Original Articles

Functional magnetic resonance imaging in The pre-operative evaluation of cerebral vascular malformations Resonancia magnética cerebral funcional en la evaluación prequirúrgica de malformaciones vasculares

Natalia Montes1 Diego Alberto Herrera2 Sergio Alberto Vargas2

Key words (MeSH) SUMMARY Vascular malformations Objective: To describe our experience with pre-operative evaluation of intracranial Magnetic resonance imaging vascular malformations using functional magnetic resonance (fMRI). Method: Assessment Cerebral arteries of eight patients with cerebral vascular malformations (seven arteriovenous malformations [AVM] and one cavernous malformation) referred for pre-operative fMRI mapping of the Palabras clave (DeCS) eloquent cortex. An oxygen level-dependent technique (BOLD) was used to localize these Malformaciones areas in relation to the cerebral vascular malformation, applying different paradigms. vasculares Results: We found one AVM in the right mid- with distribution of the visual Imagen por resonancia and spatial memory to the contralateral hippocampus and parahippocampus; one posterior magnética left temporal AVM with activation of Wernicke’s area only; one left parietal AVM without Arterias cerebrales compromise of the sensory or ; a cavernous malformation at the left angular gyrus with hemispheric language dominance on that side; one right thalamic AVM with no compromise of the eloquent cortex; one left periventricular AVM with bilateral language dominance; one small left occipital AVM with normal activation of the primary visual cortex and decreased activation of the visual association cortex; and one temporo-occipital AVM with left language dominance and neurovascular uncoupling. Conclusion: fMRI can be used to delineate the anatomical relationship between the lesion and the eloquent cortex, providing useful information for pre-operative planning, and the estimated risk of the intervention.

Resumen 1 Radiologist. Neuro-radiology Fellow. Universidad de Antioquia. Medellín, Objetivo: Describir la experiencia en la evaluación prequirúrgica de pacientes con Colombia. 2 Neuro-radiologist, Centro Avanzado malformaciones vasculares con resonancia magnética cerebral funcional (RMf). Método: de Diagnóstico Médico (Cedimed) and Se evaluaron ocho pacientes con malformaciones vasculares cerebrales (siete malfor- Universidad de Antioquia. Medellín, Colombia. maciones arteriovenosas [MAV] y una malformación cavernosa) remitidos para mapeo

Rev Colomb Radiol. 2010; 21:(4):1-11 1 prequirúrgico de la corteza elocuente con RMf. Se usó una técnica depen- diente de la concentración de oxígeno (BOLD) para localizar estas zonas en relación con la malformación vascular cerebral, aplicando diferentes paradigmas. Resultados: Se encontró una MAV en el lóbulo mesotemporal derecho, con representación de la memoria visuoespacial en el hipocampo y parahipocampo contralesionales; una MAV temporal posterior izquierda con activación contralateral exclusiva del área de Wernicke; una MAV parietal izquierda sin afectación de la corteza sensoriomotora; una malformación ca- vernosa en la circunvolución angular izquierda con dominancia hemisférica del lenguaje en ese lado; una MAV talámica derecha sin daño en la corteza elocuente; una MAV periventricular izquierda con patrón de equidominancia del lenguaje; una MAV pequeña occipital izquierda con activación normal en la corteza visual primaria y disminución en la activación de la corteza de asociación visual del lado izquierdo donde se encuentra la lesión, y una MAV temporo-occipital con dominancia hemisférica izquierda y desacople neu- rovascular. Conclusión: La RMf puede delinear anatómicamente la relación entre la lesión y la corteza elocuente y brindar información que facilita la planeación quirúrgica, incluida la estimación del riesgo de la intervención.

