Evaluation of Cerebral Arteriovenous Malformations in Children

Examination

Many patients are asymptomatic on examination.  However, a detailed neurological examination and history are always important.  Attention should be paid 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 are less than 6 months in duration.
• 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).

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, etc., may result from elevation in ICP.
• High blood flow: The increased flow resulting from arterial to venous shunting can lead to dilated scalp vessels, 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.
• Physical signs of increased ICP: Lethargy, or a tense open anterior fontanel may be seen in infants with increased ICP.
• Global signs of increased ICP: 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 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 (36).
• Best to treat before pregnancy: Treatment of a known AVM should be undertaken prior to pregnancy, whenever possible. It is rare to discover an intracranial AVMs 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 (29–35).  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, 33, 35, 37, 40). 

Laboratory Tests

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

Radiologic Tests

CT

If a child presents with a hemorrhage without clear etiology on initial evaluation, an AVM should be considered and imaging repeated in 4–6 weeks, with MRI performed to evaluate the hemorrhage cavity after the clot has cleared.

• Serpiginous areas of enhancement: An AVM typically appears as a heterogeneous area of mixed density with serpiginous areas of enhancement after infusion of contrast material. 
• Altered anatomy: Cerebral atrophy may sometimes 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 3D anatomy and identification of chronic ischemia, presumably a result of “steal” phenomena. Evidence of steal may be identified on MRI as bright signal of the surrounding brain on FLAIR or T2-weighted images.

• 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 MR angiography. 

T2-weighted axial MRI of AVM a:

T2-weighted axial MRI of AVM b:

T2-weighted axial MRI of AVM c:

T2-weighted axial MRI of AVM d:

• 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 evolution, and occasionally calcium and hemosiderin (23, 24). Susceptibility imaging will sometimes disclose evidence of previous hemorrhage as a dark “bloom” around the nidus (25).
• Signs of chronic ischemia: Chronic ischemic changes, presumably a result of a “steal” phenomenon or venous hypertension, may be identified on MRI as bright signal of the surrounding brain on FLAIR or T2-weighted images.  Improved understanding of local ischemia can also be obtained by diffusion-perfusion imaging (26) .
• 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 5–10% of children with HHT.

Angiography

Digital subtraction angiography is the definitive investigation. It establishes the nature and extent of the lesion to its blood supply and its venous drainage (27).  A recent analysis of 241 consecutive pediatric patients revealed a 0% complication rate during the procedure and a 0.4% post-procedural complication rate (53). Screening is not justified in the general population.

DSA of AVM, lateral view: Shown is an AVM that is fed from the middle cerebral artery

DSA of AVM, AP view: Shown is the AVM whose nidus is fed by middle cerebral artery and vein draining into sagittal sinus

• Carotid and vertebral arteries: Angiography generally includes bilateral injection of both the internal and external carotid arteries and the vertebral arteries to visualize all of the vessels supplying the AVM.  Three-dimensional angiography with computer-generated reconstruction is increasingly employed to depict lesional anatomy. 
• External carotid studies important: It is important to underscore that 15% of cerebral AVMs receive some blood supply from ipsilateral or contralateral meningeal arteries (28). 
• 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; i.e., arteriovenous shunting.
• Normal vessels only displaced by hemorrhage: Other vessels or structures are not displaced unless there is an intracerebral hematoma which appears as an avascular mass. 
• Abnormal findings of AVM: Evaluation by DSA should look for high flow rate lesions (as opposed to low flow rate 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 is noted to help with surgical or treatment planning.
• Aneurysms: In approximately 7–25% of cases of cerebral AVM, there is an associated arterial aneurysm, whereas 1.4% of patients with intracranial aneurysms have coexistent AVMs.  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 Testing

• EEG: EEG may be warranted if the concern for seizures exists.

Neuropsychological Testing

• Not usually done: Although not usually indicated with AVMs, neuropsychological testing may be helpful as a baseline study in selected children to help with recovery strategies.