Embryology Of Meninges

[Elly Garnand]

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The meninges are membranous layers surrounding the central nervous system. In the head, the meninges lie between the brain and the skull, and interact closely with both during development. The cranial meninges originate from a mesenchymal sheath on the surface of the developing brain, called primary meninx, and undergo differentiation into three layers with distinct histological characteristics: the dura mater, the arachnoid mater, and the pia mater. While genetic regulation of meningeal development is still poorly understood, mouse mutants and other models with meningeal defects have demonstrated the importance of the meninges to normal development of the calvaria and the brain. For the calvaria, the interactions with the meninges are necessary for the progression of calvarial osteogenesis during early development. In later stages, the meninges control the patterning of the skull and the fate of the sutures. For the brain, the meninges regulate diverse processes including cell survival, cell migration, generation of neurons from progenitors, and vascularization. Also, the meninges serve as a stem cell niche for the brain in the postnatal life. Given these important roles of the meninges, further investigation into the molecular mechanisms underlying meningeal development can provide novel insights into the coordinated development of the head.

The adult central nervous system (CNS) is largely encased by three concentric connective layers named dura mater, arachnoid, and pia mater. They constitute a fibrous envelope, which provides for mechanical protection of the nervous system and participates in formation of the blood-brain barrier. The embryogenesis of the meninges varies across vertebrate species. The human meningeal development is still a matter of great controversy. Although comparative embryologic and anatomic studies have demonstrated that main developmental landmarks are conserved among the species, these findings should be cautiously extrapolated to the human embryonic development (1). Detailed studies on the embryogenesis of the meninges in humans by O'Rahilly and Mller in the late 1980s (2) presented the most comprehensive analysis yet on this complex issue. In this chapter I will provide a review of the development of the cranial and spinal human meninges and their correlation with the morphologic aspects of the adult meninges.

Between the ligamentum flavum and the superficial dura mater is the spinal epidural space. This location contains various structures such as adipose tissue, connective tissue, nerves, the internal vertebral venous plexus, and lymphatics. It is a site commonly used for analgesic purposes and is a potential site for infection.[1][2]

The most superficial layer of the meninges is the dura mater. While it has two layers in the cranial segment, the spinal dura mater only has the deep meningeal layer. The periosteal layer, which is the superficial layer of the dura within the calvarium, ends at the foramen magnum, with only the meningeal layer continuing down along the spinal cord.[1] The dura mater is the strongest of the three layers, with some animal studies showing that the thickness of the dura decreases as it descends towards the coccyx.[3] As they make their way out of the vertebral canal, the spinal nerves are coated with dura mater as they exit into the epidural space, creating the epineurium.

The spinal subarachnoid space is located between the arachnoid and pia mater and is filled with CSF. Arachnoid trabeculae extend between these two layers within the subarachnoid space to give the subarachnoid space its characteristic spiderweb appearance. The choroid plexus produces CSF within the brain ventricles, and CSF enters the spinal subarachnoid spaces via the median and lateral apertures. The functions of the CSF include protection and nourishment of the brain and spinal cord.[4] The spinal subarachnoid space, specifically the lumbar cistern inferior to the conus medullaris, has clinical significance in diagnosing meningitis, as it is the site of lumbar puncture.

The spinal pia mater is the deepest layer of the meninges and is directly attached to the surface of the spinal cord. The pia mater is composed primarily of collagen and reticular fibers.[5] The pia mater will continue past the conus medullaris and fuse into the filum terminale, anchoring the spinal cord to the coccyx inferiorly. One of the main functions of the spinal pia mater is that it has important elastic qualities that help maintain the stiffness of the spinal cord, and it assists the cord return to its original shape after compression.[6] The spinal pia mater also contains denticulate ligaments, which extend outwards to help anchor the spinal cord to the spinal dura mater, further assisting with stabilizing the cord.[7]

The spinal meninges, along with the cranial meninges, have a complex embryologic origin. The pia and arachnoid mater, collectively known as the leptomeninges, are derived from the neural crest. The neural crest itself forms from the ectoderm-derived neuroectoderm and neural plate. The dura mater derives from the mesoderm.[4][8]