Introduction A case series is presented in order to illustrate the usefulness Localization of the eloquent cortex is difficult even with the of this method. use of multiplanar magnetic resonance imaging (MRI). There Patients and methods may be distortion and displacement of this area with congenital We reviewed the clinical records of patients with a diagnosis lesions such as cerebral vascular malformations (1). Functional of cerebral vascular malformation referred for fMRI between magnetic resonance mapping (fMRI) using a blood level oxygen- March 2007 and December 2008 in order to assess the rela- dependent technique (BOLD) has gained popularity as part of the tionship between the lesion and cortical functional areas. Nine therapeutic planning process in patients who are candidates for patients (five women and four men) ranging from 17 to 50 years surgical, endovascular o radiosurgical treatment. This technique of age were included in the study (Table 1), and the retrospective is based on the local increase in oxyhemoglobin (molecule with paramagnetic properties) concentration in the cerebral vascu- review was approved by the Ethics Committee of the institution. lature, resulting from increased blood flow and volume in the The assessment included the localization, type and morphology cortex under stimulation (1,2). of the vascular malformation and its relationship (10) with the Mapping of cerebral function in the adjacent areas may be adjacent anatomical and functional structures. performed using intra- or pre-operative methods, including fMRI A 1.5 T Avanto (Siemens, Erlangen, Germany) magnetic as an alternative to positron emission tomography (3), magnetic resonance machine was used to acquire a T1 magnetization- encephalography (4,5), electrocorticography and the Wada test prepared rapid gradient echo (MP-RAGE) sequence in the (1,6,7), for example. Although these procedures, in particular sagittal plane in 20 healthy volunteers as follows: FOV = 240, fMRI, are very accurate for localizing the different cerebral matrix = 192x192, resolution = 1.3x1.3x1.3 mm, RT = 1,670 functions, they do not provide information about the time course ms, ET = 3.6 ms, flip angle = 8°, IT = 1,000 ms, averages = 2, of the activations and, consequently, about the organization of concatenations = 1, slices = 128, slice overmeasurement = 25%, the neural networks supporting each function (4,5). distance factor = 50%, bandwidth = 180 Hz/Px, duration, 4’39”. fMRI makes the therapeutic planning easier as it allows An echoplanar T2* gradient echo (RT = 3,000 ms, ET = 50 to define the relationship between the vascular lesion and the ms; matrix = 64x64; voxel size = 3x3x3 mm) sequence with functional cortex before proceeding to the surgical resection or continuous acquisition was used for the functional imaging endovascular exclusion, thus preventing a clinical deficit (8). (Table 2). Functional images were acquired following a block Language mapping is essential in these lesions because cerebral pattern, including alternating series every 30 s between basal and vascular malformations may be congenital and may give rise to active states. The paradigms (Table 3) consisted of alternating the reorganization of functional areas (6,9). closing and opening of the hand in order to activate the sensory- The purpose of this study is to describe our initial experience motor cortex, generation of verbs to assess language function, with the localization of the eloquent cortex using fMRI, in order modified Roland test to assess visual and spatial memory (11), to establish its relationship with cerebral vascular malforma- opening and closing of the eyes for visual activation, plus a tions and determine its importance in pre-operative planning. breath-holding paradigm.

