eMedicine Specialties > Neurosurgery > Vascular
Intracranial Arteriovenous Malformation
Updated: Mar 26, 2009
Introduction
Abnormalities of the vascular structures of the head and brain have long been recognized. McCormick published an influential classification system in his 1966 paper, "The Pathology of Vascular ('Arteriovenous') Malformations."1 He described the arteriovenous malformation (AVM), cavernous malformation, venous malformation, telangiectasia, and varix. Intracranial varices are not of significant current clinical concern. This overview focuses on the previous 4 classes. A 44-year-old woman presented with left-sided hemiparesis and intraventricular hemorrhage on her head CT. This axial T2-weighted MRI shows arteriovenous malformation nidus on the right side. The arrows demonstrate large draining veins within the right lateral ventricle.
A 44-year-old woman presented with left-sided hemiparesis and intraventricular hemorrhage on her head CT. This axial T2-weighted MRI shows arteriovenous malformation nidus on the right side. The arrows demonstrate large draining veins within the right lateral ventricle.
Arteriovenous Malformation
History
Luschka and Virchow originally described arteriovenous malformations (AVMs) in the mid 1800s. Olivecrona performed the first surgical excision in 1932.
Definition
Lesions of the cerebral vasculature develop such that blood flows directly from the arterial system to the venous system without passing through a capillary system. The arteriovenous (AV) shunt is the definitive characteristic of these lesions.
Frequency
The estimated incidence of AVM in the US general population is 0.14% (140 cases per 100,000 persons or 1 case per 700 persons). This is approximately one fifth to one seventh the incidence of intracranial aneurysms.
Etiology
One or more persisting direct connections from the arterial to the venous systems are present. AVMs are considered congenital lesions and are characterized by a failure of the embryonic vascular plexus to fully differentiate and develop a mature capillary bed in the affected area. The formation of AVMs probably relates to sequential formation and resorption of cerebral surface veins. Their structures may change and grow postnatally but only in relation to a prenatally extant lesion. Molecular biologic factors are thought to be important to AVM development. These may include vascular endothelial growth factor (VEGF) and basic fibroblast growth factor (bFGF). Tissues adjacent to the AVM may be persistently mildly hypoxic because the malformation may steal blood from adjacent healthy tissue, further promoting angiogenesis.
Pathophysiology
The direct connection between the arterial and venous systems supplies a low-resistance shunt for arterial blood and exposes the venous system to abnormally high pressures. This results in a system of enlarged feeding vessels, the tangled nidus of the AVM itself, and enlarged draining venous structures.
Clinical presentation
- Hemorrhage (53% of cases)
- Acute onset of severe headache
- May be described as the worst headache of the patient's life
- Depending on the location of hemorrhage, may be associated with new fixed neurologic deficit
- Seizure (46%)
- Headache (34%)
- Progressive neurologic deficit (21%)
- May be caused by mass effect or ischemia resulting from local vascular steal phenomenon
- Presence and nature of deficit depend on location of lesion
- Pediatric patients
- Heart failure
- Macrocephaly
- Prominent scalp veins
Hemorrhage is more likely to be caused by small lesions, while seizures are more likely to be caused by large lesions.
An increasing number of lesions now are found incidentally upon brain imaging.
The annual risk of intracranial hemorrhages associated with AVMs is 2-3%. The mortality rate associated with the initial bleed is 10%. The mortality rate associated with the second bleed is 13%, and the rate increases to 20% for each subsequent bleed. The incidence of new neurologic deficit occurring with each bleed is 50%. These numbers are generalized for all AVMs. The location and size of each patient's lesion greatly affects their risk of morbidity and mortality.
Patients with an AVM have an increased risk of developing a cerebral aneurysm. Approximately 7.6% of patients with an AVM develop an aneurysm. Alternatively, 1.1% of patients with an aneurysm are found to have an AVM. Most commonly, aneurysms are found on arteries feeding the AVM.
