ARTERIOVENOUS MALFORMATIONS OF THE BRAIN AND SPINAL CORD

Published on 10/04/2015 by admin

Filed under Neurology

Last modified 22/04/2025

Print this page

rate 1 star rate 2 star rate 3 star rate 4 star rate 5 star
Your rating: none, Average: 3 (1 votes)

This article have been viewed 2013 times

CHAPTER 44 ARTERIOVENOUS MALFORMATIONS OF THE BRAIN AND SPINAL CORD

Soke Miang Chng, Hortensia Alvarez, Georges Rodesch, Pierre Lasjaunias

An arteriovenous malformation (AVM) consists of one or more arteriovenous shunts, which corresponds to an abnormal capillary bed with a shortened arteriovenous transit time. Two broad categories of arteriovenous shunts can be recognized: AVMs and arteriovenous fistulae (AVFs). AVMs are characterized by a network of abnormal channels (nidi) between the arterial feeders and the draining veins. AVFs, in contrast, consist of a direct communication or opening between a feeding artery and a draining vein. AVMs and AVFs are the two basic forms of arteriovenous shunts that can be found throughout the central nervous system.

AVMs of both the brain and the spinal cord are not common diseases. Spinal cord AVMs (SCAVMs) in particular are still underdiagnosed entities that can give rise to acute-subacute spinal cord symptoms or progressive myelopathy. Clinical signs and symptoms vary, depending on the location and angioarchitecture of the lesion.

A complete clinical evaluation combined with imaging information are necessary for making the correct therapeutic decision. The primary diagnostic modality is currently magnetic resonance imaging (MRI), which is excellent in topographically localizing lesions. Digital subtraction angiography (DSA) gives important complementary information regarding the angioarchitecture and hemodynamics of lesions, which is crucial in treatment planning. The aim of treatment should be a significant improvement over the natural history of the disease, in comparison with the risks of therapy.

In the past, most AVMs were diagnosed during clinically recognized episodes. The access to imaging facilities has allowed their preclinical diagnosis. Follow-up of this incidentally discovered population of patients with AVMs suggests that the clinical course is more benign than previously believed. The classic postulate that AVMs are congenital malformations, hence implying their presence at birth, has not been supported by antenatal or pediatric imaging. On the contrary, it is likely that lesions found in young adults, although probably resulting from an early in utero “event,” are not present at birth. Pediatric cases or even neonatal series represent only a small portion of the cases and pertain to specific disease groups (hereditary hemorrhagic telangiectasia [HHT], vein of Galen malformations, pial AVFs).1

The purpose of this chapter is to give an overview of the classifications, angioarchitectures, clinical manifestations, and natural history of these diseases, with a brief review of the diagnostic and therapeutic approaches.

BRAIN ARTERIOVENOUS MALFORMATION

Incidence

The prevalence of brain AVMs (BAVMs) in a given population is difficult to estimate. It is believed that between 0.14% and 0.8% of the population may present with a BAVM in a given year.2,3 The variation in statistics results from studies of disparate populations, ranging from the residents in a small community4 to subjects of autopsy series.3 As previously alluded to, these numbers represent data collected before the era of noninvasive high-quality imaging modalities.

Classification and Angioarchitecture

There are two broad categories of arteriovenous shunts: malformations (AVMs) and fistulae (AVFs). AVMs may be small (micro-AVMs) with one or more “normal”-sized arteries, one or more draining veins, and a nidus smaller than 1 cm in diameter. Macro-AVMs, in contrast, have arteries and veins that are larger than normal; the size of the nidus is larger than 1 cm in diameter. Compartments can be observed within lesions either during angiography or at surgery. Each compartment may have a single or multiple arterial feeders. There may be single or multiple draining veins (Fig. 44-1).

image

Figure 44-1 Arteriovenous malformation (AVM) in the brain. The patient, a 57-year-old woman, presented with chronic headache for several years. There was no associated seizure or neurological deficit. A and B, Magnetic resonance imaging (axial T2-weighted images) showed a nidus-type AVM located in the left precentral sulcus, displacing the precentral gyrus anteriorly. This AVM drained via a superficial cortical vein. C, Angiography (left carotid injection, arterial phase) showed the corresponding precentral cortical vein draining into the superior sagittal sinus.

Similarly, AVFs may be of the micro or macro type. AVFs are more frequent in children and are rare in adults (Fig. 44-2).

image

Figure 44-2 Brain arteriovenous fistula (AVF). The patient, a 4-year-old girl, presented at the age of 3 years with language delay. There was no family history to suggest hereditary hemorrhagic telangiectasia. A and B, Magnetic resonance imaging (coronal T2-weighted and axial fluid-attenuated inversion recovery images) revealed a single-hole AVF located in the left sylvian fissure, associated with a large venous pouch. C and D, Angiography (left carotid injection in the frontal and lateral projections) showed a single, ectatic arterial feeder arising from the left middle cerebral artery, opening directly into the venous pouch. Venous drainage was via an embryonic tentorial sinus into the left sigmoid sinus, with reflux into the opposite transverse and sigmoid sinuses. Embolization of this fistula was subsequently performed.

The architecture of an AVM is specific to the lesion. However, the chronicity of the shunt and the shear stresses on the remaining vasculature create nonmalformative secondary changes called high-flow angiopathy. These may by themselves create additional symptoms; under certain circumstances, they may also regress if the AVM is treated even partially.

Topography

The topography of a BAVM is best assessed by combining both MRI and angiographic information. Lesions in most locations recruit predictable arterial feeders and specific draining veins (Table 44-1). The primary defect is at the capillary level. In contrast to aneurysms (arterial defective) or cavernomas (venous defective), in which associated arterial and venous anomalies are seen, respectively, the arterial tree from where the AVM feeders originate and the venous system that drains the AVM have a classic anatomical disposition.

image

TABLE 44-1 Topography of Intracranial Arteriovenous Lesions and Vascular Territories

Rights were not granted to include this table in electronic media. Please refer to the printed book.

From Berenstein A, Lasjaunias P, Ter Brugge KG: Surgical Neurorangiography, vol 2.2: Clinical and Endovascular Treatment Aspects in Adults, 2nd ed., Berlin: Springer-Verlag, 2004.

Several general types of lesions can be differentiated on the basis of location. Of note, however, is that both macro- and micro-AVFs are encountered mostly on the surface of the brain. All so-called BAVMs are subpial in location with regard to the meningeal spaces. Vein of Galen aneurysmal malformation and adult choroidal AVMs are separate groups located outside the subpial space.

Lesions at the cortex

Arteriovenous lesions exclusively involving the cortex are exclusively fed by cortical arteries and drain into superficial veins. These lesions represent sulcal AVMs, as described by Valavanis and Yasargil.5

Cortical-subcortical lesions recruit cortical arteries and drain into superficial veins but may also drain into the deep venous system if the transcerebral venous system is patent. These represent the gyral type of AVMs described by Valavanis and Yasargil.5

In both cortical and cortical-subcortical lesions, some regions of the cortex drain to deeply located veins that should not be considered as truly part of the “deep venous system.” Such vessels include the medial veins of the temporal lobe and the basal vein of Rosenthal, the veins of the cerebellar vermis, and the precentral cerebellar veins.