2 Functional magnetic resonance imaging in The pre-operative evaluation of cerebral vascular malformations, Montes N; Herrera DA, Vargas SA Original Articles Table 1. Patients with cerebral vascular malformations assessed with fMRI before surgery (Medellin, Colombia, 2007-2008) Clinical Treatment No. Gender Laterality Malformation Paradigm fMRI interpretation Manifestation outcome Only left 18 year-old Right mid- hippocampal and Uncomplicated 1 Right Seizures Memory male temporal AVM parahippocampal embolization activation Mixed dominance Resection, mild Language 50 year-old Prior bleeding, Left temporal (left Broca’s post-surgical 2 Right (verb female headache AVM area and right dysphasia with generation) Wernicke’s area) full recovery Non-displaced activation in 39 year-old Motor (right left pre- and Uncomplicated 3 Right Headache Left parietal AVM male hand) post-central gyri embolization (sensorymotor cortex) Left temporal Language Left language 36 year-old 4 Right Seizures cavernous (verb dominance, lesion No intervention female malformation generation) in Wernicke’s area Non-displaced 17 year-old Bleeding, left Right thalamic Motor (left Uncomplicated 5 Right activation in right female hemiparesis AVM hand) embolization paracentral gyrus Bilateral language Corona radiata dominance, Bleeding, right Language 19 year-old and left semi- non-displaced Uncomplicated 6 Right hemiparesis, and right female oval white activation in embolization dysphasia hand motor matter AVM sensorymotor cortex Visual Partial seizures Reduced activation 38 year-old Left occipital (opening and Waiting for 7 Right with visual in left visual male AVM closing of embolization component association area eyes) Language (sentence Left hemisphere Intra- completion) 50% Left language 12 year-old parenchymal and breath- embolization 8 Right temporoccipital dominance and female hematoma. No holding and waiting for AVM neurovascular motor deficit (apnea and radiosurgery uncoupling breathing cycle)

Rev Colomb Radiol. 2010; 21:(4):1-11 3 Table 2. Acquisition technique Parameter Anatomical Sequence Functional Sequence 1.5 T Siemens Avanto magnetic resonance 1.5 T Siemens Avanto magnetic resonance Machine machine machine Sequences T1 MP-RAGE T* Echoplanar FOV 240 192 Matrix 192x192 64x64 Resolution 1.3x1.3x1.3mm 3x3x3 mm Repetition Time (RT) 1,670 ms 3,000 ms Echo Time (ET) 3.6 ms 50 ms Flip Angle (degrees) 8 90 IT 1,000 ms ... Averages 2 1 Concatenations 1 1 Slices 128 32 Distance factor 50% 30% Bandwidth 180 Hz/Px 1,736 Hz/Px Duration 4 minutes 39 seconds 5 minutes

Table 3. Paradigms: block pattern Paradigms Basal state Active state Motor 10 scan off 10 scan on Number of cycles 3 3 Duration 3 minutes Dummy First cycle was discarded to eliminate T1 effect Task Staying still Alternating finger movement Verb generation 10 scan off 10 scan on Number of cycles 5 Duration 5 minutes Dummy First cycle discarded to eliminate T1 effect Nouns every 3 s as auditory input and the Task Alternating high-low frequency auditory input patient is asked to think of a related verb (10 nouns per cycle) Memory 10 scan off 10 scan on Number of cycles 5 Duration 5 minutes Dummy First cycle was discarded to eliminate T1 effect Breath-hold 15 scan off 15 scan on Number of cycles 4 Duration 4 minutes Dummy First cycle was discarded to eliminate T1 effect Task Normal breathing Apnea Visual 10 scan off 10 scan on Number of cycles 4 Duration 4 minutes Dummy First cycle was discarded to eliminate T1 effect Task Eyes closed Eyes open

