Feline intracranial meningioma with skull erosion and tumour extension into an area of skull hyperostosis

Abstract

Skull hyperostosis is a frequently recognised feature of meningioma in feline and human patients, occurring at a frequency of around 4.5% of human cases. Evidence of osteolysis with extension of meningioma into, and in some cases through, the region of skull hyperostosis is much less commonly described in human patients. Here we present a 12-year-old cat with marked skull hyperostosis secondary to an intracranial meningioma, with magnetic resonance imaging and computed tomography evidence of tumour extension into the skull, centrally within the region of hyperostosis. Only a thin layer of bone was remaining between the mass and the extracranial region. Surgical resection of the region of skull demonstrating tumour invasion and the underlying mass resulted in good resolution of clinical signs and no post-surgical recurrence of meningioma within the 5 months follow-up period. Histopathological examination confirmed the mass to be fibroblastic meningioma.

Osteoblastic changes characterised by skull hyperostosis are a well-recognised feature of feline intracranial meningiomas. ¹ In human patients, skull hyperostosis is observed in around 4.5% of intracranial meningiomas, including all histological types, but is more frequent in meningioma en plaque where the incidence is between 13% and 49%. The precise mechanism of hyperostosis associated with meningioma remains unclear. ^2,3 Many hypotheses regarding the mechanism of hyperostosis have been proposed, including previous trauma, vascular disturbance or irritation of the bone by the tumour without invasion, stimulation of osteoblasts in the normal bone via humoral factors secreted by tumour cells, formation of bone by the tumour and tumour invasion of the bone. ^3,4 The histological type of meningioma appears to have no relationship with the development of hyperostosis in human patients and the presence of skull invasion by meningioma does not appear to be associated with a more aggressive histopathological grade in these patients. ^3,4 In this report we describe the clinical and imaging features of an intracranial meningioma characterised by skull hyperostosis and invasion of the region of skull hyperostosis by the tumour.

A 12-year-old male neutered Maine Coon cat was referred for evaluation of a 2-month history of ataxia and episodes of collapse. The owners reported lethargy, unwillingness to jump and ataxia affecting mainly the pelvic limbs. On presentation a complete physical examination demonstrated no clinical abnormalities besides the neurological abnormalities. Neurological examination revealed the cat to be obtunded with an absent menace response in the left eye. The cat was ambulatory with mild ataxia of the pelvic limbs. Conscious proprioception was reduced in the left thoracic and pelvic limbs. Segmental spinal reflexes were normal and no pain was elicited on palpation of the spine. Based on these findings, the neuroanatomical localisation was the right forebrain.

A complete blood count and serum biochemistry were performed and the results were within normal ranges for all values. Thoracic radiographs and computed tomography (CT) (Siemens, Volume Zoom) of the thorax did not reveal any abnormalities, with no evidence of pulmonary metastasis. A rostrocaudal radiograph of the skull demonstrated a well-defined area of osteolysis and bony proliferation in the right parietal region (Fig 1A). CT of the skull revealed a sharply circumscribed, homogenous, hyperdense, extra-axial mass lesion affecting the right occipital and parietal region and resulting in marked compression of the brain parenchyma and a midline shift to the left. The mass had some areas of mineralisation and showed a broad base attachment to the calvarium. At the level of attachment there was marked hyperostosis of the right frontal, parietal and occipital bones and, in one area, erosion of the parietal bone was evident (Fig 1B and C). Following intravenous administration of ioversol (127 mg/kg, Optiray; Tyco Healthcare, UK) there was marked and homogeneous contrast enhancement of the mass.

Fig 1.

Skull hyperostosis secondary to intracranial meningioma with skull invasion by tumour tissue. (A) Rostrocaudal skull radiograph demonstrating hyperostosis of the skull on the right, with skull erosion correlating to the location of the tumour (arrows). Transverse pre-contrast CT scan (B) and 3-dimensional CT reconstruction (C) through the level of the tumour demonstrating marked skull hyperostosis, with skull erosion and invasion of tumour into the region of hyperostosis (arrows). Pre- (D) and post-contrast (E) T1-weighted MR images demonstrating marked skull hyperostosis (arrow in D) and tumour invasion into the region of hyperostosis. There is homogenous enhancement of the extra-axial tumour mass, with a characteristic ‘dural tail’ (open arrow in E) consistent with the imaging appearance of a meningioma. Contrast enhancement is evident overlying the external surface of the skull (arrowheads), suggestive of local reaction (no evidence of tumour spread was evident on histopathology). (F) Haematoxylin and eosin-stained section following fixation and bone decalcification demonstrated the mass to be intimately associated with the overlying skull and invading a large cavity within the bone (Bar=1 mm). The mass was composed of streams and woven bundles of neoplastic spindle cells embedded within a collagenous matrix consistent with a fibroblastic meningioma (inset – bar=200 μm).

