer becomes clearly visible and one can easily distinguish the two superimposed layers. The upper layer is made of interlaced collagen fibers that form a disorganized thin net, and the lower layer is made up of bundles of collagen fibers, most of which are oriented in the same direction. D: At very high magnification, it is possible to distinguish the stripes of collagen fibers at 67 nm and better visualize the disposition of the 2 superimposed layers. In particular, it is possible to observe some collagen fibers running between and connecting H-shaped collagen bundles (asterisk). E: Higher magnification of B. The transverse section of the bone surface layer at a high magnification is easily distinguishable from the external median layer underneath. It is also possible to visualize the shape of collagen bundles lying between the external median and bone surface layers (arrow).

  • View in gallery

    Bone surface layer. A: Specialized focal aggregations of disorganized collagen fibers are clearly visible among regularly directed underlying fibers. B: At higher magnification, these fibers reveal a characteristic 180°-angled shape. C: Detail of a collagenic lacuna corresponding to the site occupied by fibroblast under normal conditions. Note the modification of the regular arrangement that is characteristic of the bone surface layer and the gathering of collagen fibers that line the borders of the lacuna (asterisk). Single collagen fibers run from one side to the other, sectioning the empty space (number sign). At the bottom of the hole, collagen bundles with almost the same orientation are visible (ampersand). The lacuna is partially covered by variously interlaced collagenic fibers (section symbol). D: At higher magnification, these fibers appear to be disorganized without any prevalent direction, but they form an interlaced dense net of fibers that, at very high magnification, appear tortuous and angled. E: the fibers' regular 67-nm stripes are clearly distinguished.

  • View in gallery

    Transverse section of the dura mater. The major fibrous collagenic component of the median layers is seen using the 1 N NaOH maceration method and scanning electron microscopy. A: At low magnification, these fibers, depending on their reciprocal direction and arrangements, are clearly subdivided into 3 different layers: the external median layer (β), the vascular layer (γ), and the internal median layer (δ). B: At high magnification, the external median layer is noted to be made of bundles of collagen fibers all oriented in a signal direction. C: A thin interlaced net of collagen fibers is present over these bundles, and some specialized structures seen as collagen bridges extending between and connecting these bundles are visible. D and E: In the transverse section, the vascular layer is characterized by vascular collagenic channels (D) that at high magnification (E) are noted to be composed of fibers arranged in a whorl-like pattern. F: The internal median layer is clearly distinguishable from the upper layer because of the direction of the collagen fibers that appear to be organized in collagen bundles that are all oriented in the same direction.

  • View in gallery

    The arachnoid layer appears to be characterized by a disorganized disposition of collagen bundles (low magnification). Collagen fibers are tortuous and are not oriented in any common direction. A and B: The final effect is a corrugated surface with deep invaginations and furrows. C and D: At higher magnification, small holes, probably due to the signs of a capillary plexus (C), and bundles of spiral collagen fibers (D) are visible.

  • View in gallery

    A and B: Colorimetric analysis of the bone surface layer (A) compared with that of the arachnoidal layer (B). C and D: Graphs demonstrating the predominance of a single direction of collagen fibers in the bone surface layer (C) and the various directions of the collagen fibers visible in the arachnoid layer (D).


  • 1

    Alcolado RWeller ROParrish EPGarrod D: The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol 14:1171988

  • 2

    Barbolt TAOdin MLéger MKangas LHoiste JLiu SH: Biocompatibility evaluation of dura mater substitutes in an animal model. Neurol Res 23:8138202001

  • 3

    Benini ABonar SK: Andreas Vesalius 1514–1564. Spine 21:138813931996

  • 4

    Biroli FFusco MBani GGSignorelli AEsposito Fde Divitiis O: Novel equine collagen-only dural substitute. Neurosurgery 62:3 Suppl 12732742008

  • 5

    Chaplin JMCostantino PDWolpoe MEBederson JBGriffey ESZhang WX: Use of an acellular dermal allograft for dural replacement: an experimental study. Neurosurgery 45:3203271999

  • 6

    Collins RLChristiansen DZazanis GASilver FH: Use of collagen film as a dural substitute: preliminary animal studies. J Biomed Mater Res 25:2672761991

  • 7

    Conegero CIChopard RP: Tridimensional architecture of the collagen element in the arachnoid granulation in humans: a study on scanning electron microscopy. Arq Neuropsiquiatr 61:5615652003

  • 8

    Costantino PDWolpoe MEGovindaraj SChaplin JMSen CCohen M: Human dural replacement with acellular dermis: clinical results and a review of the literature. Head Neck 22:7657712000

  • 9

    Fricke BAndres KHVon Düring M: Nerve fibers innervating the cranial and spinal meninges: morphology of nerve fiber terminals and their structural integration. Microsc Res Tech 53:961052001

