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May 10, 2013 - J Neurosurg / Volume 119 / September 2013. ©AANS, 2013. Yaşargil defined .... No deaths occurred among our series of patients. Discussion.
See the corresponding editorial in this issue, pp 591–593.

J Neurosurg 119:594–602, 2013 ©AANS, 2013

Cerebral microarteriovenous malformations: a series of 28 cases Clinical article José F. Alén, M.D., Ph.D.,1 Alfonso Lagares, M.D., Ph.D.,1 Igor Paredes, M.D.,1 Jorge Campollo, M.D., 2 Pedro Navia, M.D., 2 Ana Ramos, M.D., Ph.D., 2 and Ramiro D. Lobato, M.D., Ph.D.1 Department of Neurosurgery and 2Division of Neuroradiology, Hospital 12 de Octubre, Universidad Complutense de Madrid, Spain 1

Object. Microarteriovenous malformations (micro-AVMs) are a rare subgroup of brain AVMs characterized by a nidus smaller than 1 cm. The authors’ purpose in this study was to assess the clinical presentation, radiological features, therapeutic management, and outcome of these lesions. Methods. All angiography studies performed at the authors’ institution since 2000 for the diagnosis of AVM were retrospectively reviewed. Clinicoradiological findings, therapeutic management, and outcome were evaluated. Results. Twenty-eight patients had presented with AVMs having a nidus diameter smaller than 1 cm or no clearly identifiable nidus but an early draining vein. All patients, except 2, presented with intracranial hemorrhage, and 12 patients had a focal deficit. Supratentorial hematomas were large (mean volume 25 ml), and in 8 patients hematomas were evacuated urgently. In 6 patients cerebral digital subtraction angiography studies were normal. Magnetic resonance imaging and dynamic MR angiography revealed an AVM in 4 of these 6 patients. Treatment of the AVM consisted of surgery in 16 cases, radiosurgery in 6, and endovascular embolization in 2, and there were no posttreatment deficits. Four patients received no treatment because of their poor condition. The AVM was occluded at the follow-up in all patients treated with surgery or embolization and in 4 of the 6 patients treated with radiosurgery. The Glasgow Outcome Scale (GOS) score was good (GOS 4–5) in 23 patients (82%) and poor (GOS 3–2) in 5 (18%). Conclusions. Patients with micro-AVMs generally present with large intracranial hemorrhages and neurological deficits. If the initial angiography is negative, then delayed or superselective angiography is recommended. Magnetic resonance imaging may reveal the existence of these lesions. Surgery is the treatment of choice for superficial microAVMs, and radiosurgery or embolization can be considered for deep lesions. (http://thejns.org/doi/abs/10.3171/2013.4.JNS121740)

Key Words      •      arteriovenous malformation      •      vascular disorders      • unexplained intraparenchymal hemorrhage      •      microarteriovenous malformation

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defined cerebral microarteriovenous malformations as a subgroup of pial AVMs characterized by a nidus of 1 cm or smaller.22 He differentiated this subgroup from occult AVMs (not seen on angiography, not seen by the surgeon, and not demonstrated pathologically but assumed to be present) and cryptic AVMs (invisible on angiography and at surgery but recognized on histological examination if the hematoma is carefully removed and not aspirated away).22 Micro-AVMs are visible on angiography, sometimes just as an abnormal arteriole without draining veins or as an abnormal draining vein with the feeding vessels remaining undetectable. Other times a tiny lesion with the clasaşargil

Abbreviations used in this paper: AVM = arteriovenous malformation; DSA = digital subtraction angiography; GOS = Glasgow Outcome Scale; MIP = maximum intensity projection; MRA = MR angiography; TOF = time-of-flight.

594

sic appearance of pathological arterioles and pathological draining veins is visible on angiography. Micro-AVMs account for < 8% of surgically treated AVMs, and most reports of micro-AVMs as defined by Yaşargil are either isolated cases or cases included in series of angiographically occult vascular malformations. In the literature we have found only 4 small series of patients suffering from this pathological entity. Our aim in the present study was to assess the clinical presentation, radiological features, therapeutic management, and outcomes in a consecutive series of patients with microAVMs.