Magnetic resonance imaging (MRI) of the brain was performed using a 1.5 Tesla unit (Siemens, Magnetom) and the results of the MRI were consistent with the CT findings, revealing a large (2×3×2 cm), well-circumscribed, extra-axial mass in the right parietal and occipital region. The mass was mainly isointense to grey matter in T2- and T1-weighted images and showed marked homogenous contrast enhancement after intravenous gadopentetate dimeglumine (94 mg/kg, Magnevist; Bayer HealthCare Pharmaceuticals, UK) administration. The mass was resulting in a severe midline shift to the left, obliteration of the right lateral ventricle and caudal subtentorial brain herniation. At the level of the erosive region evident on CT, the mass extended into the calvarial bone (Fig 1D and E).

Surgery was performed 2 days after the MRI study was completed. The cat was premedicated with methadone intramuscular (0.2 mg/kg, Methadone; Martindale Pharmaceuticals, UK). Anaesthetic induction was performed using intravenous propofol (dose to effect, PropoFlo; Abbott Laboratories, UK) and maintained with inhalatory sevofluorane (SevoFlo; Abbott Laboratories, UK) and oxygen. A dose of 0.25 g/kg intravenous mannitol (20% w/v Mannitol; Baxter Healthcare, UK) was administered as a bolus prior to the start of surgery to pre-emptively treat for raised intracranial pressure. In addition, intravenous amoxicillin/clavulanic acid (20 mg/kg, Augmentin; GlaxoSmithKline, UK) was administered prior to the skin incision and repeated every 90 min for the remainder of the surgery. An intravenous constant-rate infusion of fentanyl citrate (3 μg/kg/h, Fentanyl citrate; Martindale Pharmaceuticals, UK) was administered intraoperatively.

The cat was positioned in sternal recumbency during the surgical procedure. A routine midline skin incision was made, extending from between the eyes to the occipital protuberances. The underlying muscles were elevated and retracted, exposing the dorsal and lateral aspects of the right frontal parietal and occipital bones. A right rostrotentorial craniectomy was performed using a high-speed air drill to remove the area of skull hyperostosis with tumour invasion. The intracranial portion of the mass was removed using a combination of sharp and blunt dissection and the dural deficit was filled with a collagen graft (Vet BioSISt; Cook, UK). The soft tissue portion of the mass and associated skull were placed in 10% neutral buffered formalin. The soft tissue mass was routinely processed for histopathology and stained with haematoxylin and eosin. The associated portion of skull was routinely decalcified, processed for histopathology and stained with haematoxylin and eosin. The cat was hospitalised for 6 days after surgery. Intermittent intramuscular injections of methadone (0.2 mg/kg) q4h and then q6h and Meloxicam q24h (0.1 mg/kg, Metacam; Boehringer-Ingelhein, Germany) were used for post-surgical analgesia. On discharge the neurological examination was normal and the cat had made a full recovery at follow-up 3 months after the surgery.

On histological examination, the mass was intimately associated with the overlying skull, invading a large cavity within the bone (Fig 1F). The cavity was lined with smooth woven bone with no evidence of recent bone resorption or new bone formation. Osteoclasts and osteoblasts were not present along the margin of the cavity. The mass itself was composed of streams and woven bundles of neoplastic spindle cells embedded within a collagenous matrix (Fig 1F inset). The neoplastic cells had scant eosinophilic cytoplasm and indistinct cell borders. The nuclei were elongated and oval with finely stippled chromatin and inconspicuous nucleoli. There was mild anisocytosis and anisokaryosis. Multifocal areas of mineralisation were observed within the mass. These findings favoured the diagnosis of a fibroblastic meningioma with erosion and invasion of the overlying region of skull hyperostosis.

Intracranial neoplasia occurs relatively frequently in cats, with a reported incidence of 2.2%. ⁵ Meningioma is the most common primary intracranial tumour (58.1%) and the most common extra-axial intracranial tumour (83%) in cats. ⁶ The CT and MRI features of feline meningiomas have been reported in the veterinary literature. ^1,7 To the authors’ knowledge this is the second report of erosion of the calvarium associated with intracranial meningioma in a cat and the first one describing the imaging findings. ⁸ Reactive changes within the bone adjacent to meningiomas are recognised in 74% of feline and 30–60% of human cases. ^1,9 Two main categories of reactive bone changes are possible, namely osteoblastic and osteolytic changes, however, osteolysis in meningiomas is rare. ^9,10 In the veterinary literature, only one previous report describes the post-mortem findings of a transitional meningioma in an elderly Persian cat causing complete erosion of the skull; however, no advanced imaging findings were reported in this case. ⁸ In the case presented in this report, MRI and CT demonstrated severe bone erosion with only a thin layer of bone remaining between the mass and the temporal muscles. Osteolytic changes of skull bone are recognised in 10–17% of human meningiomas. ⁹ Recognition of these changes is believed by some authors to be associated with a poor prognosis. ^11,12 However, other studies report that osteolytic changes in association with intracranial meningioma are not related to a more malignant pathology, with bone involvement only predicting a poor outcome in atypical meningiomas. ^2,4,10 One study has suggested that invasion of the skull by intracranial meningioma might be related to matrix metalloproteinase-2 expression in human meningiomas. ² In our case and the single previously reported feline case the histological grade of the meningioma was benign.

In summary, osteolysis of the adjacent bone can be observed with radiology and advanced imaging in feline intracranial meningiomas, and is not necessarily associated with a more malignant histopathological grade.