Rare case reports describe multiple intracranial AVMs and/or concomitant intracranial and intraspinal AVMs, but these are too rare to be well characterized. AVMs may present as part of a neurocutaneous syndrome, including Sturge-Weber syndrome or Rendu-Osler-Weber syndrome.
Workup
- Lab studies (these are for routine preoperative evaluation and not for diagnosis, per se)
- CBC count
- Prothrombin time (PT)/activated partial thromboplastin time (aPTT)
- Typing
- Screening
- Imaging studies
- CT scan is the first imaging choice in an emergent setting in which a patient is thought to have an intracranial bleed. It is fast and widely available.
- CT angiography provides better vascular detail than MRI or magnetic resonance angiography (MRA), and can be performed in most emergency rooms. It can be a useful non-invasive alternative to cerebral angiography.
- MRI is the first imaging choice in a nonemergency setting (eg, workup of seizure, headache, or neurologic deficit). It provides significantly greater resolution and flexibility in diagnosis. MRAs can reveal the anatomy of the AVM noninvasively but have lower resolution than conventional angiography and do not provide functional information. MRI is useful compared to computed tomoangiography (CTA) or cerebral angiography in that it provides better visualization of the surrounding cerebral structures. Functional MRI can assist in treatment planning by defining the functionality of adjacent brain.
- Cerebral angiography provides definitive diagnosis. It documents a functional AV shunt; however, because it is an invasive test, it is not performed as the first imaging study. Cerebral angiography also allows grading of the AVM via the following Spetzler and Martin criteria.
- The Spetzler-Martin grading system described in Table 1 helps predict the likelihood of satisfactory outcome if an attempt at surgical resection is made. The Spetzler-Martin grade is determined by adding the 3 individual scores from the table. High-grade AVMs are more difficult to resect, and, therefore, neurologic deficits from the surgery itself are more likely. Other grading systems have been proposed for radiosurgery planning.
Spetzler-Martin Grading System for AVMs
Open table in new window
Table
| Size of AVM* | Eloquence of adjacent brain† | Pattern of venous drainage‡ | |||
| Small (<3 cm) | 1 | Noneloquent | 0 | Superficial only | 0 |
| Medium (3-6 cm) | 2 | Eloquent | 1 | Deep component | 1 |
| Large (>6 cm) | 3 | … | … | ||
| Size of AVM* | Eloquence of adjacent brain† | Pattern of venous drainage‡ | |||
| Small (<3 cm) | 1 | Noneloquent | 0 | Superficial only | 0 |
| Medium (3-6 cm) | 2 | Eloquent | 1 | Deep component | 1 |
| Large (>6 cm) | 3 | … | … | ||
* Measure the largest diameter of the nidus of the lesion on angiography.
† Eloquent areas include sensorimotor, language, visual, thalamus, hypothalamus, internal capsule, brain stem, cerebellar peduncles, and deep cerebellar nuclei.
‡ The lesion is considered superficial only if all drainage is via the cortical drainage system.
Treatment
Trials directly comparing treatment approaches are lacking, and information on outcomes derives largely from case series. Complete obliteration is the goal of treatment as partial obliteration does not affect the rate of hemorrhage.
- Surgery (craniotomy)
- Advantages: Cure is immediate and permanent after complete resection by craniotomy. Surgery is generally recommended for grade 1, 2, and 3 lesions, sometimes for grade 4 lesions, and not for grade 5 lesions.
- Disadvantages: The potential for significant intraoperative bleeding, damage to adjacent neural tissue, and ischemic stroke are disadvantages. The "arteries of passage" supply intact neural tissue and must not be destroyed while attempting to interrupt the arterial supply to the AVM. A risk also exists for perfusion-breakthrough bleeding, ie, hemorrhage into the healthy part of the brain caused by sudden hemodynamic shifts, which results from the removal of a large AV shunt and the subsequent increased flow to previously underperfused vessels. Reports of rates of permanent neurologic deficit range from 0-15%, while mortality rates are close to zero in Spetzler-Martin grades 1-3 AVMs. Much higher morbidity and mortality rates are reported with grades 4-5 AVMs.
