Occipital Bone Angiomatosis and Chronic Subdural Hematoma Causing Severe Cerebellar and Brainstem Compression and Obstructive Hydrocephalus in a Young Adult Cat

ABSTRACT

A 2‐year‐old cat was presented for a 1‐month history of cautious ambulation, head shaking, and lethargy, with severe spinal pain on neurologic examination. MRI and CT demonstrated marked endophytic thickening of the occipital bone diploe with widened intertrabecular spaces, irregular internal cortical margins, relative preservation of the outer cortex, and strong internal and perilesional contrast enhancement. Histopathology revealed an anomalous blood vessel proliferation consistent with angiomatosis. An associated chronic subdural hematoma caused severe cerebellar and brainstem compression, foramen magnum herniation, and obstructive hydrocephalus. This represents the first report of occipital bone angiomatosis with concomitant subdural hematoma in a cat.

1. Signalment, History, and Clinical Findings

A 2‐year‐old female spayed domestic shorthair cat (3.9 kg) was presented to MedVet Cincinnati's Neurology Service for further evaluation of cautious ambulation, head shaking, and lethargy, which had begun 1 month prior and was partially responsive to transdermal buprenorphine, oral robenacoxib, and oral gabapentin prescribed by the referring veterinarian.

Neurologic examination revealed severe thoracic and lumbar spinal hyperesthesia. The remainder of the neurologic and physical examination was normal. Differential diagnoses included inflammation (e.g., discospondylitis, meningomyelitis), vertebral malformation(s), and neoplasia.

2. Imaging, Diagnosis, and Outcome

The patient was positioned in dorsal recumbency under general anesthesia in preparation for a spinal MRI, using a 1.5 T unit (MAGNETOM Symphony; Siemens Medical Solutions, Erlangen, Germany) and a spine coil. Sagittal half‐Fournier acquisition single‐shot turbo spin‐echo (HASTE) sequences did not reveal abnormalities in the cervical or thoracolumbar spine. However, at the cranial edge of the cervical spine field of view, a large CSF‐isointense fluid accumulation was visible in the dorsal caudal fossa, and the squamous occipital bone was thickened and bulbous. The cerebellum was severely compressed, and foramen magnum herniation resulted in dorsal subarachnoid CSF signal attenuation at the atlantooccipital junction. In the absence of compressive myelopathy, the caudal fossa abnormalities most likely explained the clinical signs; thus, further spinal examination was not pursued, and subsequent imaging was instead focused on the intracranial region.

Pulse sequences of the brain were as follows: Sagittal and transverse T2W TSE, transverse T2‐FLAIR, transverse diffusion‐weighted imaging (DWI) and apparent diffusion coefficient (ADC), pre‐ and post‐contrast sagittal, transverse, and dorsal T1W TSE, post‐contrast PDW TSE, and post‐contrast T2*W GRE. Gadobutrol (Gadavist 1 mmol/mL; Bayer Healthcare Pharmaceuticals, Wayne, NJ) was administered at 0.1 mL/kg IV.

There was severe, well‐defined, predominantly left‐sided, endophytic thickening of the squamous occipital bone diploe with heterogeneous T2W/T1W signal intensity (Figure 1). A small, ill‐defined, relatively T2W/T2‐FLAIR hyperintense region within the diploe bordered a focal region of dorsal outer cortical thinning. The outer cortex was otherwise preserved and smooth. The inner cortex was undulant and irregularly marginated. There was strong heterogeneous contrast enhancement within the diploe and a thin rim of enhancement of the dura mater adherent to the inner cortex of the caudal fossa, involving the occipital bone anomaly and the bone cranial to it.

FIGURE 1.