Methods

We retrospectively reviewed all DSA studies (260 cases) performed at our institution between 2000 and 2010 for the diagnosis of AVM. Cases were included in J Neurosurg / Volume 119 / September 2013

A series of cerebral microarteriovenous malformations the present study if angiographic assessment demonstrated an AVM with a nidus diameter smaller than 1 cm (micronidus) or without a clearly identifiable nidus but an early draining vein. Patients in whom surgical exploration revealed a nidus larger than 1 cm, as might occur with partially thrombosed AVMs or AVMs compressed by mass effect due to associated hemorrhage, were excluded. One patient harboring a large, partially treated AVM with a residual nidus diameter smaller than 1 cm was also excluded. The charts, neuroradiographic features, and outcomes of patients with cerebral micro-AVMs were retrospectively reviewed. All patients underwent at least 1 cerebral DSA before definitive treatment of the micro-AVM. Digital subtraction angiograms were analyzed for the presence and morphological features of the AVM nidus, the phase of the angiogram during which the micro-AVM was opacified, the nature and size of the feeding vessels, and the presence of associated arterial aneurysms. Venous drainage characteristics, including ectasia, stenosis, and caliber of venous outflow were noted. Magnetic resonance imaging on a 1.5-T scanner included sagittal T1-weighted sequences with an inversion recovery technique and axial and coronal high-resolution fast spin echo T2-weighted sequences using a 2.5-mm thickness with 0.2-mm skip, 512 × 320 matrix, and 24 × 24 FOV. Magnetic resonance angiography included contrast-enhanced sequences followed by 3D TOF sequences. Contrast-enhanced MRA was performed using k-space sampling with elliptical center order and fluoroscopic triggering to obtain the sequence in an arterial phase (matrix 320 × 256, thickness 1.2 mm). Contrast 3D TOF images were obtained with a higher spatial resolution than the contrast-enhanced MRA (matrix 512 × 320, thickness 0.7 mm). A T1-weighted postcontrast sequence was also obtained to exclude other causes of hemorrhage. Data from the MRA sequences were transferred to a commercially available workstation with 3D capability (Advantage Windows 4.3, GE Medical Systems, Inc.). Source and MIP images were obtained for each sequence to delineate the abnormal vessels. Hemorrhage volumes were calculated on CT scans using the formula a × b × c/2, where a, b, and c represent the maximal diameters of the hematoma in the 3 orthogonal planes. The established management protocol for microAVMs in our series was as follows. In general, when we encounter a young patient with a lobar hematoma who needs urgent surgery because of neurological deterioration, we try to evacuate the hematoma, but we do not usually look for an AVM within the hematoma without a previous angiogram. After surgery, we perform an angiography study as soon as possible and plan a second surgery to resect the AVM. When the patient does not need an urgent operation, we usually obtain an angiogram in the first 24–48 hours after presentation. Once the diagnosis of a micro-AVM has been established and depending on the localization of the nidus, we treat the patient with open microsurgery (superficial nidus) or with embolization or radiosurgery (deep lesion). We routinely use MRI neuronavigation in surgeries for micro-AVMs to plan the craniotomy and to localize the nidus. J Neurosurg / Volume 119 / September 2013

Follow-up evaluations of the patients consisted of clinical examinations performed by a neurosurgeon during the outpatient visits and telephone interviews at the last follow-up. Final outcome was classified according to the GOS.9 The mean follow-up period was 61 months (range 5–120 months).

