of the Spinal Meninges


Fig. 1

Embryo at 27 days post-conception , stage 12, transverse section, hematoxylin and eosin staining. The neural tube is surrounded by a mesenchyme without meningeal differentiation. Courtesy of Pr P. Dechelotte


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Fig. 2

Embryo at 37 days post-conception , stage 16, transverse section at thoracic level, toluidine blue. The pia mater has differentiated in the form of a thin cell layer particularly at the ventral aspect of the spinal cord. All around this, the mesenchyme has transformed into a loose reticular tissue evoking the arachnoid mater. The dura mater is still absent. Courtesy of Pr P. Dechelotte


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Fig. 3

Embryo at 48 days post-conception, stage 19, sagittal section, hematoxylin and eosin. The choroid plexuses have differentiated , the subarachnoid spaces surround the neuraxis particularly at its cranial part. The spinal cord, coated by the dura mater, occupies the whole length of the vertebral canal. Courtesy of Pr P. Dechelotte


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Fig. 4

Embryo at 50 days post-conception , stage 20, sagittal section, hematoxylin and eosin. The spinal cord still occupies the whole length of the vertebral canal. The subarachnoid spaces develop ventrally while the dura mater thickens. Courtesy of Pr P. Dechelotte


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Fig. 5

Embryo at 54 days post-conception , sagittal section, hematoxylin and eosin. The pia mater and the subarachnoid spaces are now clearly individualized. The dura mater lines the arachnoid mater of the spinal cord and the nerve roots, but still cannot be distinguished laterally from the perichondrium of the vertebra. Courtesy of Pr P. Dechelotte


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Fig. 6

Embryo at 27 weeks post-conception . Transverse section of the spinal cord with its meningeal coverings, hematoxylin and eosin. Meningeal structures are present in a form similar to their adult presentation, but subarachnoid spaces are still not fully developed. The linea splendens has differentiated. Courtesy of Pr P. Dechelotte



Before the 11th week of gestation the spinal cord fills the full width of the vertebral canal and extends caudally to the coccygeal region (Figs. 3 and 4). Thereafter tail structures regress progressively and the spinal cord within its meningeal sheath contracts into the filum terminale and the coccygeal ligament. The spine growing more rapidly than the spinal cord, the caudal end of the conus terminalis lies at the base of the sacrum (S1) by the end of the 5th month of gestation and at the level of the 3rd lumbar vertebra (L3) by full term [14]. About 2 months after birth the conus terminalis takes its place at the adult level between L1 and L2 [15]. Then the dural sac below the conus terminalis contains lumbosacral nerves forming the cauda equina, the filum terminale, and their vascular supply in their leptomeningeal coating. Outside, the epidural adipose tissue separates the dural sac from the walls of the vertebral canal. Laterally the meninges encase spinal nerve roots by two separate sheaths (Fig. 7).

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Fig. 7

Embryo at 27 weeks post-conception. Cross section of spinal nerve roots. Hematoxylin and eosin. Ventral and dorsal nerve roots are clothed by separate dural coverings. Note the large subarachnoid sleeve around ventral nerve root. Courtesy of Pr P. Dechelotte


Descriptive and Topographical Anatomy of the Spinal Meninges in Adults


The spinal meninges consist of three concentric layers that envelop the spinal cord, the filum terminale, and nerve roots.


The Dura Mater


Morphology


The dura mater is the thick superficial meningeal layer or pachymeninx. It forms a white, inelastic but deformable sheath that grossly follows the contour of the spinal cord, the filum terminale, and nerve roots. Its thickness varies with individuals and decreases over a lifetime ranging from a thin transparent membrane to a thick pearly wall. The spinal dura corresponds to the inner, meningeal layer of the cranial dura with which it is continuous at the foramen magnum . Ventrally, the meningeal layer separates from the periosteal layer at the 3rd cervical vertebral body.