Corticoventricular arteriovenous lesions correspond to the classic pyramid-shaped malformation, reaching the ventricular wall at their apex. Feeding arteries are both perforating and cortical. Draining veins are also deeply and superficially located.

Corticocallosal lesions belong to the corticoventricular group, inasmuch as they have the same venous characteristics, but they do not recruit “basal perforating” arteries. They drain into the subependymal veins and, later, into the deep venous system. The arterial supply to the corpus callosum is linked to the cortical arterial network (even though it may simulate perforating arterial channels in the supraoptic region) and to choroidal arteries at the splenium.

Deep-seated lesions

Deep-seated lesions can be located supratentorially or infratentorially in the depth of the telencephalon, diencephalon, brainstem, or cerebellum. The nidus involves the deep nuclei and the long fiber tracts with their arterial and venous connections. They recruit exclusively perforating arteries and drain into the deep venous system. They may use transcerebral veins if patent, either as a direct venous outlet or as a collateral pathway. Transcortical arteries from the insular branches of the middle cerebral artery and the hemispherical collateral vessels of the cerebellar arteries can be involved in lenticulostriate and in dentate nuclear lesions, respectively. MRI and DSA are able to distinguish these deep-seated lesions from corticosubcortical lesions, particularly because the dominant supply of the intracerebrally located deep lesions arises from the perforators.

Choroid plexus lesions

Choroid plexus AVMs are important to recognize because of their extra-axial location. These lesions are fed by choroidal and subependymal arteries arising from the circle of Willis. There is no cortical arterial supply in this type of lesion. Drainage is via ventricular veins, with occasional recruitment of transcerebral veins. These extra-axial lesions, too, can be distinguished from intra-axial ones with angiographic criteria.

Angioarchitecture

Analysis of the angioarchitecture of BAVMs should include the study of the various components of the lesion (arteries, nidus, and veins) and how these components affect the rest of the circulation. The clinician should be able to distinguish the primary abnormality (the BAVM) from the secondary changes (high flow angiopathy) that occur in response to an increased diastolic fraction resulting from arteriovenous shunting. These include arterial stenosis, aneurysms, angiectasia, venous stenosis and ectasia, and angiogenesis. The high-flow hemodynamics and/or decreased tissue perfusion associated with chronic arteriovenous shunting stimulate these angiogenetic developments. Thrombosis of a draining vein, development of transdural supply, or intranidal ectasias may also be observed after previous hemorrhage within the AVM. These changes may be temporary or permanent.

Calcifications

Calcifications in BAVMs are usually related to venous ischemia. In children, calcifications may occur at a distance from the shunt, in watershed venous zones, in the white matter, or in the deep nuclei.

Multiple Brain Arteriovenous Malformations

Multiple BAVMs are rare. In this heterogeneous group of multifocal BAVMs, three types of patients can be distinguished: (1) those with HHT, also known as Rendu-Osler-Weber disease; (2) those with cerebrofacial arteriovenous metameric syndrome (CAMSs); and (3) those with unclassified multiple lesions. This distinction refers to the timing of the insult that created the malformations, later to be revealed morphologically or clinically (e.g., germinal, somatic-segmental).

Hereditary hemorrhagic telangiectasia

HHT is an autosomal dominant disorder characterized by a multisystemic vascular dysplasia and recurrent hemorrhage.6 Two gene mutations have been identified: on chromosome 9 (affecting production of endoglin; this form is known as type 1)7 and on chromosome 12 (affecting production of activin receptor-like kinase; this form is known as type 2). An uncharacterized third mutation is also suspected. These mutations lead to the formation of abnormal vessels and abnormal connections between vessels. It has to be emphasized that the target of dysfunction in HHT is not in arteries but in venules.

In the general population of patients with BAVMs, up to 2.2% of cases may be associated with HHT.8 With multiple BAVMs, however, up to 25% of cases are associated with HHT.9 Ten percent to 20% of HHT patients have cerebral involvement.10 In these patients, the cerebral vascular malformations manifest in three main phenotypes: large AVFs, small AVMs with a nidal diameter between 1 and 3 cm, and micro-AVMs with a nidal diameter smaller than 1 cm. These AVMs are often multiple and are almost exclusively located near the cortex.8,11 Although characteristic telangiectasia occur in the skin, oral mucosa, and the lips of patients with HHT, telangiectasia is not known to develop in the brain. High-flow type AVFs with venous ectasias are seen in children younger than 5 to 6 years of age; nidus-type lesions both large and small are seen in older children and in adults.1,12–14 Twenty-five percent of single AVFs in children and 50% of multifocal AVFs occur in patients with HHT.

Cerebral DSA may demonstrate multiple areas of arteriovenous shunting, always cortical in location, either supratentorial or infratentorial. In addition, high-quality cerebral DSA can demonstrate tiny lesions, particularly micro-AVMs, which may appear occult on MRI, because these lesions usually have normal-sized feeding arteries and draining veins.10

However, patients with HHT who present with systemic complaints are more likely to develop acute neurological symptoms from embolic phenomena related to underlying pulmonary AVFs (recurrent brain abscesses, embolic stroke) than to the presence of a BAVM per se.

Cerebrofacial arteriovenous metameric syndromes

CAMSs,15 also called Wyburn-Mason or Bonnet-Dechaume-Blanc syndrome, are associated with ipsilateral AVMs of the brain, retina, and facial regions. Their segmental expression reflects their common origin from tissues involved in cerebrofacial vasculogenesis and angiogenesis. The metameric pattern of involvement is suggestive of a disorder of the neural crest or adjacent cephalic mesoderm15 at early segmental stages of differentiation.

Unclassified multiple brain arteriovenous malformations

Several case reports have described so-called multifocal BAVMs. They seem to be twice more frequent in children than in adults. They can be randomly spread on the cortex; mirror-image deep-seated nidi have been reported. One half of multifocal AVFs in children belong to this group.1,14

False Arteriovenous Malformations

Proliferative and hemorrhagic angiopathies

Proliferative and hemorrhagic angiopathies are entities often confused with BAVMs. They are rare, proliferative, vascular lesions seen usually in children and young women.

The appearance of proliferative angiopathy is typically that of a nidus-like cortical network of vessels intermingled with normal brain parenchyma, and the veins are either normal sized or only slightly enlarged. The “nidus” is typically diffuse, involving a hemisphere. There are no dominant arterial feeders. The early venous filling that is observed results from a faster capillary transit time rather than true arteriovenous shunting. Late proximal cerebral arterial occlusion may occur, resulting in ischemic phenomena and diffuse transdural angiogenesis. The most common clinical manifestation is seizures. Headaches and progressive neurological deficit are less common, and hemorrhage is exceptional. Treatment is directed at the management of seizures with medical therapy. Embolization is employed in exceptional cases: when there is evidence of focal angioarchitectural weakness within the lesion, for which partial targeted embolization to reduce any constraints to functional parts of the brain may be beneficial. The effects of medication on headaches and seizure are often beneficial. The role of surgery is limited to the correction of hemispherical ischemia by bur holes, as in moyamoya disease, when spontaneous transdural angiogenesis is absent or insufficient.

