INTRODUCTION

Meningiomas located below the C2 vertebral level are termed spinal meningiomas. Meningiomas are the second most common tumor in this location, next to tumors of the nerve sheath. Spinal meningiomas are most commonly completely intradural and extramedullary. However, cases with extradural extension may be seen.

According to Guidetti,^1,2 in 1887, Sir William Gowers had been treating a British Army major with paraplegia. He eventually diagnosed a spinal tumor and referred the patient to Sir Victor Horsley for operation. Sir Horsley planned thoracic laminectomy, which was only successful in locating the tumor after removing additional laminae, though with some trepidation. He removed an intradural extramedullary tumor that was consequently typed as a fibromyxoma.^1,3 Remarkably, with rehabilitation the major regained his gait, and this case has come to be known as the first spinal tumor in medical history to be cured surgically. In 1925, Elsberg⁴ compiled his experience with the diagnosis and treatment of all spinal tumors in which he described the surgical techniques of intradural tumor removal that rank him high in the history of neurosurgery. In 1938, Cushing collaborated with Eisenhardt to publish his meticulous and refined surgical techniques in a book in which they defined the successful removal of a spinal meningioma as “one of the most gratifying of all operative procedures.”^5,6

In the following four decades no major advancement was achieved in terms of surgical techniques for spinal tumors, and most of the progress henceforth owes more to the advances made in related fields such as myelography, angiography, and electromyography, followed by computer-assisted tomography (CT) and magnetic resonance imaging (MRI), which have revolutionized the diagnosis of intraspinal tumors, allowing for early detection and improved anatomic location. Introduction of microneurosurgery by Yasargil in the 1970s, together with developments in neuroanesthesiology, computer-assisted planning of operations, and a better understanding of microanatomy have resulted in more aggressive surgical approaches for even complex spinal meningiomas.⁷

INCIDENCE

Spinal intradural tumors can be categorized as extra- or intramedullary tumors. Although intramedullary tumors have a higher incidence in the pediatric age group, extramedullary tumors have a higher incidence (70%) in adults.^8,9 The annual incidence of primary intraspinal neoplasm is approximately five per million for females and three per million for males and is expected to rise as life expectancy is increasing in industrialized nations.¹⁰ Spinal meningiomas occur less frequently than intracranial ones and account for approximately 7.5% to 12.7% of all meningiomas.¹¹ Meningiomas have a very low incidence in the first two decades of life,^12,13 and in the first five decades they occur more frequently in the cervical spine (39% of spinal meningiomas).¹⁴ Meningiomas in middle-aged women between the fourth and fifth decades account for 80% of all spinal meningioma cases.¹⁵

Various reports consistently show the most common distribution of meningiomas along the spinal axis to be the thoracic segment (67%–84%), followed by the less frequent high cervical levels (14%–27%). They are extremely rare at lumbar levels (2%–14%).^7,12,16–21 Although most of the spinal meningioma cases are intradural, 5% to 14% occur at extradural or extraspinal locations.^{7,13,16,22,23}

PATHOLOGY AND ETIOLOGY

Spinal meningiomas are thought to originate from arachnoid cap cells that are most densely located within the arachnoid villi at the entry zone of the nerve roots or at the junction of dentate ligaments and dura mater, where the spinal arteries penetrate.^24,25 For this reason, lateral tumors are more common than dorsal and ventral lesions.^17,20,25,26 Gottfried and colleagues⁷ performed a meta-analysis including 566 cases from 6 published series, reaching the conclusion that most spinal meningiomas were located lateral to the spinal cord or had a component that extended laterally assuming a posterolateral or anterolateral location, of which they determined the posterolateral was the more frequent. Interestingly, Levy and colleagues¹⁸ reported that cervical meningiomas were more likely to be located ventrally.

The striking preponderance of meningiomas for postmenopausal women has led to a controversy over a causal relationship between the sex hormones and meningiomas.²⁷ Hormonal studies that have shown the existence of various receptor types in meningioma, of which progesterone is the most notable, followed by estrogen and others, support the argument for this relationship.^27–29 Preston-Martin and colleagues³⁰ suggested that the overwhelming tendency of spinal meningiomas to occur in the thoracic segments of postmenopausal women may be due to increased trauma of the meninges related to the osteoporotic collapse of thoracic vertebrae. Ionizing radiation is another known risk factor for the development of these tumors.^31,32

Multiple meningiomas occurring both at intracranial and spinal locations is a rare entity. Only 18 such cases have been reported worldwide, for which in only 10 cases were surgery and histopathologic investigations performed separately for the tumors at both locations. In five of these cases, the tumors revealed the same histopathologic classification, only one being malignant. In the other five cases, which revealed different histopathology for intracranial versus intraspinal lesions, the meningiomas had a benign character.³³ These cases strongly support the idea that spinal or cranial meningiomas may be derived from the same clone of cells and provide foundation for the theory of development of multiple meningiomas from the spreading of tumor cells via cerebrospinal fluid (CSF) as a possible mechanism, which eventually may progress to assume different histologic subtypes.³⁴