The dural sac begins cranially at the foramen magnum (Fig. 8) and contracts caudally at the junction between first and second sacral vertebral bodies by a cul-de-sac which extends caudally into the filum of the dura mater or coccygeal ligament. The filum of the dura mater is a thin tubular formation 5 cm long that encases the filum terminale and terminates through fibrous processes at the periosteum of the dorsal aspect of the coccyx (Figs. 9 and 10). At both its cranial and caudal ends the spinal dura fuses with the periosteum of the vertebral canal. Laterally, the dura encases dorsal and ventral nerve roots in separate tubular sheaths (Figs. 11 and 12).

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Fig. 8

Upper part of spinal meninges after opening of the foramen magnum and the posterior cranial fossa, and laminectomy of C1 C2, schematic drawing. Apices of ligamenta denticulata are inserted on the dura mater in the intervals between nerve root exits. The first ligamentum denticulatum is interposed between the first cervical nerve and the accessory nerve dorsally, and the vertebral artery ventrally. M. Chalus and L Sakka


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Fig. 9

Cauda equina and filum terminale after opening of the dura mater, dorsal view, schematic drawing. The dural cul-de-sac is located at the level of S1–S2, the filum of the dura mater is inserted on the first coccygeal piece, epidural space. JP Monnet


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Fig. 10

Leptomeningeal coverings of the conus terminalis and the cauda equina, dorsal view after laminectomy of L1–L2 and opening of the dura mater. Cranially (left) the arachnoid mater has been opened to display perimedullary vessels. Perimedullary vessels are covered by the pia mater. The superficial arachnoid layer can be easily dissected from the dura mater


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Fig. 11

Nerve roots in their meningeal sheath in the intervertebral foramen, schematic drawing. JP Monnet


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Fig. 12

Lumbar nerve root exit through opening of the dura mater


Dural ultrastructure is made of three distinct layers : an outermost fibroelastic layer, a middle fibrous layer, and an innermost cellular layer. The abundance of elastic fibers and the helicoidal arrangement of collagen bundles provide the flexibility and the resistance of the dural sheath that protect the spinal cord during movements [16].


The Fixation-Points of the Spinal Dura Mater


Cranially, the spinal dura tightly adheres to the periosteum of the foramen magnum where it continues the outer layer of the cranial dura. Laterally, the spinal dura covers the nerve roots by two separate sheaths that blend into one at the lateral side of the spinal ganglion, where it gives rise to the epineurium (Fig. 11). The dura is attached to the periosteum of the intervertebral foramina by the fibrous opercula of Forestier that constitute its lateral fixation-points. Dorsally, the spinal dura adheres to the posterior arch of the atlas and the axis and to the posterior atlanto-occipital membrane. Ventrally, the dura adheres to the 2nd and 3rd cervical bodies and to the dorsal longitudinal ligament, more particularly at cervical and lumbar segments. At these levels, both dorsally concave and mobile, ventral attachments hold the spinal cord at the inside of the spine curve during movements. Dural attachments to the dorsal longitudinal ligament are provided by fibrous strands which constitute the ventral ligament of the spinal dura mater. They strengthen caudally from the intervertebral disc L4–L5 to the vertebral body of S5 to form the sacrodural ligament of Trolard. At this level, dural attachments are made of arcuate fibrous formations spanning adjacent vertebral bodies by their endings and adhering to the dural sac by their convexity. Caudally, the filum of the dura mater is attached to the periosteum of the dorsal aspect of the first coccygeal segment (Fig. 13).

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Fig. 13

Attachment of the dural sac and the filum of the dura mater to the ventral wall of the vertebral canal by the ligament of Trolard after sagittal section of the lumbosacral junction, schematic drawing. M Chalus and L Sakka


Vascularization


Arteries

The spinal dura is poorly vascularized. Arterial supply is performed by thin branches of radicular arteries whose diameter does not exceed 0.5 mm. Dorsally a dense anastomotic network supplied by two cranio-caudal arterial axes contrasts with a loose ventral anastomotic network supplied by a ventro-median arterial axis. This disposition resembles the spinal cord arterial supply. This arterial network displays a metameric disposition with numerous anastomoses. At the dorsal aspect of the thoracic segment, spiral arteries and tufts of capillaries bulge into the epidural space. The significance of these formations is not understood [17].