- Endovascular neurosurgery (obliterating vessels with glues or particles delivered via arterial catheter in the angiography suite)
- Advantages: Significant reduction of pathologic blood flow through the lesion can be achieved. Its main use is as adjuvant therapy prior to craniotomy to decrease intraoperative bleeding and technical difficulty. It has also been used to decrease the size of an AVM to make it sufficiently compact for effective targeting by stereotactic radiosurgery. Embolization may be curative in lesions less than 1 cm in diameter that are fed by a single artery. Improved obliteration rates of approximately 20% have been reported when using the embolic agent Onyx.
- Disadvantages: This is an invasive procedure, and its major risks are similar to those for open surgery, ie, ischemia and hemorrhage. The main risk is causing ischemic stroke by occluding a feeding vessel that also supplies normal brain. Postembolization hemodynamic alterations can cause rupture of the AVM, resulting in new neurologic deficit from subarachnoid and/or intraparenchymal hemorrhage, analogous to the perfusion-breakthrough bleeding described above. This technique is not normally used by itself, as it rarely achieves complete eradication of the lesion and the pathologic vessels usually recanalize over time.
- Stereotactic radiosurgery
- Advantages: Stereotactic radiosurgery is noninvasive and can access all anatomic locations of the brain. New techniques available include staged radiosurgery for larger lesions (Grade IV and V), which has promising results.
- Disadvantages: It can only treat smaller lesions (<3 cm in diameter) and requires 2 or more years for a full destructive effect. The risk for hemorrhage is not reduced during this lag time. The risks of radiation necrosis of adjacent healthy tissue or cyst formation also exist. The cure rates for lesions smaller than 3 cm range from 81-90%. Therefore, a small subset of these lesions still hemorrhage after treatment.
- Combination therapy
- Total eradication of the lesion may require more than one modality. Partial treatment may increase the risk of hemorrhage.
- Endovascular neurosurgery can be performed before surgical excision to reduce the difficulty of surgery or before radiosurgery to bring the size of the lesion to within the limits of the machine.
- Radiosurgery may be used to eradicate small residual disease left after craniotomy (due to technical difficulty or involvement of eloquent structures).
- Aneurysms associated with AVM
- Aneurysms on an artery that does not feed the AVM can be managed as any unruptured intracranial aneurysm.
- Aneurysms less than 5 mm in size have been reported to regress after treatment of AVM; in other cases, they have ruptured after treatment.
- Given concern about aneurysms greater than 5 mm, treatment via microsurgical clipping or endovascular coiling is generally done prior to the treatment of the AVM.
Outcome and prognosis
Prognosis for untreated AVMs has been reported to include either a 2-3% or a 4% (depending on study cited) risk of bleeding per year, with an approximate 10% mortality rate associated with the bleed. Some studies suggest a 1% yearly mortality risk. The yearly combined major morbidity and mortality risk has been reported to be 2.7%. This figure includes only new clearly fixed neurologic deficits. It does not include other problems, such as seizures, personality changes, or memory disturbances, which also may have a significant disabling impact on the patient's life and functioning.
Risks of conservative management and surgical intervention vary dramatically depending on the location and specific characteristics of individual lesions, which must be considered when applying this data to each patient.
Typically, attempts should be made to completely eradicate the lesion. Regardless of which method or combination of methods is used for treatment, eradication is considered definitive and recurrence is not a concern (except in occasional reports in the pediatric population).
Outcomes for patients with a subarachnoid hemorrhage caused by an AVM are better than outcomes for patients with a subarachnoid hemorrhage caused by an aneurysm. Outcome studies suggest that most patients return to full preoperative psychosocial function.