The most important histologic difference between the spinal and cranial meninges is that the former has an intermediate layer and the latter does not. Electron microscopic investigations of human spinal meninges demonstrate an intermediate leptomeningeal layer lying between the arachnoid and pia mater. This intermediate layer is attached to the inner aspect of the arachnoid mater and extends in an arborizing fashion over the dorsal surface of the spinal cord, encasing the nerve roots and blood vessels.^26,35 The intermediate layer is not observed in human cerebral leptomeninges. The presence of the intermediate layer in spinal meninges might explain the hypointense rim detected via MRI around the tumor and may also be the reason why no penetration and no tumoral edema are observed in spinal meningiomas which is common with intracranial meningiomas^26,36 (Fig. 46-1). Caroli and colleagues³⁷ suggested that incomplete development of the intermediate layer may underlie the en plaque expansion of meningiomas and facilitate the involvement of the pial layer. Salpietro and colleagues²⁶ considered the intermediate layer responsible for two types of interfaces between the tumor and pial membrane. Accordingly, what they call a “floating interface” correlates with the presence of the hypointense peritumoral rim revealed by MRI. This interface is characterized by a small preserved subarachnoid space confined between the arachnoid and the intermediate leptomeningeal layer, making the tumor easily dissectible from the spinal cord. In the deep-type interface, however, no hypointense rim is observed on MRI scans. The inner arachnoid layer is difficult to identify or absent, and the blood vessels and spinal roots are extremely adherent to the tumor, making dissection of the tumor more difficult, although generally achievable as no pial disruption is present.

FIGURE 46-1 Axial section (top) and sagittal (lower left)-coronal (lower right) reconstruction myelo-CT shows displacement of spinal cord and round tumor.

Most spinal meningiomas are globoid, but a few exceptions assume a carpet-like, en plaque configuration. Reflecting the variable proportions of neoplastic cells, collagen, and psammoma bodies, meningiomas range in consistency from soft to firm to even gravel-like.¹⁸ Most meningiomas remain within the intradural space, although a few penetrate the dura or exit through root sleeves to reach the adipose tissue of the epidural compartment, rarely resulting in exclusively epidural tumors.^24,38 Only rarely do these lesions continue their infiltration into the regional soft tissue and bony structures.³⁹

Although spinal meningiomas exhibit the same histologic spectrum as the intracranial meningiomas, psammomatous lesions are overrepresented.^16,40 Intradurally, meningothelial and psammomatous meningiomas are the most common histologic subtypes of spinal meningioma.^23,40 On the other hand, atypical (WHO grade II) and malignant (WHO grade III) meningiomas are rare in the spinal meninges, with a combined incidence of 1.3% among all craniospinal meningiomas.^7,20,40,41 An unusual variant, the clear cell meningioma (WHO grade II), is rare in the spine, prone to appear in the lumbar region, and is associated with a worse prognosis.^42,43 Despite the relative frequency of psammomatous lesions, calcifications that are visible on plain radiographs are rarer than calcified intracranial meningiomas.^16,44,45 They emerge from the incipient hydroxyapatite crystals precipitate and recruit collagen fibers as they coalesce into psammoma bodies, eventually resulting in calcified or ossified meningiomas.^37,46 However, Kitagawa and colleagues⁴⁷ did not found a correlation between the ossification process and density of psammoma bodies in meningiomas and suggested that ossification is a result of metaplasia in the arachnoid cells.^45,47

The occurrence of differential patterns of genetic abnormalities and gene expression profiles in spinal meningiomas versus cranial meningiomas may provide new insights into molecular pathways involved in tumor genesis and progression of spinal meningiomas and could explain their particular clinical and histologic features.^48,49 Sayagues and colleagues⁴⁹ found differential expressions in 35 genes in spinal versus cranial meningiomas, of which only MN1 was encoded in chromosome 22, the usual suspect in meningioma pathogenesis.

PRESENTATION

Owing to the slow growing rate of these tumors, patients have a slow, indolent course of symptoms. In most patients, the presenting symptoms largely depend on tumor location and duration. Various authors reported that with the introduction of MRI into clinical practice, the average history until diagnosis was shortened by about 6 months, and consequently, patients suffered less severe neurologic deficits at the time of surgery.^7,16,20,44

Invariably, the most common presentations are motor deficit and spinal pain.^{7,16,18–20,40} However, when the natural courses of symptoms are considered, two developmental stages of the tumor can be recognized. In the first stage, symptoms appear due to irritation of nerve roots. In the second stage, symptoms develop due to compression of the spinal cord.