4 Functional magnetic resonance imaging in The pre-operative evaluation of cerebral vascular malformations, Montes N; Herrera DA, Vargas SA Original Articles The task used for memory assessment was explained in detail was used for pre-operative assessment. Activation was found before performing the scan. The patient provides information mainly in the left inferior frontal gyrus (Broca’s area), and ex- about five normal routes and during acquisition the patient is clusively in Wernicke’s area, in the right temporal lobe, when a asked to think about the route and imagine every detail. In the verb-generation paradigm was used (Figure 2). This constitutes basal state, the task consisted of counting odd numbers mentally a mixed language dominance pattern. The patient was taken to (11). An offline process was also performed where the images surgery, but presented mild dysphasia during the immediate post- acquired for the various paradigms and anatomical series were operative period, from which she recovered fully afterwards. transmitted in a DICOM format. Images were spatially normal- ized using the algorithm described by Friston et al. (12). Patient 3: left parietal arteriovenous malformation Threshold correlations for each pixel were determined with This was a 39 year-old male patient complaining of head- a 0.001 probability (13). Co-recording of anatomical and func- aches, with a diagnosis of left parietal AVM. Functional magnetic tional images, normalization of the data set according to the resonance was performed in order to assess the motor area, using Montreal Neurological Institute template (ICBM 152 template), a paradigm consisting of alternating right-hand opening and clos- anatomical image segmentation and smoothing of functional im- ing. The test revealed activation in the left pre-central gyrus near ages with a 6x6x6 gaussian Kernel were performed afterward. the sigmoid portion. The AVM did not affect the sensorymotor The first acquisition cycle for each paradigm was discarded in cortex (Figure 3), but embolization was performed, nonetheless, order to eliminate T1-dependent effects in a T2 EPI series. in order to achieve 90% occlusion of the malformation, with no After preparing the EPI images (spatial smoothing and move- residual neurological deficit. ment correction), the linear GLM model with the block pattern, Patient 4: left temporal cavernous malformation the t test generation and the Z parameter maps were applied, Thirty-six year-old female patient with convulsive syndrome followed by alignment with the anatomical images and the entire since she was 20. Over the past three years, seizures became MNI Atlas. Orientation of local or regional signal variations and refractory to medical treatment and she was referred for brain noise filtering were done with spatial smoothing of the imag- MRI. The findings revealed a cavernous malformation affecting ing data during the realignment steps, in order to prepare the the anterior and subcortical portions of the left angular gyrus. A functional images for the statistical process (12). verb-generation paradigm was used, showing left hemisphere Finally, the researchers selected certain regions of interest language dominance as a result of activation in Broca’s area, (ROI) using the WFU.PickAtlas software graphic interface, mainly in the left side. When the language reception area (Wer- executed under SPM5 and Matlab 7.0. This software offers a nicke’s) was assessed, there was activation of the transverse, means to generate ROI masks based on the Talairach Daemon superior temporal and supramarginal gyri, surrounding the database, according to the methodology described and validated cavernous malformation (Figure 4). by Lancaster et al. (14). The atlas include Brodmann’s area, lobes, hemispheres and various anatomical labels. The functional Patient 5: right thalamic arteriovenous images were fused with the anatomical images for interpretation malformation by two neuro-radiologists (DAH and SAV). This is the case of a young 17 year-old female with a history Results of cerebral hemorrhage due to right thalamic AVM, who was left with a moderate left hemiparesis. A functional MRI was Patient 1: right temporal arteriovenous performed in order to assess the motor area (Figure 5). The malformation AVM was causing a motor deficit as a result of the compression Eighteen year-old male patient complaining of a first-time caused by the residual hematoma on the corticospinal tract in the seizure and headache. He was taken to contrast computed posterior branch of the left internal capsule. A motor paradigm tomagraphy imaging of the skull that showed a hypervascular was used for the fMRI with alternating left-hand opening and lesion in the medial portion of the right temporal lobe. Cath- closing, giving rise to activation of the right pre-central gyrus. eter arteriography revealed a 6 cm arteriovenous malformation Embolization was performed, achieving a 70% occlusion of the (AVM) in the right temporal lobe, supplied mainly by branches malformation, with no residual neurological deficit. of the posterior communicating artery, with deep and superficial Patient 6: left periventricular arteriovenous venous drainage (Figure 1). Functional magnetic resonance was performed using a memory paradigm, with a finding of malformation exclusive contralateral activation in the left parahippocampal Nineteen year-old female with a history of bleeding from an and hippocampal areas. Three embolizations with Onyx were AVM in the corona radiata and left semioval white matter, with performed, achieving 70% occlusion of the lesion. The patient residual moderate left hemiparesis and conductive dysphasia. did not show deficits following the procedures. The AVM was causing a motor deficit as a result of a lesion of the corticospinal tract, while the language deficit was due to Patient 2: left temporal arteriovenous malformation damage of the arcuate fasciculus. A motor paradigm with alter- Fifty year-old female with a history of bleeding due to a left nating right-hand opening and closing was used in the fMRI. temporal AVM and four years with headaches. Functional MRI There was activation of both sensorymotor cortices, predomi-