Veins

The physiology of the connections between dural and spinal cord venous drainages remains unclear, anatomic observations and interventional neuroradiology providing conflicting data. There are generally two veins for one dural artery. At the cervical level they form a meshwork of large venous sinuses that communicate cranially with the basilar plexus and take part in the encephalic venous drainage. Anatomic studies describe radicular veins that collect from both the veins of the dura and the veins of the spinal cord, leave the vertebral canal by intervertebral foramina and drain into the internal vertebral plexus of the epidural space. Valves in radicular veins located just before they pass through the dura may prevent the blood from flowing back to the spinal cord. These can be regarded as a protective mechanism of the spinal cord in situations of hypertension in the vertebral venous system [17]. Reversely, angiographic procedures do not show communications between perimedullary and epidural veins. Perimedullary veins are described as draining upwards through the foramen magnum into the inferior cerebellar veins and the dural sinuses of the posterior cranial fossa. These reports are provided by procedures requiring the patient to be in a supine position. One can assume that the distribution of the venous return may be different in upright positions or during exercise.


Lymphatics

The lymphatic drainage of the spinal dura remains poorly understood. Lymphatic vessels were first described following experiments of ink injections into the ventricular or subarachnoid spaces of mammals. They were described as arising near the lateral points of attachment of the ligamenta denticulata, near lumbar vertebral bodies or around subarachnoid recesses [18]. They drain into paravertebral lymph nodes, the thoracic lymphatics into the nodes of the posterior mediastinum, and the lumbo-sacral lymphatics into the nodes of the posterior abdominal wall between psoas major muscles [19].


In animal models the lymphatic system has been demonstrated to take part in the absorption of cerebrospinal fluid [20]. In humans the participation of the spinal lymphatic pathway remains unknown under physiological conditions but might be significant in the upright position and during exercise. This function could be especially active in neonates whose arachnoid villi become fully functional only after the age of 18 months, and in the elderly where absorptive capacity of cranial arachnoid granulations gradually decreases.


Innervation


The ventral aspect of the spinal dura is innervated by a dense plexus supplied by sinu-vertebral nerves, the nerve plexus of the posterior longitudinal ligament and the perivascular plexus of radicular arteries. The sinu-vertebral nerve is a ventral branch of the spinal nerve (Fig. 11). It runs cranially and medially between the dorsal longitudinal ligament and the annulus fibrosus ventrally and the ventral aspect of the dura dorsally. These three structures are innervated by the sinu-vertebral nerve [2124].


The dorsal aspect of the spinal dura is poorly innervated by nerves coming from the ventral dural nerve plexus in the intervals between nerve roots. They do not reach the median part of the dorsal dura. The lack of innervation of the median dorsal dura explains why lumbar punctures are not painful while traversing the dura mater [22].


Dural nerves are non-myelinated fibers involved in vasomotricity and nociception [22, 25]. The efficacy of epidural blocks performed in anesthesiology could be at least partially related to an action on dural nerves. The innervation of the dorsal longitudinal ligament and the dorsal part of the annulus fibrosus by sinu-vertebral nerves through free endings has suggested their involvement in low back pain syndromes [26, 27] and might explain the efficiency of periradicular infiltrations with anti-inflammatory drugs in this indication.


