The collagenic architecture of human dura mater

Laboratory investigation

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Object

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.

Methods

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.

Results

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.

Conclusions

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: marina.protasoni@uninsubria.it.

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.

Headings

Figures

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    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.

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    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).

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    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.

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    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).

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