Hemorrhagic angiopathy is another entity that typically manifests with an episode of hemorrhage. Encountered in some rare cases of intracerebral hematomas in children most often after the age of 5 years, it corresponds to a network of intracerebral subcortical arterioles with normal structure and sequential venous drainage. Recurrent hemorrhage is frequent and therefore therapy is indicated. These lesions are extremely sensitive to radiation. Partial embolization of focal areas of weakness in the angioarchitecture can also be performed to reduce future hemorrhagic risk.

Developmental venous anomalies with ectasias

Developmental venous anomalies (DVAs) are anatomical variations that can involve one or both hemispheres and can also be located infratentorially. They involve extremes in variations in the venous drainage of white matter. Superficial DVAs represent the superficial medullary veins that drain the deeper medullary regions into the cortical veins. The deep group of DVAs drains the subcortical territories of the superficial medullary veins into the deep venous collectors. The venous channels are morphologically normal and drain normal functioning brain, although transit time through their venules is sometimes rapid and almost as rapid as that in slow-flow BAVMs. The frequent incidental appearance of DVAs on cross-sectional imaging and angiography attest to their benign nature. Any associated clinical symptom is caused primarily by associated malformations (cavernomas or arteriovenous shunts). Their lack of flexibility as a result of being an anatomical variant of the venous drainage to the brain in the region may also produce ischemic episodes of varying severity. However, because DVAs drain normal areas of the brain, they should never be eradicated. Rarely does a true AVM drain into a DVA. In this instance, a true arteriovenous shunt is demonstrated within an otherwise normal network of vessels. Treatment of such patients requires extreme care to preserve normal venous channels.

Pathophysiology, Clinical Manifestation, and Natural History

The clinical manifestation of BAVM may be related to the shunt itself or to secondary changes (visible on high-flow angiopathy) that occur in response to chronic shunting. It also depends on the age of the patient. Manifesting clinical features include chronic headaches, seizures, cerebral hemorrhage, and neurological deficits.

Neonates, Infants, and Children

Neonates with BAVMs may present with high-output cardiac failure related to the presence of high-flow shunts in the AVM.

In young children, alterations in cerebrospinal fluid circulation and absorption in the immature brain caused by increased venous pressure may lead to water retention, macrocrania, and hydrocephalus, and venous congestion may rapidly lead to focal ischemia, convulsions, and hemorrhage. Melting-brain syndrome can occur in neonates and young infants. This involves a rapid destruction of the brain, usually the white matter, with ventricular enlargement. This phenomenon, which is never encountered in adults, corresponds to a regional decrease in the cerebral blood flow caused by retrograde venous hypertension and subsequent venous congestion leading to hydrovenous dysfunction. It is usually bilateral and symmetrical, associated with severe neurological manifestations and no signs of increased intracranial pressure, although they are usually present before the syndrome manifests.

Hemorrhage

Hemorrhage in a patient with a BAVM represents a significant change in the compliance of the vascular system. Bleeding can result from rupture of the AVM nidus, arterial aneurysm rupture, or venous rupture, which may occur close to or remote from the AVM. It has been shown that arterial aneurysms are not significantly associated with hemorrhagic manifestation,5 of BAVMs. The presence of aneurysms within an AVM nidus is, however, noted to significantly worsen the natural history of future hemorrhages.16 Deep venous drainage and deep location of a BAVM are associated with a higher risk of hemorrhagic manifestation.17

Seizure and Neurological Deficit

Seizure is the second most frequent manifesting symptom in all BAVM patients and occurs in up to 53% of cases. The AVM locations most frequently associated with seizure production are the motor-sensory strip and the temporal areas, representing close to 70% of cases of BAVM with seizures. For most of the less functional brain areas, seizure manifestations may be overlooked unless secondarily generalized. Neurological deficit not associated with hemorrhage, in contrast, is an infrequent symptom, occurring in only 8% of patients over a 10-year period.18

Neurological deficits and seizures may be caused by an AVM by several possible mechanisms: (1) ischemia, (2) hemorrhage, (3) direct or indirect mechanical compression, and (4) postseizure neurological deficit.

Arterial ischemia may theoretically result from two types of mechanism: a “steal” phenomenon or occlusive changes. The concept of “steal” is based on the angiographic nonvisualization of vessels in a normal area of the brain that should have been visualized at the time of injection. However, careful angiographic evaluation always demonstrates the “missing” branches through leptomeningeal anastomoses from adjacent territories, thus expressing the adaptability of the brain’s circulation. Arterial stenosis and occlusion proximal to an AVM may range in appearance from a single vessel narrowing to a moyamoya pattern. Such changes are usually slowly progressive, allowing for stepwise compensation, including leptomeningeal angiectasia, which accounts for their clinically silent development. These changes may eventually lead to progressive symptoms such as headaches, neurological deficits, and seizures. Multivariate analysis has shown that patients with such occlusive changes and angiogenesis may have lesser hemorrhagic risk than do patients without such changes.19

The concept of venous ischemia is accepted by most authors involved in the management of cerebral arteriovenous lesions but is rarely acknowledged for its significance. It is important to remember that 60% to 80% of the cerebral blood volume is located in the venules of the cerebral venous system. They have all the necessary characteristics for active exchange with the surrounding tissue, a testament to their role in nutrient exchange. Flow in venules in the white matter is bidirectional, allowing them to fulfill their nutrient role even in a retrograde manner. This function is disrupted with increasing pressure in the veins. The progressive nature of deficits in relation to some BAVMs and their fluctuation reflect the attempts of the collateral circulation to overcome increased pressure in the venous outlet of a shunt. Decreased tissue perfusion secondary to venous ischemia may produce virtually any type of neurological symptom (e.g., motor or sensory deficits, neuropsychological alteration, seizures). Most of the symptoms result in effects remote from the nidus. Posterior fossa AVMs may thus manifest with supratentorial manifestations. The greater the distance between the shunt site and its venous drainage into a dural sinus, the higher are its chances of interfering with the normal brain circulation.

The onset of seizures in a previously healthy individual may also reflect an acute change in hemodynamics, which may be caused by rerouting of drainage from the malformation through a vein that previously drained normal areas of the brain. The increase in pressure produces secondary neurological dysfunction of the affected areas of the brain, and seizures may result. New-onset seizures and headaches can also occur when venous thrombosis develops in association with a BAVM.

Headache

Headache is the first symptom in approximately 60% of patients with BAVM. These headaches can be divided into (1) those that accompany an episode of intracranial hemorrhage or venous thrombosis and (2) those that are more subacute or chronic in nature.

The acute headaches associated with hemorrhage or acute venous thrombosis typically manifest abruptly and are usually severe in nature, associated with photophobia, nausea, vomiting, convulsion, and loss of consciousness.