The Relationships of the Dura Mater with the Leptomeninges and the Spinal Nerves


The inner aspect of the spinal dura is covered by the outer arachnoid layer. Laterally, as the nerve roots pass through the dura mater, the arachnoid mater constitutes subarachnoid recesses around spinal nerves (Figs. 7 and 11). Ventral and dorsal nerve roots traverse the dura by two distinct openings and run toward the intervertebral foramen within two distinct dural sheaths. The roots of the first cervical nerve and the vertebral artery traverse the dura through the same opening (Fig. 8). In the intervertebral foramen nerve roots merge into a spinal nerve covered by a unique dural sheath. The sinu-vertebral nerve runs at the ventral aspect of the spinal nerve, outside the dural sheath, among the venous plexus of the intervertebral foramen (Fig. 11). The spinal nerve and the radicular artery running at its ventral aspect are disposed centrally in the cellulo-adipose tissue of the foramen surrounded by the epidural intervertebral venous plexus. The intervertebral foramen is closed laterally by the fibrous operculum of Forestier (Fig. 11). The area between the fibrous operculum and the nerve dural sheath is the epidural space of the foramen.


The Arachnoid Mater


The arachnoid mater is a thin transparent membrane enveloping the spinal cord, nerve roots, perimedullary vessels, and the intradural segment of radicular vessels (Figs. 6, 10, 14, 15, and 16). The arachnoid is usually described as a unique thick layer lining the inner aspect of the dura mater and connected to the pia mater by a network of delicate connective trabeculae . Ultrastructural studies using electron microscope rather describe a two-layer structure with a superficial barrier cell layer lining the dura mater and a deep reticular cell layer made of interweaved trabecular cells connected to the pia mater [16]. The superficial layer is composed of tightly packed cells connected with one another by numerous tight junctions suggesting a role as a meningeal barrier between the cerebrospinal fluid of the subarachnoid space and the blood circulation of the dura [16, 29]. The superficial barrier cell layer is attached to the dura mater by collagenous fibers so that there is no subdural space, but it can be easily dissected from it without opening the subarachnoid space.

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Fig. 14

Cauda equina, CT-scan after intrathecal injection of iodine contrast, oblique section. Arachnoid recesses are usually located medially from the caudal border of the pedicles. Courtesy of Dr J Gabrillargues


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Fig. 15

Subarachnoid space of the cauda equina after opening of the superficial layer of the arachnoid. Filum terminale and nerve roots are connected to one another by fine arachnoid trabeculae


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Fig. 16

Spinal leptomeninges. The arachnoid mater and the pia mater are continuous with each other as well as subarachnoid and parenchymal perivascular spaces. The collagenous core of ligamentum denticulatum merges with the subpial space medially and the inner aspect of the dura mater laterally (Modified after Nicholas and Weller [28])


According to this description, the subarachnoid space, filled with the extra-axial cerebrospinal fluid, takes the room between the superficial barrier cell layer and the pia mater, traversed by the arachnoid trabeculae of the reticular cell layer. On traversing the arachnoid mater blood vessels and nerve roots are sheathed by extensions of the reticular cell layer. Cranially, the subarachnoid space is continuous with the cranial subarachnoid space at the foramen magnum. Around the spinal cord it constitutes the perimedullary space, divided into ventral and dorsal chambers by the ligamenta denticulata (Figs. 8 and 20). In the dorsal chamber, arachnoid trabeculae form a dense network that firmly applies blood vessels against the spinal cord and constitutes medially a sagittal septum, the septum posticum of Schwalbe. An intermediate cell layer interposed between the superficial arachnoid layer and the pia mater to which it is tightly connected, might contribute to this septum [28]. Most developed at the lower cervical and thoracic levels, the septum posticum of Schwalbe connects dorsally to a thickening of the superficial arachnoid layer: the median raphe of Magendie (Fig. 16).


Caudally the subarachnoid space widens into the large lumbosacral terminal cistern that encloses the cauda equina and terminates between the 1st and the 2nd sacral vertebrae. Laterally it follows the nerve roots from the spinal cord to the intervertebral foramina. The two arachnoid layers merge to limit subarachnoid recesses around spinal nerves at the lateral limit of spinal ganglia just before they traverse the fibrous opercula. The abundance of cell debris and activated macrophages in arachnoid recesses [30] where fine lymph vessels have been described to drain into paravertebral lymph nodes [19] suggest the subarachnoid recess as an interface between the central nervous system, the cerebrospinal fluid, and CSF immune defense. There is no specific arachnoid vascularization; the vessels are those of the spinal cord.