Rev Colomb Radiol. 2010; 21:(4):1-11 5 a b

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Figure 1. (a) Lateral view of the arteriogram prior to embolization, showing an AVM (white arrows) with a dilated posterior communicating artery supplying the lesion. (b) On a fMRI coronal section there is activation of the left hippocampus and parahippocampus (arrow heads), contralateral to the lesion (white arrows). (c) Lateral view of the arteriogram after the third embolization with 70% occlusion of the lesion.

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Figure 2. (a) Axial fMRI image in a patient with left temporal AVM (curved arrow) using a verb-generation paradigm. There was activation of Wernicke’s area only, in the right hemisphere (straight arrows). (b) Predominant left frontal activation (Broca’s area) (arrow heads).

6 Functional magnetic resonance imaging in The pre-operative evaluation of cerebral vascular malformations, Montes N; Herrera DA, Vargas SA Original Articles

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Figure 3. Motor paradigm. (a) Axial fMRI image. (b) Sagittal fMRI image. Patient with left parietal AVM (curved arrow) with activation of the left pre-central gyrus (straight arrows), with no sensory-motor cortex involvement.

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Figure 4. Patient with left temporal cavernous malformation (curved arrows) and ipsilateral language dominance, as shown by greater left inferior frontal activation. The activation zone appears in contact with the lesion. (a) Axial section of susceptibility image fusion (SWI) and language fMRI. (b) Sagittal section of SWI fusion and language fMRI.

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Figure 5. Patient with right thalamic AVM (curved arrow). (a) Image with axial T2 information. (b) Motor left-hand coronal fMRI showing the relationship between the lesion and the activated cortex (straight arrows). nantly in the left side. Bilateral activation was secondary to the Patient 7: left occipital arteriovenous malformation patient’s inability to keep the left hand still during the test, an This case is of a 38 year-old male with partial seizures with involuntary response elicited by the effort required to move visual component in the form of plain hallucinations. The MRI the paretic limb. The fMRI for language assessment using a scan showed a small left occipital AVM (Figure 7). A visual verb-generation paradigm did not show a significant difference paradigm consisting of eye closing and opening with a block in frontal activation between the two hemispheres, suggesting pattern revealed normal activation in the primary visual cortex equal dominance (Figure 6). Embolization was performed, re- and reduced activation in the visual association cortex in the sulting in a 95% occlusion of the malformation, with no residual left side, where the lesion is located. The patient is waiting for neurological deficit. endovascular treatment.

Figure 6. Patient with AVM (curved arrow) involving the periventricular white matter and the left peri-insular region. (a) Axial section with T2 information. (b) Axial fMRI showing a bilateral dominance pattern for language, with symmetrical frontal (Broca’s area) and temporal (auditory) activation (straight arrows).

8 Functional magnetic resonance imaging in The pre-operative evaluation of cerebral vascular malformations, Montes N; Herrera DA, Vargas SA Original Articles Patient 8: left temporo-occipital arteriovenous malformation The case corresponds to a 12 year-old girl with a history of intra-parenchymal hematoma due to bleeding from a left temporo-occipital AVM (Figure 8a), with no neurological deficit. The fMRI was performed with the use of a language paradigm consisting of sentence completion, and revealed activation of Broca’s area in the left side. A paradigm for assessing cerebro- vascular reactivity (breath-holding) was also used with normal breathing cycles and 20-second cycles of apnea, showing neu- rovascular uncoupling at the malformation site (Figure 8b). This patient later underwent embolization of 50% of the lesion and is now awaiting radiosurgery.

Figure 8a. The axial and sagittal sections show a left temporo-occipital AVM. The application of the language paradigm showed activation of Broca’s area on the left side. A Family Wise Error with a corrected p value of 0.05 was used.

