Evaluation of Cerebral Arteriovenous Malformations in Children

Examination

Although some patients present with significant neurological deficits and/or seizures, many patients are asymptomatic on examination. However, a detailed neurological examination and history are always important. Pay attention to evidence of neurological dysfunction in the history.

Findings suggesting an intracranial lesion

• Headaches: Headaches that occur in the early morning hours or awaken the patient from sleep suggest episodic intracranial hypertension. Typically, the headaches began within the previous 6 months.
• Persistent nausea and/or vomiting
• Altered mental status: Confusion or behavioral changes can be seen, including loss of consciousness, memory loss, or cognitive decline (including loss of milestones in younger children).
• New onset seizures: Acute onset of seizures should be investigated with intracranial imaging.

Abnormal neurological examination findings

On examination, findings may be present secondary to the following:

• Local effects: Ischemia or mass effect may give rise to focal weakness, visual changes, visual field cuts, or sensory loss.
• Increased ICP: Papilledema, increased head circumference, nausea, and vomiting may result from elevated ICP.
• High blood flow: The increased flow resulting from arterial to venous shunting can lead to dilated scalp vessels, cranial bruit on auscultation, and high-output cardiac failure.

“Red flags” on examination or history

• Cushing response: Bradycardia, hypertension, and decreased respirations may be present in acute hemorrhage.
• Uncal herniation: A dilated pupil with third nerve palsy ipsilateral to the hemorrhage and contralateral hemiparesis may occur with supratentorial hemorrhage.
• Parinaud’s syndrome: Fixed downward gaze (“sunset gaze”) may occur with increased ICP or focal lesions in the tectal region.
• Signs of increased ICP in infants: Lethargy or a tense open anterior fontanelle may be seen in infants with increased ICP.
• Signs of increased infratentorial pressure: Ataxia with nausea and vomiting can manifest as signs of increased ICP or with posterior fossa hemorrhage.
• Symptoms: Sudden onset of severe headache can occur after hemorrhage due to increased ICP from the hematoma, as can hydrocephalus and/or dural irritation from subarachnoid blood.

AVM and pregnancy

• Screening with MRI safe: MRI is safe for initial evaluation of the anatomy of the lesion (71).
• Best to treat before pregnancy: If possible, treat a known AVM prior to pregnancy (123). It is rare to discover an intracranial AVM during a pregnancy.
• Unclear risk for hemorrhage: Data in this small group of patients are inconclusive, particularly with regard to the rate of hemorrhage during the pregnancy (72,73,74,75,76,77,78). Indeed, recent studies have yielded conflicting results regarding the rate of AVM rupture during pregnancy (79,80). A large cohort-crossover analysis published in 2021 found that pregnancy and puerperium were associated with a 3.27-fold increase in the risk of hemorrhage in women with AVMs (81). No specific recommendations can be made if the AVM is diagnosed during pregnancy, because individual risk-benefit relationships need to be assessed. If the mother has an untreated or partially treated AVM, caesarean section should be considered (1,76,78,82).

Laboratory Tests

• Standard preoperative laboratory studies: CBC, clotting times (PT/PTT), type and crossmatch for blood bank, serum electrolytes, BUN, creatinine, and glucose. No abnormalities are expected.

Radiologic Tests

CT

If a child presents with a hemorrhage without clear etiology on initial evaluation (including catheter angiogram), an AVM should still be considered. Repeat imaging (MRI) in 4 to 6 weeks, to evaluate the hemorrhage cavity after the clot has cleared. CTA can also be performed to evaluate the AVM and its vascular anatomy, although DSA is preferred.

• Serpiginous areas of enhancement: An AVM typically appears as an area of mixed density with serpiginous enhancement after infusion of contrast material.
• Altered anatomy: Cerebral atrophy may be present on the affected side. A large malformation or an intracerebral hematoma may distort the normal intracranial anatomy by pushing parenchyma away from the lesion, causing a midline shift, herniation, or hydrocephalus.

MRI

MRI is useful for 3-dimensional anatomy and identification of chronic ischemia, presumably a result of steal phenomena. Evidence of vascular steal may be identified on MRI as bright signal of the surrounding brain on FLAIR or T2-weighted images. MRA may be employed to reveal feeding arteries, draining veins, aneurysms associated with the AVM, and/or venous stenosis. MRA may also be a useful tool in follow-up.