Constant headaches or episodes of throbbing (“migraine-like”) headaches can occur in the same patient. The headaches are often localized to the same side as the AVM. In most cases, the exact cause of the headache remains unclear, although in some patients, there may be a relationship between the angioarchitectural features and the headaches. Dural and posterior cerebral artery supplies to a BAVM are known to be potentially responsible for headaches that tend to disappear after embolization therapy, in our experience. Conversely, embolization of middle and anterior cerebral artery supply to a parietal lobe BAVM may worsen headaches if the posterior cerebral artery supply is increased after such embolization. It does not seem that transdural supply to an AVM causes headache; such a feature is suggestive of ischemia of the underlying cortex.

Diagnosis, Management, and Treatment

The current modes of therapy for BAVMs include endovascular embolization with glue (N-butyl cyanoacrylate), surgery, stereotactic radiation therapy, and or combined therapy. The type of treatment may vary from center to center and is dependent on physicians’ strengths and capabilities.

The discovery of a BAVM in a patient does not represent an automatic indication for treatment. There is growing evidence in both the surgical and endovascular literature that every BAVM is unique and that different BAVMs do not carry a similar risk for future symptoms.20 The risk associated with treatment should be lesser than that of the natural history of a particular lesion. The age of the patient is also important, and the therapeutic strategy should be based on the post-therapeutic clinical benefit expected over time and the therapeutic risks associated with therapy.

The treatment of BAVMs requires complete information with regard to the clinical circumstances and the imaging characteristics, including the angioarchitecture of the AVM and the brain. The angioarchitecture of the AVM influences both the approach to a lesion and the expected chances of reaching the therapeutic goal.

Imaging Modalities

The topographic location of a malformation is best assessed by MRI or computed tomography. MRI delineates accurately the location of the lesion and is more sensitive than computed tomography in demonstrating secondary effects on the brain parenchyma, particularly the changes in white matter edema secondary to chronic venous congestion and hemosiderin from previous hemorrhage. DSA, however, enables the anatomical identification of the arterial feeders, the angioarchitecture of the nidus, the draining veins, and the hemodynamic aspects of the shunt. The presence of other associated vascular lesions and significant arterial and venous variations, as well as the vascular anatomy and physiology of the normal cerebral vasculature, may also be visualized. This complete information is necessary in deciding and planning a treatment strategy.

New data from advanced MRI techniques such as diffusion-weighted imaging, perfusion imaging, and functional MRI with neuronal activation have also been useful in studying abnormal brain areas near or remote from the AVM nidus. These techniques are able to show hemodynamic and neuronal adaptive phenomena in the areas involved by the AVM and in the surrounding areas of the brain. For example, reduced cerebral perfusion in the areas around the AVM related to venous congestion may be demonstrated. Functional MRI with mapping of cortical function in relation to the AVM can also be performed. This information may help the clinician correlate clinical symptoms with their anatomical and functional substrate and influence any decisions about invasive therapy.21

Indications for Intervention

The information obtained by the angiographic investigation plays a key role in the decision about the need for treatment. This is based on the demonstration of evidence of weakness in the angioarchitecture, which may point to a potential instability. The presence of a pseudoaneurysm or an associated arterial aneurysm (on the feeding pedicle or in the nidus), venous thrombosis, outflow restriction, venous hyperpressure, venous pouches, or venous dilatations is a factor favoring active intervention. But when the risk of total elimination of the malformation (by either embolization or microsurgery or by a combination of therapies) is prohibitive, then a different management strategy, such as partial targeted embolization to eliminate the points of weakness to reduce further risk of hemorrhage, must be considered, rather than an attempt to achieve a complete cure of the lesion.

An important part of the management of incidentally discovered BAVMs is to provide the patient with information regarding the natural history as it may apply to the particular situation, as well as the treatment options and associated risks that are available in the local treatment environment. If no angioarchitectural weaknesses are demonstrated, a medical follow-up treatment strategy can be proposed with the patient reassured that he or she is expected to lead a normal, productive life without restrictions. However, the evolution of BAVMs is not linear, and biological events may produce unexpected changes, which may remain subclinical for a long time. Follow-up is therefore crucial in all patients, including those for whom a decision not to treat was chosen.

Follow-up is usually clinical with imaging (MRI), but if clinical or imaging changes are noted, then repeat angiography may be indicated.

Specific Factors Affecting Therapeutic Decisions

Hemorrhage

The treatment strategy after presentation with hemorrhage is dependent on how well the hemorrhage is tolerated. When surgical intervention is necessary to remove an intracerebral hematoma, excision of the malformation at the same time is sometimes possible. Most hemorrhages are well tolerated,22 and no immediate AVM treatment is usually necessary. There is seldom a need for urgent treatment after BAVM hemorrhage, and a treatment strategy can be planned accordingly. Careful analysis of the angioarchitecture is important in order to look for suspicious angiographic features that are probably responsible for the hemorrhage (prenidal or intranidal aneurysm, pseudoaneurysm). These represent an indication for early treatment targeted toward obliteration of such weak points (partial targeted embolization).

Large size of a BAVM is associated with increased risk of future hemorrhage.23 Partial targeted embolization with reduction of nidal size and specific angioarchitectural features has been shown to reduce future risk of hemorrhage.24

Seizures

Seizures occur at presentation in 10% to 53% of patients with BAVMs, the majority being partial or partial complex seizures. Subsequent seizure control with antiepileptic medication is achieved in most patients; therefore, seizure control by itself rarely becomes an indication for intervention. Refractory status epilepticus is an exception that may represent an indication for endovascular treatment, and such management has been successful in bringing seizure management under control. Worsening or new onset of seizures after treatment is rare.

Age

The younger the patient is at the time of presentation, the more likely it is that active treatment should be considered. Presentation at an early age represents an early imbalance between the lesion and host. Newborns with congestive heart failure are the most dramatic examples of such an imbalance. Hydrocephalus in infants may also be secondary to cerebrospinal fluid absorption abnormalities and may result in irreversible developmental delay if endovascular treatment is not undertaken. The melting brain syndrome may also develop rapidly in some young infants if treatment is delayed.25

Patients older than 60 years at presentation are at a higher risk of bleeding,18 up to 89% by 9 years, in comparison with a 15% risk in the same period for patients aged 20 to 29. In addition, in older patients, bleeding carries very high rates of morbidity and mortality, because the older brain has less plasticity to recover. This may influence the management strategy for partial targeted therapy to restore once again the equilibrium between host and AVM.

Modes of Therapy

The role of surgery, endovascular glue embolization, stereotactic radiosurgery, and/or combined therapy in the treatment of BAVMs varies from center to center, depending on the expertise available. The location of a malformation, the size, and deep venous drainage are the most important factors in determining the risks of surgical resection of an AVM,26 whereas these features are of only minor concern in the endovascular approach. Technically, morbidity associated with embolization is related to the capacity to reach the lesion endovascularly and to remain strictly within the nidus during glue embolization. Therefore, deep lesions such as brainstem, thalamic, or basal ganglia lesions, although obviously more risky to treat, can be obliterated by careful embolization, whereas surgery in such locations would carry much higher risks.