  • 10

    Gök AZorludemir SPolat STap OKaya M: Experimental evaluation of peritoneum and pericardium as dural substitutes. Res Exp Med (Berl) 195:31381995

  • 11

    Knopp UChristmann FReusche ESepehrnia A: A new collagen biomatrix of equine origin versus a cadaveric dura graft for the repair of dural defects—a comparative animal experimental study. Acta Neurochir (Wien) 147:8778872005

  • 12

    Laquerriere AYun JTiollier JHemet JTadie M: Experimental evaluation of bilayered human collagen as a dural substitute. J Neurosurg 78:4874911993

  • 13

    Maher COAnderson REMcClelland RLLink MJ: Evaluation of a novel propylene oxide-treated collagen material as a dural substitute. J Neurosurg 99:107010762003

  • 14

    Manelli ASangiorgi SBinaghi ERaspanti M: 3D analysis of SEM images of corrosion casting using adaptive stereo matching. Microsc Res Tech 70:3503542007

  • 15

    Meddings NScott RBullock RFrench DAHide TAGorham SD: Collagen vicryl—a new dural prosthesis. Acta Neurochir (Wien) 117:53581992

  • 16

    Nabeshima SReese TSLandis DMBrightman MW: Junctions in the meninges and marginal glia. J Comp Neurol 164:1271691975

  • 17

    Narotam PKJosé SNathoo NTaylon CVora Y: Collagen matrix (DuraGen) in dural repair: analysis of a new modified technique. Spine 29:286128692004

  • 18

    Narotam PKVan Dellen JRBhoola KRaidoo D: Experimental evaluation of collagen sponge as a dural graft. Br J Neurosurg 7:6356411993

  • 19

    Nordstrom MRWang TDNeel HB III: Dura mater for soft-tissue augmentation. Evaluation in a rabbit model. Arch Otolaryngol Head Neck Surg 119:2082141993

  • 20

    Ohtani O: The maceration technique in scanning electron microscopy of collagen fiber frameworks: its application in the study of human livers. Arch Histol Cytol 55:Suppl2252321992

  • 21

    Ohtani O: Three-dimensional organization of the connective tissue fibers of the human pancreas: a scanning electron microscopic study of NaOH treated-tissues. Arch Histol Jpn 50:5575661987

  • 22

    Ohtani OUshiki TTaguchi TKikuta A: Collagen fibrillar networks as skeletal frameworks: a demonstration by cell-maceration/scanning electron microscope method. Arch Histol Cytol 51:2492611988

  • 23

    Pease DCSchultz RL: Electron microscopy of rat cranial meninges. Am J Anat 102:3013211958

  • 24

    Runza MPietrabissa RMantero SAlbani AQuaglini VContro R: Lumbar dura mater biomechanics: experimental characterization and scanning electron microscopy observations. Anesth Analg 88:131713211999

  • 25

    Sakas DECharnvises KBorges LFZervas NT: Biologically inert synthetic dural substitutes. Appraisal of a medical-grade aliphatic polyurethane and a polysiloxane-carbonate block copolymer. J Neurosurg 73:9369411990

  • 26

    Sangiorgi SManelli ADell'Orbo CCongiu T: A new method for the joint visualization of vascular structures and connective tissues: corrosion casting and 1 N NaOH maceration. Microsc Res Tech 69:9199232006

  • 27

    Sangiorgi SManelli AProtasoni MRonga MRaspanti M: The collagenic structure of human digital skin seen by scanning electron microscopy after Ohtani maceration technique. Ann Anat 187:13222005

  • 28

    Shukla VHayman LALy CFuller GTaber KH: Adult cranial dura I: intrinsic vessels. J Comput Assist Tomogr 26:106910742002

  • 29

    Shukla VHayman LATaber KHFuller GTaber KH: Adult cranial dura II: venous sinuses and their extrameningeal contributions. J Comput Assist Tomogr 27:981022003

  • 30

    Vandenabeele FCreemers JLambrichts I: Ultrastructure of the human spinal arachnoid mater and dura mater. J Anat 189:4174301996

  • 31

    Viñas FCFerris DKupsky WJDujovny M: Evaluation of expanded polytetrafluoroethylene (ePTFE) versus polydioxanone (PDS) for the repair of dura mater defects. Neurol Res 21:2622681999

  • 32

    Warren WLMedary MBDureza CDBellotte JBFlannagan PPOh MY: Dural repair using acellular human dermis: experience with 200 cases: technique assessment. Neurosurgery 46:139113962000

  • 33

    Weller RO: Microscopic morphology and histology of the human meninges. Morphologie 89:22342005




All Time Past Year Past 30 Days
Abstract Views 235 235 44
Full Text Views 351 351 18
PDF Downloads 108 108 10
EPUB Downloads 0 0 0


Google Scholar