Case Report: Occult Spinal Dural Arteriovenous Malformation

Case Presentation

JD, age 67, presented with numbness, progressive paraparesis, and intermittent urinary retention. Their medical history was notable for hypertension, hyperlipidemia, diabetes mellitus, benign prostatic hyperplasia, latent childhood tuberculosis (status posttreatment), and a minor car accident.

On initial examination, JD had a wide-based gait with decreased lower extremity tone, patellar and Achilles reflexes of 1+, hip and knee flexion reflexes of 4+/5, and decreased sensation to pinprick that was not distributed dermatomally.

Progression of Symptoms

At 3 months after initial presentation, JD developed ascending numbness to the waist, worsening leg weakness, and bowel incontinence. They also required chronic Foley catheter placement owing to urinary retention. Progressive leg weakness continued through month 5, now accompanied by new arm weakness, proximal leg twitching, voice changes, and mild difficulty swallowing. These symptoms were confounded by diabetic ketoacidosis (DKA); however, motor and sensory symptoms were relatively unchanged after DKA resolved. At this point, JD had a circumduction gait and used a cane to ambulate. At month 7, leg weakness continued to progress. Specifically, they had worsening proximal leg weakness with absent patellar and Achilles reflex and leg muscle atrophy.

By 9 months after initial presentation, proximal leg strength was 2 of 5 and distal leg strength was 0 of 5. Mild proximal left arm weakness was present. JD was unable to leave their bed and had developed a sacral decubitus ulcer.

Diagnostic Process

Initial Diagnostic Testing

At presentation, JD had a lumbar and thoracic spinal MRI with and without contrast, which revealed a longitudinally extensive enhancing spinal cord lesion from T4 to the conus medullaris. The conus was expansile with enhancement and thickening of the nerve roots. There were no red or white blood cells in the cerebrospinal fluid (CSF) which had a glucose level of 101 mg/dL and protein level of 146 mg / dL. Serologic workup was remarkable for positive antinuclear antibodies (ANA) but was confounded by JD having undergone a course of treatment with intravenous immunoglobulin (IVIG) for presumptive acute inflammatory demyelinating polyneuropathy (AIDP) before transfer to our facility.

Although the differential diagnosis for longitudinally extensive spinal cord lesions is broad, the subacute-to-chronic progressive course of JD’s presenting symptoms and imaging features specified the differential to include vascular etiologies, other systemic inflammatory conditions, paraneoplastic syndromes, and infectious agents (Table).

Follow-up Diagnostic Tests

Over the next few months, JD continued to have worsening weakness. As both a therapeutic and a diagnostic intervention, JD was trialed with an empiric course of steroids for presumed neurosarcoidosis. They reported mild improvement in their symptoms prompting continuation of this treatment. However, as time went on, there was no observable improvement on exam and their hospital course became complicated by steroid-induced myopathy and hyperglycemia. Because of this overall clinical deteroration, a repeat battery of diagnostic testing was completed. Spinal MRI findings were unchanged at 3 months despite symptom progression. Digital subtraction angiography (DSA) at T6 through L4 and of the vertebral (left and right), intercostal (superior and supreme), thoracocervical, and femoral arteries was unremarkable.

Extensive serum and CSF analyses at 5 months ruled out neuroinflammatory, neuroinfectious, neoplastic, and paraneoplastic etiologies. A positron emission tomography (PET) scan was performed to assess for occult malignancy such as lymphoma and to further evaluate the possibility of sarcoidosis, which was notable only for increased conus avidity, a known physiologic finding.¹ Additional systemic imaging revealed no malignancy. EMG nerve conduction studies to better characterize JD’s motor and sensory symptoms showed sensorimotor neuropathy and chronic C6 radiculopathy. Repeat DSA exploring levels T1 through L4 to reassess the possibility of a vascular etiology, such as a spinal dural arteriovenous fistula (SDAVF), was unremarkable. Meanwhile, JD continued to clinically worsen. Owing to the progression of symptoms and negative workup at this point, a spinal cord biopsy was pursued.