Stereotactic radiosurgery with the gamma beam, linear accelerator, or proton beam is another accepted mode of BAVM therapy. Radiosurgery leads to progressive occlusion of BAVMs by inducing vessel wall thickening, thrombosis, and, finally, occlusion of the vessel lumen. This occurs over a period of typically 2 years. During this period of 2 years, however, it does not provide immediate protection from future hemorrhage. The efficacy of radiosurgery also depends on lesion size and volume,27–29 the success rate being lower for large lesions, which require a much higher radiation dose. Radiosurgery is therefore generally an option for nidus-type lesions that are smaller than 3 cm and are not easily accessible via endovascular or surgical means.

Combination treatments may facilitate the complete cure of an AVM that might not have been possible with a single modality alone. Presurgical embolization has a well-accepted role in facilitating surgical removal of AVMs. Often, the role of endovascular embolization in such cases is to eliminate a deep arterial feeder, to occlude an intranidal fistula, or to reduce overall size and flow through the nidus before surgery. Embolization before radiosurgery may also be performed with the aim of achieving reductions in lesion size and volume, and embolization may be targeted toward specific angioarchitectural features such as intranidal aneurysms, false sacs, or intranidal fistulae.

When using combination therapy, the clinician must always bear in mind the increased therapeutic risk to the patient (combined risk of the different treatment modalities), and weigh this against the overall benefits of the combined therapy.

SPINAL CORD ARTERIOVENOUS MALFORMATIONS

Incidence

Vascular malformations of the spine and spinal cord are considered uncommon lesions. Their incidence, expressed as a percentage of the total number of the various types of spinal space-occupying lesions, ranges from 3%30 to 16%.31 The discrepancy is explained by the introduction of better diagnostic modalities. Nevertheless, the true incidence of spine and spinal cord vascular malformations may be underestimated.

Although cerebral vascular malformations are more common than spinal ones, the comparative incidence in relation to brain versus spinal tumors is very similar, ranging from 2% to 4%.32,33 This suggests that the frequency of SCAVMs in comparison with BAVMs is correlated with the mass or volume ratio between spinal cord and brain tissue. The prevalence of incidental or asymptomatic spinal vascular malformations is difficult to ascertain, inasmuch as the spinal cord is usually not inspected on routine autopsy.

Classification and Angioarchitecture

SCAVMs are arteriovenous shunts located intradurally and supplied by radicular arteries (radiculomedullary and radiculopial), the anterior spinal artery, the pial network, their perforators, or any combination of these. The lesion may be located along the surface of the cord (extramedullary), within the cord substance (intramedullary), or both. This group also includes AVMs that are located along the intradural portion of the spinal nerves and on the filum terminale. They are likely to be both subarachnoid and subpial because the pial veins of the cord are subarachnoid. These lesions are distinct from AVMs that are extradural or paraspinal in location and from spinal dural AVFs, which are located within or on the outer surface of dura along the spinal canal.

As in the brain, SCAVMs may be divided into nidal (AVMs) or fistulous types (AVFs). Nidus-type lesions are characterized by a network of abnormal channels (nidi) between the arterial feeders and the draining veins (Fig. 44-3). Fistula-type lesions, in contrast, consist of a direct communication or opening between a feeding artery and a draining vein (Fig. 44-4). Large nidus-type lesions are usually embedded within the spinal cord, whereas small lesions are often more superficial, near the surface of the cord. Fistula-type lesions, which may also be distinguished as large (macro-AVFs) and small (micro-AVFs), are always found on the surface of the spinal cord (extramedullary).

image image

Figure 44-3 Arteriovenous malformation (AVM) in the spinal cord. The patient, an 18-year-old man, presented with sudden onset of paraplegia associated with urinary symptoms. A and B, Magnetic resonance imaging (MRI) (sagittal T2- and T1-weighted images) showed a hematoma within the spinal cord at the second thoracic level, associated with cord edema extending from the upper thoracic to the cervical level. Dilated vessels were noted along the dorsal surface of the spinal cord. C and D, Angiography (left third thoracic intercostal artery injection) showed an AVM nidus associated with a false aneurysm sac, which corresponded to the hematoma seen on MRI. Dilated veins could be seen draining superiorly, with smaller veins draining inferiorly, contributing to venous congestion and cord edema. Embolization of this AVM was performed with glue (N-butyl cyanoacrylate), which succeeded in removing the false aneurysm during the first session.

image

Figure 44-4 Spinal cord arteriovenous fistula (AVF). The patient, an 11-month-old boy, had presented at the age of 3 months with progressive paraparesis, associated with increasing spasticity of the lower limbs and sphincteric problems. A, Magnetic resonance imaging (MRI) showed a large vascular pouch within the spinal canal. B, Angiography showed a macro-AVF. The vascular pouch seen on MRI was due to an ectatic venous pouch. The presence of a macro-AVF was suggestive of hereditary hemorrhagic telangiectasia, but no family history could be found. This fistula was successfully embolized with glue (N-butyl cyanoacrylate) in two sessions.

SCAVMs may be classified into three main groups (Table 44-2), described as follows.34

image

TABLE 44-2 Classification of Spinal Cord Arteriovenous Malformations

Rights were not granted to include this table in electronic media. Please refer to the printed book.

Rodesch G, Hurth M, Alvarez H, et al: Classification of spinal cord arteriovenous shunts: proposal for a reappraisal—the Bicêtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery 2002; 51:374-380.

Genetic Hereditary Lesions

This first group of SCAVMs is caused by a genetic hereditary disorder, in which vascular germinal cells are affected by disease. The main syndrome in which genetic links can be recognized is HHT (see section on BAVMs). SCAVMs associated with HHT are almost always single macro-AVFs, particularly in the pediatric population. Indeed, macro-AVFs may be the first expression of the disease in children; the discovery of a spinal cord macro-AVF should therefore raise the possibility of this underlying genetic hereditary disease.13,35 These lesions are usually single at the cord but can be associated to intracranial ones.36

Genetic Nonhereditary Lesions

This second group of SCAVMs is not related to a hereditary disorder; it includes multifocal lesions potentially sharing metameric links (see also section on BAVMs).37

Each segment in the spine involves the spinal cord (corresponding myelomere); nerve root; bone; and paraspinal, subcutaneous, and skin tissues. A patient may therefore present with multiple shunts, which involve several different myelomeres (segments) of the spinal cord (multimyelomeric SCAVMs) both on the cord and on intradural nerve roots. The association of a SCAVM with a nerve root AVM in the same patient is metameric if the spinal cord segment (myelomere) involved corresponds to that of the nerve involved.

This spinal arteriovenous metameric syndrome, also known as Cobb’s syndrome, can be numbered from 1 to 31, depending on its location at the vertebral and metameric levels.

Klippel-Trénaunay and Parkes-Weber syndromes are characterized by cutaneous capillary hemangiomas or port wine stains, varicosities and lymphedema, and bone and soft tissue hypertrophy of the affected extremity, usually the lower limb. Parkes-Weber syndrome is also associated with the presence of AVMs in the involved extremity. Associated SCAVMs are known to occur in these syndromes.34,38 In such cases, the SCAVMs are usually multiple, and a metameric disposition is suspected but cannot be definitely demonstrated.

Other multifocal spinal cord lesions have been described without metameric linkage.