Results

Twenty-eight patients having a micro-AVM constitute the present series. Initial DSA findings were diagnostic of a micro-AVM in 22 patients and negative in 6 patients. A second DSA study was scheduled after hematoma resorption in 2 patients with initial negative angiographic findings. In the other 4 patients, the MRI and MRA studies after resorption of the hematoma prompted another DSA with microcatheterization of the affected vessels to display the vascular malformation. The second DSA, performed after a median time of 4 months (range 1–24 months), demonstrated the micro-AVM in these 6 patients. Twenty-two micro-AVMs were supratentorial and 6 were infratentorial (Table 1). The identification of a small feeding vessel with a poorly defined, tiny nidus and an early draining vein was the most common finding on cerebral angiography (19 cases). In 9 cases only an early draining vein was discovered, without opacification of a nidus. A single draining vein was present in all cases but 1 (Case 18) in which 2 draining veins were seen. We did not find any flow-related aneurysms in this series of patients. Twenty-one patients underwent prospective MRI and MRA. The other 7 patients were treated either at the beginning of the series or on an emergency basis, and no MRI was performed in those cases. Magnetic resonance imaging and dynamic MRA with contrast were performed in 21 patients before treatment of the microAVM. These imaging studies revealed the AVM in 4 of the 6 patients in whom an initial DSA study was negative. In the MRA studies, special attention was paid to the presence of abnormal vascular architecture suggestive of a micro-AVM nidus or draining veins. Abnormal vascular structures were defined as abnormal, hyperintense, fine tangled or tubular structures with continuity as seen on consecutive slices or as a prominent draining vein without an apparently recognizable nidus. Irregular or nodular hyperintense lesions without a branching pattern were regarded as parenchymal enhancement caused by surgery or hemorrhage. The median age at presentation was 35.5 years (range 3–77 years; Table 2). All patients, except 2 in whom the AVM was found incidentally (Cases 6 and 16), presented with intracranial hemorrhage (Table 3). In 18 patients the hemorrhage was supratentorial, in 5 it was infratentorial, and in 3 it was purely intraventricular. In 12 patients, a focal neurological deficit was present at the initial diagnosis. In 8 patients the level of consciousness was altered, ranging from only somnolence to deep coma. Supratentorial hematomas were large (mean volume 25 ml, range 10–60 ml), and they had to be urgently evacuated in 8 patients. In 3 patients, external ventricular drainage was needed because of hydrocephalus. None of the patients 595

J. F. Alén et al. TABLE 1: Summary of localization of 28 micro-AVMs Location

Supratentorial

Infratentorial

Total

cortical subcortical deep total

 6 10  6 22

2 1 3 6

 8 11  9 28

had a family history or findings indicative of Osler-Rendu-Weber disease. Definitive treatment for the AVM was surgery in 16 cases (Fig. 1), radiosurgery in 6 (Fig. 2), and endovascular embolization in 2 (Fig. 3). Magnetic resonance images were used for neuronavigation in cases in which surgery was performed. None of the patients demonstrated new neurological deficits after treatment. Four patients received no treatment either because they refused it or because of their poor clinical condition. No rebleeding was observed in our series. All patients who underwent surgery had an occluded AVM according to postoperative DSA. Of the 6 patients treated with radiosurgery, 4 had an occluded AVM, and 2 are still in the first 3 years of

follow-up with no final angiogram obtained as yet. Embolization with N-butyl cyanoacrylate cured 2 patients. The treatment did not add morbidity in any of our patients. The GOS score was excellent (GOS Score 5) for 18 patients (64%). Five patients (18%) recovered with moderate disability (GOS Score 4), and outcome was poor (GOS 3) in 5 patients (18%). No deaths occurred among our series of patients.

Discussion

In 1961 Margolis et al.12 proved through autopsy sectioning of 4 fatal intracranial hematomas that microAVMs could act as sources of hemorrhage. In the early literature, multiple reports documented tiny vascular lesions pathologically compatible with AVMs in the walls of hemorrhage cavities.4,10,12,17 Superselective angiography has increased our ability to reach a diagnosis of microAVM when regular DSA is questionable or negative, allowing for more precise localization of the lesion and characterization of the angioarchitecture.6 The true incidence of micro-AVM is difficult to ascertain. Willinsky et al.20,21 found an approximately 10% incidence in their series of brain AVMs, and Stiver and

TABLE 2: Summary of clinical data among 28 patients with micro-AVMs Parameter

Description

age at presentation in yrs (range) 37 (3–77) consultation 12 cases: focal neurological deficit; other cases: dizziness, dysphasia, seizures, cervicalgia,   loss of consciousness clinical presentation 26 cases: intracranial hemorrhage (18 supratentorial, 5 infratentorial, 3 pure intraventricular   hemorrhage); 2 cases: micro-AVM an incidental finding average size of hematoma in ml 25 (10–60)  (range) patients needing urgent surgery  8 findings at DSA most frequent finding: arterialized drainage vein w/ practically imperceptible nidus communi  cating w/ very small feeder vessels; 6 cases: initial DSA normal venous drainage 19 cases superficial drainage, 9 cases deep drainage MRI & dynamic MRA* detected micro-AVM in 15 patients; demonstrated micro-AVM in 4 of 6 patients w/ negative   initial DSA treatment  surgery 16 patients  radiosurgery   6 patients   embolization   2 patients  none   4 patients treatment results†  surgery all patients cured  radiosurgery 4 patients w/ occlusions, 2 patients w/o final angiograms (follow-up