Future and controversies
Multidisciplinary teams likely will become increasingly important for optimal management of each individual patient. Such teams may include neurosurgeons, interventional neuroradiologists, and stereotactic radiation specialists. Continuing advances in microsurgical, neurointerventional, and radiosurgical techniques will affect approaches to treatment. Algorithms guiding whether to treat or follow particular lesions will evolve. Advances in the efficacy and safety of the available interventions may emerge. Patients' individual psychological factors will remain critical. For every patient, the immediate risks of intervention versus the likelihood of cure must be balanced.
A Randomized Trial of Unruptured Brain Arteriovenous Malformations [ARUBA], an ongoing multicenter randomized trial, is comparing treatment of unruptured lesions with conservative management. This study will be of great assistance in management decisions when the results are published.2
Cavernous Angioma
Introduction
Cavernous angiomas are also known as cavernous hemangiomas or cavernomas. They can occur anywhere in the central nervous system. Occurrence is usually sporadic, but a significant proportion of cavernous angiomas are familial.
Frequency
These lesions were thought to be rare until the advent of MRI. They have since been identified in 0.5-1.0% of the population.
Genetics
Three autosomal dominant genes are associated with the familial form. The precise function of these gene products are not known. They are as follows:
- ccm1 on 7q chromosome and expresses KRIT1
- ccm2 on 7p chromosome and expresses MGC4607
- ccm3 on 3q chromosome and expresses PCD10
Pathology
Cavernous angiomas consist of enlarged capillaries with characteristics as follows:
- Sinusoidal
- Single layer of endothelium
- Thin collagenous wall
- Lack of smooth muscle fibers and elastic fibers
Capillaries are immediately adjacent to each other, with no intervening neural tissue. They typically are not associated with enlarged feeding arteries or draining veins, and blood flow is low or even stagnated. Grossly, they may range from soft to hard. Thrombosis, calcification, or ossification results in a harder lesion.
Hallmark pathologic appearance:
- Blood leakage (This results in hemosiderin staining; iron salts may incite an epileptogenic focus.)
- Gliotic reaction in the adjacent brain
One review of the literature reported the following incidences among those lesions that become symptomatic:
- Seizure (39%)
- Hemorrhage (32%)
- Mass effect (29%)
A significant percentage of lesions are asymptomatic, although accurately determining the frequency of asymptomatic lesions is difficult. Studies indicate that one tenth to one quarter of lesions are symptomatic. New research is suggesting that certain immune responses may be associated with proliferation and hemorrhage of cavernous malformations.
Occurrence generally is sporadic. One study revealed increased prevalence in Mexican American families, who also are more likely to have multiple lesions.
Lesions may be demonstrated on brain imaging studies, as follows:
- CT scans may show focal hyperdensity, reflecting calcification or recent hemorrhage or mass effect, and intravenous contrast may show faint enhancement.
- Cerebral angiograms demonstrate no vascular abnormalities. Although 8% of developmental venous anomalies have an associated cavernoma, which can be seen on angiography.
- MRI scans reveal well-defined lesions on T1 and T2 sequences with sensitivity and specificity nearing 100%. The hemosiderin ring is visualized on a T2 sequence. Blood products of various ages can be observed in the center, and local edema may be present.3
Treatment
Surgical removal eliminates mass effect and hemorrhage risk. It also removes the seizure focus. When the lesion is in a surgically accessible location, surgical removal can often be accomplished with relative ease and minimal risk. Functional MRI scans preoperatively may make resection safer. Brainstem cavernomas can be resected if the lesion reaches a pial surface. Currently, the role of radiosurgery is still debatable due to lack of follow-up studies and a reliable method to detect active lesion on radiographic examinations.
Prognosis
One study showed a 0.7% annual hemorrhage rate in cases of lesions followed prospectively. This rate increases dramatically if lesion enlargement within one year is documented. The estimated lifetime risk for hemorrhage, epilepsy, and other neurological sequelae are 50-70%. Intractable seizures, increase in lesion size on MRI, and an incident of gross hemorrhage are indications for removal of surgically accessible lesions.