The blood supply to the spinal meninges comes primarily from the anterior and posterior spinal arteries. The single anterior spinal artery originates from the vertebral arteries, which each gives of collaterals that fuse and descend as the anterior spinal artery before becoming the basilar artery. The paired posterior spinal arteries also receive their blood supply from the vertebral arteries. Additional segmental medullary arteries also feed into these anterior and posterior spinal arteries via entrance points at the nerve roots, the largest being the artery of Adamkiewicz, which provides additional blood supply to the anterior spinal artery and is typically present between T9 and L2.[9][10]

The venous drainage of the spinal meninges is through the internal and external vertebral venous plexuses. These form a complex and valve-less system of drainage that is continuous with the venous system of the brain and has drainage into the azygous venous system, the portal venous system, renal veins, and the superior and inferior vena cava, among others.[11]

The spinal meninges have significant nonspecific innervation, including both sensory and sympathetic fiber. Abundant sympathetic nerve fibers with strong associations to blood vessels are present within all three layers of the meninges.[12][13] Additionally, the peridural membrane has abundant sensory and nociceptive innervations, which likely play a role in back pain.[14]

There are many tumors of the spinal meninges, one example being a meningioma. While the majority of meningiomas appear in the cranial meninges, they are also known to grow in the spinal portions, especially in the thoracic and cervical portions. Spinal meningiomas are typically benign and slow-growing and typically occur in women aged 50 to 70. Children with neurofibromatosis type 2 are also susceptible to developing spinal cord tumors, such as meningiomas and intramedullary tumors.[15][16]

The more common tumors that impact the spinal meninges are epidural metastases, which can primarily arise from breast, lung, and prostate primary cancers. These metastases can grow on either the bony vertebra, the paravertebral tissues, or within the epidural space overlying the spinal meninges. These metastases are most common in the thoracic region and can cause significant compression of the spinal cord or cauda equina syndrome if in the lumbar-sacral region.[17]

Clinically, the spinal meninges are important for their role in the spread of cancers and diagnosing of meningitis. The spinal epidural space contains a system of epidural veins known as the Batson plexus, which appears to carry implications for the spread of various infections and metastatic cancer, such as prostate cancer, resulting in the metastatic epidural masses described earlier.[1][17] Compression of the spinal cord by tumors of the meninges and epidural space can cause a plethora of neurological symptoms, such as motor weakness, upper motor signs (i.e., positive Babinski reflex), urinary incontinence, and pain.[17]

Clinicians utilize the spinal subarachnoid space when performing a diagnostic lumbar puncture, which may be useful in assessing the presence of meningitis, a subarachnoid bleed, or recording the opening pressure of CSF. A lumbar puncture is among the first tests performed when a patient presents with the cardinal features of meningitis (headache, fever, and nuchal rigidity). In adults, the L3/L4 interspinal space is the preferred location to collect the CSF from the lumbar cistern safely. The L4 spinous process is roughly midline at the level of the iliac crests, known as the intercristal or Tuffier line, making the L3/L4 interspinal space just above this landmark.

The patient should then be in either the left lateral decubitus position or seated with the spine flexed. The needle should be inserted with the bevel parallel to the fibers of the dura mater (up or down if left lateral decubitus and bevel to either the right or left if seated position, to reduce resistance when passing through the meninges and avoid harming any fibers of the cauda equina) into the L3/L4 interspinal space at a slight angle. The needle will then pass through the following structures: skin, subcutaneous tissue, the supraspinous ligament, the interspinous ligament, the ligamentum flavum, the epidural space, the dura mater, the arachnoid mater, and the subarachnoid space/lumbar cistern. The patient should receive counsel to expect common side effects such as headache, which occurs in a third of all cases, and pain is often relieved when lying supine.[18]

Anesthesia during childbirth can also be delivered using the same landmarks as placing a lumbar puncture needle. An epidural anesthetic would be placed in the epidural space, while the placement of spinal anesthesia will be within the CSF of the lumbar cistern. Epidurals are typically more precise but have a longer onset of action and require a larger dose than spinal anesthesia. Levobupivacaine and bupivacaine are two commonly used agents for epidural and spinal anesthesia.[19]

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