At 7 months, a thoracic cord biopsy was performed. A significant number of blood vessels and arterialized veins were encountered on the spinal cord surface intraoperatively. Pathology of the specimen showed moderately cellular spinal parenchyma, predominantly reactive appearing, piloid gliosis, rare atypical glia, and marked vasculopathy with thickened and hyalinized vessel walls. There was no evidence of vasculitis, granulomatous disease, or active inflammation. These principal findings of vessel wall thickening and reactive astrogliosis were overall suggestive of chronic ischemia. For this reason, repeat DSA was obtained exploring levels T2 through L2, which was unremarkable.

Total spine MRI performed 9 months after JD’s initial presentation showed the lesion had extended to C7 (Figure 1). A fourth DSA now demonstrated a dilated vein near the midline of the cord at L5, warranting further investigation with selective angiography, which discovered an SDAVF at the L5 level, supplied by bilateral L5 branches of the iliolumbar artery (Figure 2).

Treatment

At presentation, JD received empiric treatment with IVIG, which did not result in objective improvement. At 3 months, pulsed methylprednisolone treatment resulted in mild subjective improvement, but was ineffective 2 months later. At 9 months, after discovery of the SDAVF at the L5 level, JD underwent surgical ligation of the fistula.

Case Resolution

Upon follow-up 4 months after surgery, JD reported some improvement in proximal leg strength and greater ability to transfer from the bed to a chair.

Discussion

JD presented with progressive paraparesis, numbness, and urinary retention. Over 9 months, 4 DSAs did not reveal the SDAVF at L5, which was ultimately identified by selective angiography. SDAVFs are the most common spinal cord vascular malformations, with an incidence of 5 to 10 per 1 million patients yearly.² The incidence peaks in the 5th and 6th decades of life, and incidence has been reported as more common in men than in women.³ SDAVFs are an aberrant connection between an artery and vein.² This pathologic communication often occurs in the dural nerve root sleeve, with up to 80% occurring in the thoracolumbar region (T6-L2). However, it can also occur beyond these regions, even involving branches of the iliac artery and rarely the external carotid artery.^4,5 Presenting symptoms include sensory disturbances, weakness (paraparesis and paraplegia), back pain or radicular pain, bowel/bladder dysfunction, and motor neuron signs, both upper and lower.^6,7 In terms of pathophysiology, increased pressure due to arterial flow causes the walls of intramedullary veins to become thickened and tortuous, resulting in venous hypertension and, in some cases, flow reversal.⁷ The reduced arteriovenous pressure gradient causes a decrease in tissue perfusion. There are fewer venous outflow channels in the lower thoracic region than in the cervical or lumbosacral region, so venous congestive edema is commonly transmitted in a caudocranial direction.⁷ This explains why the first symptoms of myelopathy (ascending sensory and motor symptoms) reflect dysfunction in the inferior spinal cord (eg conus medullaris) even if the fistula is at a more superior level. If arterial inflow pressure is increased, there is a concomitant increase in venous pressure, which explains why some patients report exacerbation of symptoms after exercise. Delays in SDAVF diagnosis occur because they are commonly missed on imaging or misdiagnosed as either an inflammatory or neoplastic process. As previously discussed, differential diagnoses of chronically progressive, longitudinally extensive myelopathies were extensively considered (Table).⁶ Persistent enhancement on MRI beyond 3 months and progression of symptoms despite steroid or immunomodulatory treatment should prompt consideration of noninflammatory etiologies of myelopathy, namely neoplastic and vascular etiologies.⁸

Characteristic imaging findings of SDAVFs include flow voids, conus swelling (90% of cases), and the “missing piece sign,” a focal geographic nonenhancing area within a long segment of holocord gadolinium enhancement (43% of cases).^3,9,10 Even in those who present with these characteristic imaging findings, however, the median time to diagnosis is 6 months, and the average time to definitive diagnosis is 1 to 3 years.^6,11 Spinal angiography is the standard modality to confirm and identify the location of an SDAVF, but this is a time-consuming procedure often complicated by variant anatomy. Smaller branches, as were present in this case, often require selective angiography with additional equipment and clinical expertise. Multidisciplinary communication amongst neuroradiology, neurosurgery, neuroendovascular, and neurology specialists is vital to the diagnosis and treatment of SDAVFs.

This case highlights an atypical but clinically devastating SDAVF supplied by L5 branches of the iliolumbar artery. If clinical suspicion is high, selective angiography, which includes vessels such as the iliac artery and its branches, is a valuable tool for the diagnosis of SDAVF.