Symptomatic lesions are likely to remain symptomatic or progress, but patients treated surgically experience remission or a reduction of symptoms. Approximately 50% of patients experience elimination of seizures, and the remainder have a decreased frequency of seizures. Elimination of seizures is more likely if the patient has not had seizures for many years. Successfully excised lesions are considered cured, and recurrence is not a concern.
Venous Angioma
Introduction and pathology
The venous angioma, also known as a developmental venous anomaly, is the most common type of intracranial vascular malformation, as determined by incidental findings at autopsy. One autopsy study estimated a prevalence of 2.6%.
Pathologically, a venous angioma is an enlarged collection of veins. The architecture is essentially normal, except for the size. The veins receive drainage from adjacent healthy tissues. The veins appear as a radial arrangement, all converging on an enlarged central venous trunk. This trunk drains into healthy superficial or deep venous systems. No interruption of physiologic drainage occurs; therefore, the lesions are considered anomalies rather than pathological structures. Venous angiomas are postcapillary structures and are not associated with abnormal arteries.
Presentation, treatment, and prognosis
Venous angiomas frequently are incidental radiographic findings, although some patients may present with intracranial hemorrhage. Patients also may present with a seizure or focal neurologic deficit. Posterior fossa lesions are more likely to result in a deficit.
Angiograms usually have a "hydra" or caput medusae appearance, resulting from the image of smaller radial veins converging on a central draining venous trunk. CT scan or MRI reveals a curvilinear structure that is described as resembling the spokes of a wheel. CT scans also may reveal a rounded enhancing area. MRI images may have sufficient resolution to reveal the caput medusae form.
Venous angioma has either no or very low risk of hemorrhage. Generally, patients are completely asymptomatic, and their cases should be followed conservatively.
Excision or ablation of venous angiomas is avoided. The angioma may be part of normal venous drainage for adjacent healthy neural tissue. Therefore, excision can lead to venous infarction of this tissue and significant morbidity and mortality.
Because many lesions are clinically silent and likely to escape diagnosis, comparing the natural history and associated prognosis of treated lesions versus untreated lesions is difficult.
Importantly, venous angiomas have been postulated to be pathophysiologically related to cavernous angiomas. In the case of a hemorrhage associated with a venous angioma, investigate for an adjacent cavernous angioma. If a cavernous angioma is found, resect the clot and the cavernous angioma, but do not resect the venous angioma.
Capillary Telangiectasia
Introduction and pathology
The presence of capillary vessels with saccular or fusiform dilations characterizes capillary telangiectasias. These vessels lack muscular and elastic components in their walls. They are intercalated among healthy brain parenchyma. They are not associated with gliosis. Typically, no evidence of associated hemorrhage is present. Upon gross inspection, they are tiny lesions having the appearance of punctate hemorrhages.
Capillary telangiectasias almost always are clinically silent and not detectable radiographically. They are found incidentally on autopsy. Clinically significant intracranial hemorrhage has been reported very rarely.
These lesions may be related pathologically to cavernous angiomas. Some recommend considering the 2 as a single entity, referred to as capillary malformation.
Presentation, treatment, and prognosis
Most capillary telangiectasias are clinically silent and are found incidentally on autopsy. Rare anecdotal reports of substantial hemorrhage exist. Previously, these lesions were undetectable radiographically. However, they may be visualized as a tiny area of hypointensity on T2-weighted MRI scans. These hypodensities may represent previous subclinical hemorrhage.
No treatment is indicated.
Importantly, capillary telangiectasias have been postulated to be pathophysiologically related to cavernous angiomas. Transitional forms with vessel histology sharing features of each entity have been described.