MRI of the caudal fossa. Sagittal and transverse T2W TSE (A and B), transverse T1W TSE (C), and post‐contrast transverse and dorsal T1W TSE (D and E). Parts (B–D) are at the level of the caudal medulla oblongata. The third ventricle is severely dilated (A, asterisk). A large subdural fluid accumulation, T2W isointense to CSF, fills the dorsal caudal fossa (A and B, diamonds), spanning the tentorium cerebelli to foramen magnum, causing cerebellar and brainstem compression and foramen magnum herniation (A, solid arrow). There is severe left occipital bone diploic thickening (A, solid arrowheads) with T2W/T1W heterogeneity, focal T2W hyperintensity bordering outer cortical thinning (B, hollow arrow), and strong heterogeneous internal contrast enhancement (D). A thin rim of enhancement of the outer dura mater also borders the inner cortex (D and E, hollow arrowheads). Rostral is on the left (A) and at the top (E), and the patient's right is on the left (B–E) of the images.

A large fluid collection filled the dorsal caudal fossa (Figure 2), spanning the tentorium cerebelli to the foramen magnum, and bordering the entirety of the occipital bone lesion's inner surface. Relative to normal CSF, the fluid was T2W isointense, non‐suppressing on T2‐FLAIR, T1W mildly hyperintense (isointense to gray matter), and PDW strongly hyperintense. A wispy susceptibility artifact along the dorsal margin of the fluid collection was observed on the GRE sequence. There was no restricted diffusion. This fluid did not extend into the cerebellar sulci, was confined to the infratentorial compartment, and caused significant mass effect, consistent with a subdural location [1, 2]. There was secondary severe ventral cerebellar displacement and compression, foramen magnum herniation, mild ventral brainstem compression, and severe symmetrical dilation of the lateral and third ventricles and olfactory recesses.

FIGURE 2.

MRI of the brain. Transverse T2W‐FLAIR (A and B), transverse T2*W GRE (C), transverse PDW TSE (D), transverse T1W TSE (E), and sagittal T1W TSE post‐contrast (F). Part (A) is at the level of the midbrain. Parts (B–E) are at the level of the rostral medulla oblongata. CSF in the ventricular system appropriately FLAIR suppresses (A, asterisks). The subdural fluid (B–E, diamond) is FLAIR, PDW, and T1W hyperintense to CSF. A small wispy susceptibility artifact is along the fluid's dorsal margin on the GRE sequence (C, arrow). Contrast enhancement of the skull‐adherent meningeal dura mater abuts and extends rostral to the occipital bone lesion (F, arrowheads). The patient's right is on the left (A–E), and rostral is on the left (F) of the images.

CT was subsequently performed in sternal recumbency (SOMATOM go.Up, 64‐slice; Siemens Healthineers) for its superior characterization of osseous architecture, with the goals of evaluating for subtle aggressive features and determining lesion extent for potential surgical planning. Helical transverse images of the head (0.6 mm slice thickness) were obtained and reconstructed using low‐ and high‐frequency kernels. Sagittal and dorsal reconstructions were also made using 1.0 mm slice thickness. IV contrast was not administered. Occipital diploic thickening was endophytic, and internal punctate low‐attenuating areas were interpreted as widened intertrabecular spaces (Figure 3). The internal cortex was irregularly marginated and thin. The shape of the outer cortex was preserved, but there was focal lysis dorsally. The subdural fluid was mildly hyperattenuating (20–25 HU) compared to CSF (0–15 HU).

FIGURE 3.

Sagittal (A), dorsal (B), and transverse (C–E) CT images of the skull. A–C are in a bone window (WL 500 HU, WW 2000 HU), and D and E are in a brain window (WL 40 HU, WW 80 HU). The occipital bone lesion's internal cortex is irregular (A and B, brackets). The outer cortex is normal except for focal punctate lysis (C, arrow). Numerous hypoattenuating foci in the diploe represent widened intertrabecular spaces (C, arrowhead). The subdural fluid accumulation (D, diamond) is hypoattenuating to the cerebellum but is slightly hyperattenuating to CSF (E, asterisks). Rostral is on the left (A) and at the top (B), and the patient's right is on the left (B–E) of the images.

For the occipital bone abnormalities, an anomalous vascular proliferation (e.g., angiomatosis, hamartoma, and arteriovenous malformation) was prioritized over a benign osseous tumor (e.g., exostosis and osteoma), as the former differential accounted better for the patient's age and presence of widened intertrabecular spaces and strong internal contrast enhancement. Malignant neoplasia (e.g., multilobular osteochondrosarcoma) was less likely given the lack of aggressive characteristics. Initial interpretation of the subdural fluid was proteinaceous/cellular material as a component of or sequela to the osseous lesion, potentially with a small component of hemorrhage to explain the minute susceptibility artifact.