Subarachnoid spaces can be precisely explored using CT-scan after intrathecal injection of iodinated contrast medium. MRI visualizes the subarachnoid space by the hypersignal of the cerebrospinal fluid in T2-weighted sequences.


Subarachnoid recesses have relationships with bone structures that constitute the safety landmarks of periradicular infiltrations, procedures commonly performed in anesthesiology and rheumatology (Fig. 14). Inadequate site of puncture can lead to CSF leak, nerve-root damage, or intra-arterial administration. Lateral limits of subarachnoid recesses vary according to vertebral segments and subjects. At cervical levels subarachnoid recesses usually stop at the anterior border of the pedicles. At thoracic and lumbar levels they usually do not extend laterally beyond the caudal border of the upper pedicle. To be safe, the tip of the trocar should remain extraforaminal, that is, outside the lateral recess to avoid intrathecal injection, puncture of a radiculomedullary artery, or a vertebral artery in the cervical segment.


In healthy subjects, the perimedullary space occupies about a third of the cervical vertebral canal in sagittal MRI sections (Fig. 17a, b). In a study including 140 healthy volunteers, the part of the subarachnoid space in the vertebral cervical canal was shown to vary according to sex, body height, and vertebral segment. Its relative anteroposterior diameter decreased from C1 to C6, confirming the lower cervical segments as more specifically exposed to compressive myelopathy. Its relative anteroposterior diameter increased with body height suggesting a lower susceptibility of taller subjects to the risk of cervical cord compression [31]. In clinical practice, the presence of hypersignal on T2-weighted sequence at the ventral or dorsal aspect of the cervical cord is a valuable sign for cervical stenosis (Fig. 17c).

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Fig. 17

Sagittal section of the cervico-thoracic spinal cord ; (a) healthy subject, T1 weighted sequence; (b) healthy subject, T2 weighted sequence; (c) cervical canal stenosis with myelopathy, T2 weighted sequence. Perimedullary space appears as a hypersignal in T2-weighted sequence and hyposignal in T1-weighted sequence. Epidural fat appears as a hypersignal in T1 and T2-weighted sequences. Note the position of the spinal cord at the concavity of spine curves. Courtesy of Dr E. Chabert


Below the 2nd lumbar vertebra the subarachnoid space constitutes the lumbosacral terminal cistern around the cauda equina visualized by MRI as a large hypersignal on T2-weighted sequences. At this level the particularly developed epidural fat gives a hypersignal on both T1 and T2-weighted sequences (Fig. 18). Assessment of both subarachnoid space and epidural fat on T2-weighted sequences are essential in the diagnosis of lumbar canal stenosis, either congenital or acquired (Fig. 19). In the acquired syndrome, the stenosis of the vertebral canal and/or lateral recesses occurs secondary to degenerative changes involving intervertebral disc bulging, spondylolisthesis, hypertrophy of facet joints, and/or hypertrophy of the ligamentum flavum. Patients usually complain with low back pain, radicular pain, and a typical neurogenic claudication. The symptoms of neurogenic claudication typically described by patients consist of fatigue, heaviness or weakness in the legs without radicular topography, generated by standing upright or walking and relieved by sitting or flexion of the spine. The postural nature of symptoms is related to the variations in the size of the vertebral canal according to spine curvature changes. The symptoms are triggered by extension of the spine which decreases the anteroposterior diameter of the canal and relieved by flexion of the spine which increases the anteroposterior diameter [32, 33]. The pathophysiology of this affection remains unclear since anatomic stenosis of the canal is often observed in asymptomatic subjects. The signs reported by patients evoke a global effect on the cauda equina. While radicular symptoms can be explained by a direct compression of nerve roots or their vascular supply by degenerative changes, the impact of postural changes on neurogenic claudication favors a disturbance in the cerebrospinal fluid dynamics. One can assume that symptoms settle when CSF and venous pressures overcome the blood pressure in the cauda equina arterial supply.