Multimedia
 | Media file 1: A 44-year-old woman presented with left-sided hemiparesis and intraventricular hemorrhage on her head CT. This axial T2-weighted MRI shows arteriovenous malformation nidus on the right side. The arrows demonstrate large draining veins within the right lateral ventricle. |
 | Media file 2: This anteroposterior projection of the right internal carotid artery angiogram shows the outline of the arteriovenous malformation (AVM). Arrows indicate the internal carotid artery (ICA), deep draining vein (Vein), and artifact from a previously placed aneurysm clip (Clip). |
 | Media file 3: This lateral late-phase angiogram shows extensive venous drainage and a focal stenosis of venous outflow (arrow) contributing to raised intracranial pressure. This is a Spetzler-Martin grade 5 arteriovenous malformation (AVM), 3 + 1 + 1. The patient underwent partial treatment by embolization but had a fatal hemorrhage 2 years later. |
 | Media file 4: A 32-year-old woman presented with visual seizures. Sagittal T1-weighted MRI is consistent with an occipital arteriovenous malformation. |
 | Media file 5: This axial T1-weighted MRI with gadolinium contrast shows enhancement of the left occipital arteriovenous malformation. |
 | Media file 6: This lateral projection of a left internal carotid artery angiogram shows feeding vessels from the middle cerebral artery (MCA) and posterior cerebral artery (PCA). |
 | Media file 7: This lateral projection of a left internal carotid artery angiogram was taken after partial embolization. The embolization was of the posterior cerebral artery feeders. |
 | Media file 8: This lateral projection of a left internal carotid artery angiogram was taken after surgery. The arteriovenous malformation has been obliterated. |
 | Media file 9: This postoperative sagittal T1-weighted MRI shows artifacts from metal clips used in removing the arteriovenous malformation (AVM) but no evidence of residual arteriovenous malformation. |
 | Media file 10: A 25-year-old man presented with acute onset of severe headache. Emergent noncontrast head CT scan reveals right frontal hemorrhage. |
 | Media file 11: This lateral projection of a right internal carotid artery angiogram shows arteriovenous malformation (AVM) nidus. |
 | Media file 12: This shows a lateral projection of a right internal carotid artery angiogram after surgery. This image shows elimination of nidus and subsequent elimination of arteriovenous shunting. |
 | Media file 13: CT angiogram provides 3-dimensional visualization of the arteriovenous malformation nidus (arrowheads), feeding artery (black arrow), and draining vein (yellow arrow). |
 | Media file 14: A 29-year-old woman presented with generalized seizure. Noncontrast head CT scan demonstrates a high-signal well-circumscribed lesion in the right Sylvian fissure. |
 | Media file 15: An axial T1-weighted MRI better delineates the margin of the lesion and demonstrates blood products within the lesion. |
 | Media file 16: A coronal T1-weighted MRI with gadolinium contrast shows minimal enhancement of the lesion. |
 | Media file 17: An axial T2-weighted MRI shows the circumferential hemosiderin ring classic for cavernous angioma (indicated by arrows). |
 | Media file 18: This intraoperative photograph shows the opened Sylvian fissure, with the cavernous angioma exposed (indicated by arrows). |
 | Media file 19: A 30-year-old woman presented with headaches. MRI demonstrated a dilated vein consistent with arteriovenous malformation (AVM). However, this lateral projection late-phase view of an internal carotid artery injection demonstrates the classic caput medusae draining pattern of a venous angioma. The 4 arrows indicate smaller veins converging on the large central draining vein. Note the subsequent drainage to normal structures (the superior sagittal sinus in this case). |
Keywords
intracranial arteriovenous malformation, arteriovenous malformation, intracranial arteriovenous malformations, arteriovenous malformations, AVM, cavernous angioma, cavernoma, venous angioma, capillary telangiectasia, vascular abnormalities, vascular malformation, vascular malformations, AVMs, brain abnormality, vascular abnormality, brain abnormalities, cerebral arteriovenous malformation, brain arteriovenous malformation, brain arteriovenous malformations
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Further Reading
Keywords
intracranial arteriovenous malformation, arteriovenous malformation, intracranial arteriovenous malformations, arteriovenous malformations, AVM, cavernous angioma, cavernoma, venous angioma, capillary telangiectasia, vascular abnormalities, vascular malformation, vascular malformations, AVMs, brain abnormality, vascular abnormality, brain abnormalities, cerebral arteriovenous malformation, brain arteriovenous malformation, brain arteriovenous malformations