• Flow voids: The typical MRI appearance is that of a latticework of signal-void spaces, highly contrasted against surrounding cerebral tissue on both T1- and T2-weighted sequences. The serpiginous shape of vessels may be distinctive, identified as flow voids, and relevant anatomy can be well visualized with MRA.

T2-weighted axial MRI of AVM (white arrow).

T2-weighted axial MRI of AVM (white arrow).

T2-weighted axial MRI of AVM (white arrow).

DSA of AVM, lateral view: Image shows an AVM (white arrow) fed from the MCA.

DSA of AVM, AP view: Image shows an AVM (white arrow), the nidus of which is fed by the MCA. There is superficial venous drainage into the superior sagittal sinus.

• Signs of old hemorrhage: Intermixed with the flow voids of the AVM’s vessels can be regions of various signal intensities corresponding to blood products in different stages of decomposition and, occasionally, calcium and hemosiderin deposits (83,84). Susceptibility-weighted or gradient echo imaging will sometimes disclose evidence of previous hemorrhage as a dark “bloom” around the nidus (85).
• Signs of chronic ischemia: Chronic ischemic changes, presumably a result of a steal phenomenon or venous hypertension, may be identified on MRI as a bright signal of the surrounding brain on FLAIR or T2-weighted images. Diffusion-perfusion imaging can provide improved understanding of local ischemia as well (86).
• Screening tool for patients with HHT: Patients with HHT may be candidates for MRI/MRA studies of the CNS during childhood to screen for AVMs, as they may be present in 5% to 10% of children with HHT (87,88).
• Functional MRI: Functional MRI testing typically relies on T2* (T2 BOLD) signal, which is altered by cerebrovascular flow. It can often be difficult to determine function adjacent to a brain AVM and disordered flow. Therefore, the lack of activation on fMRI testing may not definitively rule out adjacent eloquence.

Angiography

DSA (including lateral and AP views) is the definitive investigation for cerebral AVM. It establishes the nature and extent of the lesion to its blood supply and its venous drainage (89). An analysis of 241 consecutive pediatric patients revealed a 0.0% complication rate during the procedure and a 0.4% postprocedural complication rate (90). Screening is not justified in the general population.

• Carotid and vertebral arteries: Angiography generally includes bilateral injection of both the internal and external carotid arteries, as well as the vertebral arteries, to visualize all the vessels potentially supplying the AVM. Rotational angiography with computer-generated reconstruction can depict lesional anatomy.
• External carotid studies important: Note that 15% of cerebral AVMs receive some blood supply from ipsilateral or contralateral meningeal arteries (91).
• Rapid circulation time: The typical angiographic appearance of an AVM is that of distended, tortuous afferent and efferent vessels connecting with a tangled vascular mass, through which the circulation time is rapid — that is, AV shunting. Smaller AVMs or residual AVMs after treatment may have reduced levels of shunting that are difficult to detect without adequate temporal resolution (often four or more frames per second).
• Abnormal findings of AVM: Evaluation by DSA should look for high-flow lesions (as opposed to low-flow lesions), outflow stenosis in vessels draining the AVM, and varices in subarachnoid or ventricular spaces. Particular attention is paid to the feeding vessels of the AVM. Their number and location are noted to help with surgical or treatment planning. The relationship with normal parenchymal supply is important to reduce the risk of stroke from neurointervention or neurosurgery.
• Aneurysms: Approximately 10% to 20% of patients with cerebral AVMs have an associated arterial aneurysm, whereas 1.4% of patients with intracranial aneurysms have coexistent AVMs (92). Often these flow-related aneurysms will spontaneously regress when the blood flow is reduced after treatment of the AVM.

Nuclear Medicine Tests

• Not usually indicated.

Electrodiagnostic Tests

• Electroencephalogram: EEG may be warranted if there is a concern for seizures.

Neuropsychological Tests

• May be useful in some cases: Although not usually indicated with AVMs, neuropsychological testing may be helpful as a baseline study in selected children to help with recovery strategies (93). Neurocognitive testing can be used to evaluate for developmental delay, especially for long-term follow-up.