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Fig. 18

Lumbosacral terminal cistern in a healthy subject; (a) T1 weighted sequence; (b) T2 weighted sequence. The cerebrospinal fluid of the lumbosacral terminal cistern appears as a hypersignal in T2-weighted sequence and a hyposignal in T1-weighted sequence. Epidural fat appears as a hypersignal in T1 and T2-weighted sequences. In this healthy subject, the conus terminalis is located at the caudal part of L1. Courtesy of Dr E. Chabert


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Fig. 19

Acquired lumbar canal stenosis ; (a) T1 weighted sequence, sagittal section; (b) T2 weighted sequence, sagittal section; (c) T2 weighted sequence, transverse section. In this case, the canal stenosis is related to intervertebral disc bulging and hypertrophy of facet joints. The stenosis affects both the lumbosacral terminal cistern and epidural fat. Courtesy of Dr E. Chabert


Around spinal nerve roots the arachnoid mater has been described to differentiate into arachnoid villi. Morphological similarities with cranial granulations and their relationships with epidural veins have suggested their involvement in CSF reabsorption [34, 35]. Usually located at or medially to subarachnoid recesses, they could be more frequent in thoracic or lumbar regions. In animal models, spinal arachnoid villi have been assessed to be responsible for about 25% of CSF drainage [36, 37]. In humans, their contribution in CSF absorption has never been assessed but might be effective in the first year of life and later on in upright posture or during exercise [38].


The Pia Mater


The spinal pia mater is a thin areolar tissue closely adhering to the glia limitans (Figs. 6 and 16). Cranially the spinal pia mater continues as the cranial pia mater at the foramen magnum. Caudally it encases the filum terminale below the conus terminalis. Classically considered a pial formation, the filum terminale was demonstrated to originate from apoptotic degeneration of the caudal spinal cord [39]. In human fetuses, the filum terminale is constituted of a connective tissue rich in type III collagen with nerve fascicles, blood vessels, ganglion cells, ependymal, glial, and adipose tissues [40]. The same components are found in adults, but connectives fibers are mostly type I collagen, elastin and elaunin fibers longitudinally arranged in a network of transversal type III collagen fibers [41]. The filum terminale appears a bluish, white formation of about 20 cm long and less than 2 mm wide. Its upper part, located inside the dural sac (filum terminale internum), runs down along the lumbosacral terminal cistern among the roots of the cauda equina. Its lower part, located beyond the dural sac (filum terminale externum), is encased by the filum of the dura mater from the lower border of the first sacral vertebra to the dorsal aspect of the first coccygeal piece. Laterally the pia mater follows nerve roots and spinal nerves, fusing with the arachnoid before commencement of the perineurium.


In the ventral fissure of the spinal cord, the pia mater forms the linea splendens, a dense network of fibrous strands that bridge the two walls of the fissure and wrap the ventral spinal artery (Fig. 6).


Laterally the pia mater forms on each side of the spinal cord 20–22 ligamenta denticulata that anchor the spinal cord to the dural sac. Each ligamentum denticulatum is a triangular formation extending from the lateral side of the spinal cord by its base to the inner aspect of the dural sac by its apex, in the intervals between nerve roots (Fig. 20). The first ligamentum denticulatum, located above the first cervical roots, is inserted onto the dura of the medial aspect of the condylar part of the occipital bone (Fig. 8). The vertebral artery runs ventrally and the spinal root of the accessory nerve runs dorsally. The last ligamentum denticulatum is located above the first lumbar nerve. The ligamentum denticulatum is made of a collagenous core which fuses with the inner aspect of the dura mater laterally and merges with the subpial layer medially (Fig. 16). Ligamenta denticulata form incomplete septa that separate the subarachnoid space in ventral and dorsal compartments where the cerebrospinal fluid flows in opposite directions. It probably stabilizes the spinal cord within the subarachnoid space along the movements of the vertebral column [42].

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Apr 25, 2020 | Posted by in ORTHOPEDIC | Comments Off on of the Spinal Meninges
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