Single Lesions

This third group of SCAVMs consists of all classic single lesions, either nidal or fistulous. This group may reflect an incomplete expression of one of the previously described situations and includes lesions of the spinal cord, nerve root, and filum terminale.

Clinical Presentation

In SCAVM series that include adults and children, the mean age of presentation is in the mid-20s.39–41 However, in close to 20% of cases, the lesion is diagnosed in children younger than 16 years of age.42 In a more recent series,43 30% were children.

Common clinical manifestations include acute neurological symptoms usually caused by hemorrhagic events, chronic progressive neurological deficit associated with venous congestion, and acute nonhemorrhagic symptoms.

Spinal Hemorrhage

The most striking symptom in the clinical presentation of SCAVMs is the high incidence of hemorrhage, which may be either subarachnoid or within the spinal cord itself (hematomyelia) and occurs in 50% of all SCAVM patients. Hemorrhage, particularly hematomyelia, is associated with the onset of new, significant, and often devastating neurological deficits or with aggravating preexisting deficits. Hemorrhage is seen more frequently in cervical lesions than in thoracic and lumbar lesions.39–41 Hemorrhage is also more common in children.43

Hemorrhage may be caused by rupture of associated aneurysms, rerupture of a false aneurysm, rupture of spinal cord veins, or rupture of the AVM nidus. Hemorrhagic transformation of venous infarction is not observed in the cord.

The typical syndrome of spinal hemorrhage is severe pain, which frequently starts in the interscapular region and/or at the site of the rupture and then rapidly spreads to the rest of the back, to the nuchal area, and to the legs. When hemorrhage is profuse or, in cervical lesions, when blood extends into the intracranial cavity, there may be headaches and disturbance of consciousness. In severe cases, papilledema, cranial nerve palsies, and convulsions may be observed. The signs and symptoms can be so severe and rapid in their onset that they may be mistaken for intracranial subarachnoid hemorrhage. In other cases, limb weakness, sensory loss, and disorders of micturition or defecation may follow bleeding within the cord itself (hematomyelia) or may result from compression of the cord by a blood clot. In rare instances, in cases of severe upper cord dysfunction, respiratory paralysis can occur.

Nonhemorrhagic Symptoms

Acute, nonhemorrhagic neurological deficit may result from acute intralesional venous thrombosis. This may occur as a venous response to chronic hemodynamic changes in the SCAVM. More often, patients present with chronic progressive neurological symptoms caused by venous congestion within the spinal cord. Of note is that the venous proportion of the vascular system is of greater hemodynamic significance in the spinal cord than in the cerebral circulation. This can be explained by the contragravity venous drainage of the spinal cord (which is mostly below the level of the heart), in comparison with that of the brain.

Chronic progressive symptoms may manifest in a continuous or stepwise manner. Early symptoms include nerve root or back pain. Weakness eventually develops in over 90% of affected patients. Other common symptoms include sensory changes and impotence. Bowel and bladder dysfunction is present in almost all patients. The presence of a bruit is a relatively uncommon finding. If present, however, a bruit is strongly suggestive of a high-flow lesion.

Muscle atrophy and sensory disturbances that may result in multiple injuries can be observed in patients with SCAVMs. Spinal deformities such as kyphosis and scoliosis are also seen. In addition, complications common to other types of spinal cord dysfunction, such as urinary tract infections, respiratory infections, and decubitus ulcerations, may also be present and must be taken into consideration in determining the morbidity and final outcome of these patients.

Diagnosis and Clinical Assessment

The first step in the assessment of patients with suspected vascular disorders of the spinal cord is a complete clinical history and physical examination. The neurological status needs to be accurately determined and often must be repeated in time to objectively establish stability or worsening of neurological status.

This is followed by a complete pretherapeutic evaluation, including noninvasive imaging techniques and spinal angiography.

Noninvasive Imaging Techniques

MRI has become the modality of choice in the preliminary assessment of patients referred for investigation of vascular pathology of the spinal cord. Computed tomography and myelography no longer have a significant role in the initial screening of suspected SCAVM, except for cases in which MRI is contraindicated.

MRI is both sensitive in lesion detection and able to demonstrate the extent of an AVM, including the demonstration of any extraspinal extension in cases of metameric syndromes. MRI is also useful in delineating intramedullary pathologic processes such as spinal cord hematoma, intravascular thrombosis, and subarachnoid hemorrhage and the secondary changes of cord edema, intramedullary cavities, or cord atrophy secondary to chronic venous hypertension. Changes at a distance from the malformation may be present and may explain otherwise confusing neurological symptoms.

MRI remains limited in its ability to accurately locate the site of arteriovenous communication and the evaluation of the angioarchitecture of an AVM. Pitfalls of this technique in the assessment of patients with vascular lesions of the spinal cord are related primarily to cerebrospinal fluid pulsation artifacts that may produce images highly suggestive of spinal cord vascular lesions.44 This is of particular importance in pediatric patients, in whom such artifacts may lead to unnecessary angiographic exploration.

If, however, the study findings are negative or inconclusive and if the diagnosis is compatible with venous congestion from a small arteriovenous shunt draining into the ventral spinal cord vein, spinal DSA should be performed.45 For treatment planning, spinal DSA still remains the study of choice.

Spinal Angiography

DSA remains a “gold standard” in the diagnosis and treatment planning of vascular lesions of the spine and spinal cord. Spinal DSA is usually performed with the patient under general anesthesia and with controlled respiration.

Spinal DSA is performed according to different protocols at different institutions and may be guided by MRI. However, as in any other vascular study, a territorial approach must be undertaken. As in all other anatomical areas, the angiographic examination must outline the normal vasculature around the vascular pathology to ensure that the full extent of the lesion is visualized and that the effect of the lesion on the remainder of the spinal cord is understood and in order to properly plan and monitor treatment. Specific attention should be paid to the angioarchitecture of the lesion and remaining vascular supply to the cord. Features such as radicular aneurysms, intranidal aneurysms, and venous congestion should be noted.

Treatment and Management

The final outcomes of patients with vascular lesions of the spinal cord are directly related to the prompt diagnosis and treatment of the abnormality.

Endovascular Embolization and Surgery

The main modes of therapy are surgery and endovascular embolization. In current practice, the first line of treatment for SCAVMs is usually endovascular embolization with glue (N-butyl cyanoacrylate). In rare instances in which endovascular embolization is not possible or may carry high risk, surgery may be considered. Radiosurgery currently has no role in the treatment of SCAVMs.

The indications for treatment include all symptomatic lesions that can be cured. Factors that modify the objectives in a particular patient include (1) the age of the patient; (2) the clinical manifestation (e.g., hemorrhage, more than one hemorrhage); (3) the angioarchitecture of the lesion (the presence of, e.g., an aneurysm, venous ectasia); and (4) impaired arterial flow or venous drainage of the spinal cord (stagnation in the anterior spinal artery circulation; nonvisualization of the medullary veins, indicating impaired venous drainage). In the young symptomatic patient, treatment should be pursued aggressively.