Lumbar CSF tap was performed at the attending neurologist's discretion due to the unusual appearance of the lesion. The risk of performing this procedure was assessed to be low compared with the potential benefit of further characterizing the lesion. It revealed hemodilution, with no infectious organisms, significant inflammation, or atypical cells identified. A CSF PCR panel (coronavirus, bartonella, cryptococcus, toxoplasma, and FeLV/FIV) and serum antibody testing (toxoplasma) were negative.

Medical treatment was initiated, consisting of omeprazole (Glenmark Pharmaceuticals Inc.), gabapentin (Amneal Pharmaceuticals LLC), and a tapering course of prednisolone (PrednisTab, Lloyd Inc.).

Upon examination 4 weeks later, the patient's spinal hyperesthesia was less severe than previously, and the owners reported significant improvement in clinical signs of pain at home. After consultation on continued medical or surgical management, the owners elected to proceed with surgical debulking.

A suboccipital craniectomy was performed. The occipital bone appeared grossly thickened and roughened (Figure 4A). A large portion of the lesion was excised and submitted for histopathology. A large volume of clear yellow fluid emerged upon entering the calvarium, with mild blood contamination, which was submitted for cell/protein quantification and cytology. The cerebellum subsequently appeared decompressed and grossly normal. Gelfoam was placed over the craniectomy window, and the soft tissues were closed. Anesthetic recovery was uneventful, and the patient was discharged two days later following in‐hospital analgesia and monitoring.

FIGURE 4.

Intraoperative photograph (A) with the patient in sternal recumbency. The patient's right is on the left of the image. An occipital craniectomy window was created 3 mm ventral to the external occipital protuberance (*). The dorsal aspect of the C1 vertebra (**) is caudal to this window. Subdural fluid has been drained, and the cerebellum is grossly normal after decompression. Histopathologic section (B) of the occipital bone, H&E stained. Intertrabecular spaces are filled by a proliferation of well‐differentiated, variable‐caliber blood‐filled vascular spaces (capillary, arteriolar, and venous) lined by a single layer of endothelial cells lacking malignant criteria.

Histopathology (Figure 4B) revealed irregular anastomosing trabeculae of woven bone with marked variability in thickness. The intertrabecular spaces were expanded by a vascular proliferation composed predominantly of well‐defined capillary and arteriolar vessels in disorganized clusters, enmeshed in a loose connective tissue stroma. Constituent endothelial cells lining these vessels were well differentiated, with absent atypia and very low mitotic activity (<1 mitotic figure in 10 high‐power fields (2.37 mm²)). Hemosiderin‐laden macrophages were present throughout the stroma within and surrounding the lesion. The periosteal surface was irregular and scalloped. The subdural fluid collection was low‐cellularity and protein‐rich (4.3 g/dL protein, <100,000 red blood cells/µL, and <100 nucleated cells/µL) and contained few pigment‐laden macrophages. Diagnostic findings were consistent with occipital bone angiomatosis with chronic intralesional and subdural hemorrhage.

A 3‐week recheck examination revealed a normal neurologic examination. Spinal hyperesthesia was resolved. The owner reported no signs of discomfort at home, with less frequent head shaking. The medication regimen was slowly tapered, and the allowed activity level was gradually increased. The patient remained neurologically normal 3 months later; head shaking had resolved.

3. Discussion

Skeletal angiomatosis and intraosseous vascular hamartoma are entities characterized by proliferation of histologically well‐differentiated small‐caliber blood vessels with well‐differentiated walls within pre‐existing bone [3, 4, 5]. In the authors’ opinion, these lesions could be the same process given overlapping histopathological descriptions and clinical and biological behavioral features [5, 6].