In the first stage, the most notable symptom of nerve root involvement is pain, which predominates and may precede all other symptoms by months or years. The pain may assume a radicular, radiating character or may present as a localized back pain. The other common symptoms of this stage are partial weakness and sensory loss (hypoesthesia, paresthesia). As the tumor begins to compress on the spinal cord, symptoms of the second stage develop that may progress simultaneously with pain or in a small percentage of cases without pain.²⁵ If the tumor is situated anterolaterally, the symptoms will progress to produce a Brown–Sequard-like syndrome that presents as motor loss and impairment of tactile and deep sensations on the same side below the level of the lesion, together with loss or diminution of pain and temperature perception on the opposite side. In posteriorly located tumors the posterior columns of the cord are the first to be compressed by the tumor, the deep sensibility is decreased, and ataxia appears.

In advanced cases, complete paralysis below the level of the tumor will develop as a result of extreme cord compression, accompanied by total loss of sensory functions. In addition, these patients will have definite loss of control of both vesical and rectal sphincters.

Sphincter disturbances are generally late findings in the course of symptoms and are ominous signs for the recovery of functions that can be expected after surgery.^7,20

It should be kept in mind that the clinical picture created by spinal meningiomas is not specific, and the differential diagnosis should consider spinal tumors of all types even after most advanced imaging techniques.⁵⁰

DIAGNOSIS

In the era before the revolutionary introduction of MRI, during which myelography was the radiological modality of choice for diagnosis, spinal meningiomas were often confused with other medical conditions such as multiple sclerosis, syringomyelia, and herniated disc.^{1,7,16,19,25,44} Levy and colleagues¹⁸ reported a 33% rate of misdiagnosis in their series for cases antedating MRI, which led to delayed treatment and sometimes, to inappropriate surgeries. Today, the use of myelography is confined to cases with previous surgical implants incompatible with MRI.

In the past, plain radiography was valued for its ability to detect calcified meningiomas, although calcifications are only visible on 1% to 5% of plain x-ray films.⁴⁶ Further, spinal meningiomas with calcifications that are visible on plain radiographs are rarer than calcified intracranial meningiomas. This is thought to be due to the fact that intraspinal spaces are much smaller than intracranial spaces and symptoms appear more rapidly leaving less time for visible calcifications to occur.⁵¹

CT is more reliable than plain radiographs in demonstrating these tumoral calcifications,⁵² because it is highly sensitive to alterations in bone mineralization and is particularly useful in evaluating the bony matrix. Combined with MRI, it provides valuable information as to the aggressiveness of the tumor. This is because, in general, it is possible to infer the benign or malignant nature of the lesion from the pattern of bony destruction. Bony changes that occur in an expansive manner respectful of the original topography suggest a slowly expanding benign lesion. Generally, long-standing tumors demonstrate an enlarged spinal canal with scalloping of the vertebral bodies, pedicle erosion, and thinning of the lamina.⁵² Particularly, contrast-enhanced CT, with its ability to demonstrate tumoral lesions and their interactions with bony structures, provides more superior information than non-contrast CT. Further, myelo-CT, although an invasive procedure, can still be used today to demonstrate intradural tumors where MRI is unavailable or for patients with MRI-incompatible instruments (Fig. 46-2).

FIGURE 46-2 A, T1-weighted sagittal MRI with contrast clearly showing the level of an enhancing thoracic meningioma. B, T1-weighted coronal MRI with contrast clearly showing the dural base and extradural extension of an enhancing laterally situated thoracic meningioma (arrow).

With its superior contrast sensitivity and multiplanar capabilities, MRI is the gold standard for diagnosing spinal meningiomas. It provides crucial information for surgical planning, as it clearly delineates the level of the tumor and its relationship to the cord. Contrast-enhanced MRI defines the relationship of the tumor to the spinal cord, nerve roots, and thecal sac, differentiating the tumor from peritumoral edema and cysts, determining tumor extent, and evaluating the cord’s intrinsic signal abnormalities.⁵² When investigating an intraspinal pathology, both T1-weighted images (T1WI) and T2-weighted images (T2WI) should be obtained in the axial and sagittal planes. T1-weighted slices should also be obtained following contrast injection. Coronal imaging is particularly useful for laterally situated tumors or for tumors extending longitudinally over multiple levels (Fig. 46-3). MRI is an excellent tool to delineate both intradural and extradural meningiomas. In principle, when an intradural, extramedullary lesion is detected on MRI, only one of a few benign lesions should be considered in differential diagnosis.⁵⁰ Typically, spinal meningiomas are isointense to the normal spinal cord on T1- and T2-weighted images, and they display intense enhancement after gadolinium (Fig. 46-4).^40,51,53 Coronal scanning planes are especially very helpful in detecting dural tails, which are very suggestive of meningiomas.^53–55