As in BAVMs, even when complete cure may not be possible at an acceptable level of risk, partial targeted treatment can be proposed with the aim of arresting or improving the clinical situation or favorably modifying the natural history of disease. The purpose of a partial targeted approach is to obliterate weak points in the angioarchitecture (e.g., arterial aneurysm and nidus aneurysm) and to reduce nidal size and flow to decongest the venous drainage. These procedures relieve the venous drainage of the normal spinal cord, often with beneficial effect.

In the acute stage after a spinal hemorrhage, the neurological deficit may be severe, including total loss of function. Although rebleeding is a risk, most patients improve significantly over the next several weeks or months. Emergency and aggressive intervention is generally unnecessary and may interfere with the process of natural recovery. Spinal angiography may be performed early to rule out a pseudoaneurysm or another potentially risky angioarchitectural feature that may justify early targeted embolization, usually if more than one hemorrhage has occurred.

In patients with a fixed deficit or severe clinical signs of cord transection, treatment is of unlikely functional benefit. Nonetheless, treatment is indicated, especially in cases of repeated hemorrhage and in high cord lesions, to reduce the risk of repeated life-threatening spinal hemorrhage. In some patients with severe pain related to compressive symptoms, palliative embolization may also be beneficial.

Medical Therapy

Medical treatment for the various complications of spinal vascular lesions is an important part of patient management and should be provided. Physical therapy, nursing, pain control management, and psychotherapy all play important roles in the management of patients with SCAVMs. A properly trained team is essential for obtaining the best overall results.

CONCLUSION

Both BAVMs and SCAVMs are relatively uncommon diseases. The exact incidence of these diseases is, however, difficult to estimate. Differences in the disease prevalence reported in the literature are probably related to differing referral patterns and population differences, as well as the diagnostic modalities available.

Patients may present with a wide range of clinical symptoms, which vary according to lesion location, the angioarchitecture of the malformation, and the age of the patient. When either a BAVM or SCAVM is suspected in a patient, a complete clinical and neurological assessment is crucial. This is essential both in the pretreatment evaluation and for subsequent follow-up of the patient’s progress after therapy.

Current imaging modalities in the evaluation of these vascular lesions involve mainly MRI and DSA, the latter being necessary for the accurate delineation of lesion angioarchitecture and hence in treatment planning.

Of the therapeutic modalities discussed, endovascular embolization is becoming an increasingly important tool in the treatment of both BAVMs and SCAVMs. Whereas a complete cure is often obtained in single-hole fistulae or small AVMs, it may not be possible in many complex lesions without risk of increased morbidity. In such cases, a partial targeted approach may be taken instead, to treat high-risk areas within such lesions. The aim of treatment is, above all, to improve the natural history of the disease, in comparison with the risk of therapy, and to achieve amelioration of clinical symptoms when possible.

KEY POINTS

• Arteriovenous malformations (AVMs) in the brain and spinal cord are uncommon. The concept that AVMs are congenital (morphologically detectable at birth) is not supported by antenatal or pediatric imaging and clinical experience. On the contrary, it is likely that lesions found in young adults, although likely to result from an early in utero “event,” are not present at birth but appear later as a result of various (unknown) exogenous or endogenous “revealing” triggers. This empirical observation contributes to the evolution of the malformation concept from a morphological (detectable) to a biological (quiescent) one. Pediatric cases or even neonatal series represent only a small proportion of AVMs and pertain to specific disease groups.
• Magnetic resonance imaging and digital subtraction angiography are currently the modalities of choice in the diagnosis and evaluation of these lesions.
• The aim of treatment is an improvement over the expected natural history of the disease rather than a morphological endpoint. The treatment strategy is specific to each patient and based on the clinical circumstances, the age of the patient, and the angioarchitecture of the lesion.

Suggested Reading

Berenstein A, Lasjaunias P, Ter Brugge KG. Surgical Neurorangiography, vol 2.2: Clinical and Endovascular Treatment Aspects in Adults, 2nd ed., Berlin: Springer-Verlag; 2004:609-735. 760–847.

Hofmeister C, Stapf C, Hartmann A, et al. Epidemiological, clinical and morphological characteristics of 1289 patients with cerebral arteriovenous malformation. Stroke. 2000;31:1307-1310.

Lasjaunias P. Vascular Diseases in Neonates, Infants and Children: Interventional Neuroradiology Management. Berlin: Springer-Verlag, 1997;203-319.

Mansmann U, Meisel J, Brock M, et al. Factors associated with intracranial hemorrhage in cases of cerebral arteriovenous malformation. Neurosurgery. 2000;46:272-281.

Meisel HJ, Mansmann U, Alvarez H, et al. Cerebral arteriovenous malformation and associated aneurysms: analysis of 305 cases from a series of 662 patients. Neurosurgery. 2000;46:793-802.

Rodesch G, Hurth M, Alvarez H, et al. Angioarchitecture of spinal cord arteriovenous shunts at presentation. Clinical correlations in adults and children: the Bicêtre experience on 155 consecutive patients seen between 1981–1999. Acta Neurochir. 2004;146:217-227.

Stefani MA, Porter PJ, Ter Brugge KG, et al. Angioarchitectural factors present in brain arteriovenous malformations associated with hemorrhagic presentation. Stroke. 2002;33:920-924.

Valavanis A, Yasargil MG. The endovascular treatment of brain arteriovenous malformations. Adv Tech Stand Neurosurg. 1998;24:131-214.

References

1 Weon YC, Yoshida Y, Sachet M, et al. Supratentorial cerebral arteriovenous fistulas (AVFs) in children: review of 41 cases with 63 non choroidal single-hole AVFs. Acta Neurochir. 2005;147:17-31.

2 Garretson HD. Intraranial arteriovenous malformations. In: Wilkins RH, Rengachary SS, editors. Neurosurgery. New York: McGraw-Hill; 1985:1448-1457.

3 Jellinger K. Vascular malformations of the central nervous system: a morphological overview. Neurosurg Rev. 1986;9:177-216.

4 Mohr JP. Neurological manifestations and factors related to therapeutic decisions. In: Wilson CB, Stein BM, editors. Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins; 1984:12-23.

5 Valavanis A, Yasargil MG. The endovascular treatment of brain arteriovenous malformations. Adv Tech Stand Neurosurg. 1998;24:131-214.

6 Guttmacher AE, Marchuk DA, White RIJ. Hereditary hemorrhagic telangiectasia. N Engl J Med. 1995;333:918-924.

7 McAllister KA, Grogg KM, Johnson DW. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary hemorrhagic telangiectasia type 1. Nat Genet. 1994;8:345-351.

8 Mahadevan J, Ozanne A, Yoshida Y, et al. Hereditary haemorrhagic telangiectasia cerebrospinal localization in adults and children: review of 39 cases. Interv Neuroradiol. 2004;10:27-35.

9 Willinsky RA, Lasjaunias P, Ter Brugge KG, et al. Multiple cerebral arteriovenous malformations: review of our experience from 203 patients with cerebral vascular lesions. Neuroradiology. 1990;32:207-210.

10 Fullbright RK, Chaloupka JC, Putman CM, et al. MR of hereditary hemorrhagic telangiectasia: prevalence and spectrum of cerebrovascular malformations. AJNR Am J Neuroradiol. 1998;19:477-484.