Figure 8b. Axial and sagittal sections using a breath-holding paradigm that shows neurovascular uncoupling at the site of the malformation. Figure 7. The axial image with T2 information shows a pial AVM (curved arrow) in the left occipital lobe. Using a visual fMRI paradigm, normal activation was found in the primary visual cortex (arrows) and reduced activation of the visual association cortex on the left This potential change in the structure of neural networks makes side, where the lesion is located. it critical to determine the exact anatomical localization of the eloquent cortex before undertaking any form of intervention Discussion (15). An example of this is the representation of the visual and The eloquent cerebral tissue may be at risk during treatment spatial memory exclusively in the contralateral hemisphere in of vascular malformations. It is important to know the relation- one of our patients with a right mid-temporal AVM who did not ship between the lesion and the eloquent cerebral territories in develop a deficit after three embolizations (Figure 1). order to balance the benefit from obliterating the malformation It has been accepted that fMRI is no substitute for intra- with the risk of residual neurological deficits (1,15). operative electrical cortical stimulation. However, it is useful Magnetic resonance imaging provides excellent anatomi- for pre-operative planning and mapping, because it reduces the cal details and is a reasonable approximation to the location of length and extent of the craniotomy (16, 17). The determination the eloquent areas in the normal brain. However, conventional of hemispheric dominance of language using fMRI is highly imaging does not provide direct information about functional consistent with the Wada test (18), and has the added advantage areas and may lead to localization errors, especially in patients of being a non-invasive technique that provides additional infor- with intracranial masses that cause anatomical distortions. mation about the spatial relationship between the lesion and the This problem also occurs in cases of vascular malformations language area (19). In this study, a qualitative method was used that may give rise to developmental cortical reorganization (1). to determine language lateralization and to define dominance in

Rev Colomb Radiol. 2010; 21:(4):1-11 9 the side that showed greater inferior frontal activation (Broca’s sisting of opening and closing the eyes, and we found normal area). This interpretation modality has been described previously activation in the primary visual cortex, and reduced activation with good agreement among different evaluators (19). of the visual association cortex on the left side, where the lesion Three activation patterns were identified in the patients is located (Figure 7). studied: left dominance for language (patients 4 and 8), mixed dominance (patient 2) and bilateral dominance (patient 6). Conclusion These types of responses with the use of language paradigms We described the use of fMRI in patients with vascular mal- in fMRI have already been described (20). We did not find a formations, showing complex activities of the in fourth atypical pattern described as right language dominance one or both hemispheres, depending on the paradigm employed where Broca’s area is localized in the right (19,20). and the relationship with the lesion, as a way to provide useful Aside from language reorganization found in patients with information for treatment planning. One of the limitations of the vascular malformations, there are also blood-flow abnormalities study was that fMRI findings were not validated by a different such as blood steal, with retrograde feedback of the distal ter- invasive or non-invasive technique. This is a preliminary report ritory that may interfere with signal intensity changes in fMRI describing the use of this method in patients with this type of when the BOLD technique is used (6). This fMRI method detects abnormality. A correlation of fMRI with other functional map- small changes in the magnetic properties of blood resulting ping techniques is required in order to determine its role in the from metabolic and vascular responses of neuronal activity (9). treatment of cerebral vascular malformations. A study found that blood-flow abnormalities associated with these malformations alter language lateralization in fMRI (6). This effect might explain the post-operative deficit (dyspha- References sia) found in one of the patients in our study after the resection of a left temporal AVM, with exclusive representation of Wer- 1. Latchaw RE, Hu X, Ugurbil K, Hall WA, Madison MT, Heros nicke’s area in the right side, according to the fMRI findings RC. Functional magnetic resonance imaging as a management (Figure 2). In order to avoid mistakes in the interpretation of tool for cerebral arteriovenous malformations. 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