This is the first reported case of angiomatosis affecting the occipital bone, or any cranial bone, in a cat. Skeletal angiomatosis is rare in cats, and previous reports are almost exclusively in vertebrae, except for one reported in the mandible [7]. Most involve the thoracic spine and are monostotic, except for one case involving two sequential vertebrae [3, 4, 5, 6, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18]. The vertebral body, arch, articular facets, and rarely spinous process [8, 13] can be affected. Most patients present between 1 and 2 years of age [9]. Review of previously reported feline vertebral angiomatosis cases [3, 4, 5, 6, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18] showed that 50% of affected cats were domestic shorthairs, with Maine Coons overrepresented at 17%, and two‐thirds were neutered or intact males. Typical clinical signs include several weeks to months of spinal pain, lethargy, paraparesis, and proprioceptive ataxia, often progressive. Reports of canine angiomatosis more commonly reveal a broader anatomical distribution, including cutaneous, meningeal, skeletal, and multifocal manifestations [19, 20], though involvement of the cranial bones has also not been reported in dogs.

The osseous lesion in the present case shared imaging features with prior reports of vertebral angiomatosis, including trabecular thickening, irregular internal cortical margins, relative preservation of outer cortex, punctate hypoattenuating regions (widened intertrabecular spaces), and strong heterogeneous gadolinium contrast enhancement [5, 10, 18]. Additionally, the histopathological findings were commensurate with those previously reported for vertebral (skeletal) angiomatosis and distinct from meningioangiomatosis, a similar entity of meningothelial proliferation affecting similar anatomic locations [12, 21].

This case is the first to describe subdural fluid accumulation associated with skeletal angiomatosis. The protein‐rich, xanthochromic fluid and pigment‐laden macrophages were consistent with chronic hemorrhage [22, 23, 24]. The CT and MRI features of the fluid were, in retrospect, also consistent with this diagnosis. Chronic subdural hematomas (cSDH) are hypoattenuating on CT in people [23]. Although MRI features of cSDH can vary, most uncomplicated cSDHs are T2W hypo‐ to isointense, T2‐FLAIR hyperintense, T1W hyperintense, and PDW hyperintense to CSF; have no restricted diffusion; and contrast enhance along the skull‐adjacent outer membrane corresponding to the outer (meningeal) layer of dura [22, 23, 25]. Unlike parenchymal hematomas, cSDHs less commonly form a hemosiderin rim, because the absence of a blood–brain barrier in the subdural space allows macrophages that store it to be largely reabsorbed into the bloodstream [22, 23, 25]. This may explain the relative paucity of susceptibility artifacts on the GRE sequence. Microhemorrhage within the occipital bone lesion was documented histopathologically, making the angiomatosis lesion the presumed origin of the hematoma. Angiomatosis lesions are prone to spontaneous hemorrhage [5], which the authors speculate could be caused by chronic microtrauma, thrombotic occlusion, or localized hypertension, with resultant compressive and expansile forces. In humans, calvarial cavernous hemangiomas are benign vascular tumors arising within the diploe [26]. Pressure from intradiploic hemorrhages within these lesions can result in erosion of the inner table of the skull and formation of a subdural hematoma, when also associated with dural erosion, or an epidural hematoma if the dura remains intact [26]. A similar mechanism may explain the subdural hematoma in the present case, though extension of the lesion through the dura could not be confirmed histopathologically given the limited scope of the biopsy, and gross perforations of the dura were not specifically noted at surgery.

Occipital bone angiomatosis should be considered a differential diagnosis in young adult cats presenting with chronic spinal pain, and for which MRI and/or CT demonstrates well‐defined occipital diploic thickening, an irregular internal cortex, widened intertrabecular spaces, and strong contrast enhancement.

Author Contributions

Mark Chalkley: investigation, writing – review and editing. Matthew Baron‐Chapman: supervision, writing – review and editing, investigation. Jonathan Cohen: conceptualization, writing – original draft, writing – review and editing, investigation, visualization. Alba Maria M. Shank: investigation, writing – review and editing, visualization. Kelli Mossine: writing – review and editing, supervision, investigation.

Disclosure

The authors have nothing to report.

Ethics Statement

Ethical approval to use this patient's clinical data was obtained from the hospital's medical director.

Consent

The owner provided informed consent for all diagnostic and treatment decisions.

Conflicts of Interest

The authors declare no conflicts of interest.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.