11 Matsubara S, Mandzia JL, Ter Brugge KG, et al. Angiographic and clinical characteristics of patients with cerebral arteriovenous malformations associated with hereditary hemorrhagic telangiectasia. AJNR Am J Neuroradiol. 2000;21:1016-1020.

12 Krings T, Ozanne A, Chng SM, et al. Neurovascular phenotypes in hereditary haemorrhagic telangiectasia patients according to age: review of 50 consecutive patients aged 1 day–60 years. Neuroradiology. 2005;47:711-720.

13 Garcia-Monaco R, Taylor W, Rodesch G, et al. Pial arteriovenous fistula in children as presenting manifestation of Rendu-Osler-Weber disease. Neuroradiology. 1995;37:60-64.

14 Yoshida Y, Weon YC, Sachet M, et al. Posterior cranial fossa single-hole arteriovenous fistulae in children: 14 consecutive cases. Neuroradiology. 2004;46:474-481.

15 Bhattacharya J, Luo CB, Suh DC, et al. Wyburn-Mason or Bonnet-Dechaume-Blanc as cerebrofacial arteriovenous metameric syndromes (CAMS): a new concept and a new classification. Interv Neuroradiol. 2001;7:5-17.

16 Meisel HJ, Mansmann U, Alvarez H, et al. Cerebral arteriovenous malformation and associated aneurysms: analysis of 305 cases from a series of 662 patients. Neurosurgery. 2000;46:793-802.

17 Stefani MA, Porter PJ, Ter Brugge KG, et al. Angioarchitectural factors present in brain arteriovenous malformations associated with hemorrhagic presentation. Stroke. 2002;33:920-924.

18 Crawford PM, West CR, Chadwick DW, et al. Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry. 1986;49:1-10.

19 Mansmann U, Meisel J, Brock M, et al. Factors associated with intracranial hemorrhage in cases of cerebral arteriovenous malformation. Neurosurgery. 2000;46:272-281.

20 Hofmeister C, Stapf C, Hartmann A, et al. Epidemiological, clinical and morphological characteristics of 1289 patients with cerebral arteriovenous malformation. Stroke. 2000;31:1307-1310.

21 Ducreux D, Desal H, Bittoun J, et al. Diffusion, perfusion and activation functional MRI studies of brain arteriovenous malformations. J Neuroradiol. 2004;31:25-34.

22 Berenstein A, Lasjaunias P, Ter Brugge KG. Goals and objectives in the management of brain arteriovenous malformations. In Surgical Neurorangiography, vol 2.2: Clinical and Endovascular Treatment Aspects in Adults, 2nd ed., Berlin: Springer-Verlag; 2004:703.

23 Stefani MA, Porter PJ, Ter Brugge KG, et al. Large and deep brain arteriovenous malformations are associated with risk of future hemorrhage. Stroke. 2002;33:1220-1224.

24 Meisel HJ, Mansmann U, Alvarez H, et al. Effect of partial targeted NBCA embolization in brain AVM. Acta Neurochir. 2002;144:879-888.

25 Lasjaunias P. Vascular Diseases in Neonates, Infants and Children: Interventional Neuroradiology Management. Berlin: Springer-Verlag, 1997;41.

26 Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476-483.

27 Karlsson B, Lindquist C, Steiner L. Prediction of obliteration after gamma knife surgery for cerebral arteriovenous malformations. Neurosurgery. 1997;40:425-431.

28 Pollock B, Flickinger J, Lunsford D, et al. Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery. 1998;42:1239-1247.

29 Schlienger M, Atlan D, Lefkopoulos D, et al. Linac radiosurgery for cerebral arteriovenous malformations: results in 169 patients. Int J Radiation Oncol Biol Phys. 2000;46:1135-1142.

30 Wyburn-Mason R. The Vascular Abnormalities and Tumours of the Spinal Cord and Its Membranes. London: H. Kimpton, 1943.

31 Pia HW, Vogelsang H. Diagnose und Therapie spinaler Angiome [Diagnosis and therapy of spinal angioma]. Dtsch Z Nervenheilkd. 1965;187:74-96.

32 Olivecrona H. The cerebellar angioreticulomas. J Neurosurg. 1957;9:317-330.

33 Krenchel NJ. Intracranial Racemose Angiomas: a Clinical Study. Copenhagen: Universitetsforlaget i Aarhus, 1961.

34 Rodesch G, Hurth M, Alvarez H, et al. Classification of spinal cord arteriovenous shunts: proposal for a reappraisal—the Bicêtre experience with 155 consecutive patients treated between 1981 and 1999. Neurosurgery. 2002;51:374-380.

35 Mandzia JL, Ter Brugge K, Faughnan ME, et al. Spinal cord arteriovenous malformations in two patients with hereditary hemorrhagic telangiectasia. Childs Nerv Syst. 1999;15:80-83.

36 Mazighi M, Porter P, Alvarez H, et al. Associated cerebral and spinal AVM in infant and adult: report of two cases treated by endovascular approach. Intervent Neuroradiol. 2000;6:321-326.

37 Matsumaru Y, Pongpech S, Laothamas J, et al. Multifocal and metameric spinal cord arteriovenous malformations: review of 19 cases. Interv Neuroradiol. 1999;5:27-34.

38 Nimii Y, Ito U, Tone O, et al. Multiple spinal perimedullary arteriovenous fistulae associated with the Parkes-Weber syndrome. Interv Neuroradiol. 1998;4:151-157.

39 Djindjian M, Djindjian R, Hurth M, et al. Spinal cord arteriovenous malformations and the Klippel-Trénaunay-Weber syndrome. Surg Neurol. 1977;8:229-237.

40 Rosenblum B, Oldfield EH, Doppman JL, et al. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulae and intradural AVM’s in 81 patients. J Neurosurg. 1987;67:795-802.

41 Berenstein A, Lasjaunias P. Surgical Neuroangiography. vol 4. Berlin: Springer-Verlag; 1992:197-251.

42 Yasargil MG, Symon L, Teddy PG. Arteriovenous malformations of the spinal cord. Symon L, editor. Advances and Technical Standards in Neurosurgery. vol 11. Vienna: Springer-Verlag; 1984:61-102.

43 Rodesch G, Hurth M, Alvarez H, et al. Angioarchitecture of spinal cord arteriovenous shunts at presentation: clinical correlations in adults and children. The Bicêtre experience on 155 consecutive patients seen between 1981–1999. Acta Neurochir. 2004;146:217-227.

44 Levy LM, di Chiro G, Brooks RA, et al. Spinal cord artifacts from truncation errors during MR imaging. Radiology. 1988;166:479-483.

45 Lasjaunias P, Berenstein A, Terbrugge KG. Spine and spinal cord arteries and veins. In Surgical Neuroangiography, vol 1: Clinical Vascular Anatomy and Variations, 2nd ed., Berlin: Springer-Verlag; 2001:73-164.

Related posts:

GAIT DISTURBANCES AND FALLS SLEEP APNEA PARASITIC AND FUNGAL INFECTIONS NEUROLOGY OF PREGNANCY AND THE PUERPERIUM GENETIC CAUSES OF BLINDNESS OPTIC NEUROPATHIES