AINR - Associazione Italiana di Neuroradiologia

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VOLUME 27 - No. 2 - APRIL 2014

CENTAURO S.r.l., BOLOGNA

Bimestrale - Poste Italiane s.p.a. - Sped. in a.p. - D.L. 353/2003 (conv. in L. 27/02/2004 n° 46) art. 1, comma 1, DCB/BO

Euro 30,00 ISSN 1971-4009

Official Journal of:

AINR - Associazione Italiana di Neuroradiologia and: The Neuroradiologists of Alpe-Adria ANRS - Albanian Neuroradiological Society PANRS - Pan Arab NeuroRadiology Society Radiological Society of Saudi Arabia, Division of Neuroradiology Egyptian Society of Neuroradiology ISNR - Indian Society of Neuroradiology Indonesian Society of Neuroradiology Neuroradiology Section of the Radiology Society of Iran Israeli Society of Neuroradiology College of Radiology Malaysia

Neuroradiology Section - Pakistan Psychiatry Research Center Section of Neuroradiology - Polish Radiological Society The Neuroradiologists of Romania Section of Neuroradiology of Serbia and Montenegro SILAN - Sociedad Ibero Latino Americana de Neurorradiologia Neuroradiology Section of Singapore Radiological Society Slovenian Society of Neuroradiology The Neuroradiological Society of Taiwan TSNR - Turkish Society of Neuroradiology

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Official Journal of:

AINR - Associazione Italiana di Neuroradiologia and The Neuroradiologists of Alpe-Adria ANRS - Albanian Neuroradiological Society PANRS - Pan Arab NeuroRadiology Society Radiological Society of Saudi Arabia, Division of Neuroradiology Egyptian Society of Neuroradiology ISNR - Indian Society of Neuroradiology Indonesian Society of Neuroradiology Neuroradiology Section of the Radiology Society of Iran Israeli Society of Neuroradiology College of Radiology Malaysia Neuroradiology Section - Pakistan Psychiatry Research Center Section of Neuroradiology - Polish Radiological Society The Neuroradiologists of Romania Section of Neuroradiology of Serbia and Montenegro SILAN - Sociedad Ibero Latino Americana de Neurorradiologia Neuroradiology Section of Singapore Radiological Society Slovenian Society of Neuroradiology The Neuroradiological Society of Taiwan TSNR - Turkish Society of Neuroradiology

Index Methodology Brain Targets: Can You Believe Your Own Eyes?

133

Giovanni Stefanoni, Marco Tironi, Lucio Tremolizzo, Maria Letizia Fusco, Jacopo Di Francesco, Mirko Patassini, Carlo Ferrarese, Ildebrando Appollonio

Predicting Arterial Injuries after 138 Penetrating Brain Trauma Based on Scoring Signs from Emergency CT Studies

Uttam K. Bodanapally, Jaroslaw Krejza, Nitima Saksobhavivat, Paul M. Jaffray, Clint W. Sliker, Lisa A. Miller, Kathirkamanathan Shanmuganathan, David Dreizin

Anatomical Variants Into the Septum I Go, a Case of Bilateral 146 Ectopic Infraorbital Nerves: a Not-to-Miss Preoperative Sinonasal CT Variant Hosam Elnil, Jarrah A Al-Tubaikh, Ahmed H El Beltagi

Goldenhar Syndrome Associated with Contralateral Agenesis of the Internal Carotid Artery

150

Arachnoid Cyst of the Cavum Velum Interpositum in a Septuagenarian: Radiological Features and Differential Diagnosis

154

Elisa Ventura, Francesca Ormitti, Girolamo Crisi, Enrico Sesenna

S Rajesh, Shorav Bhatnagar, Udit Chauhan, Shailesh Gupta, Nitesh Agarwal, Vivek Kasana

fMRI Functional Connectivity MRI and Post-Operative Language Performance in Temporal Lobe Epilepsy: Initial Experience

Emanuele Pravatà, Carlo Sestieri, Gabriella Colicchio, Cesare Colosimo, Gian Luca Romani, Massimo Caulo

Cover: Pablo Picasso (1881-1973), Mousquetaire au Chapeau, Buste, 1967 - Oil on canvas, 78,8 × 64 cm Private collection - Di Cea - http://www.flickr.com

158

Tumours Neuroradiology and Histopathology in Two Cases of Adult Medulloblastoma

163

Alfredo E. Romero-Rojas, Julio A. Diaz-Perez, Sharat Raju, Alfonso Lozano-Castillo

Neural Stem Cells and Glioblastoma

Rossella Rispoli, Carlo Conti, Paolo Celli, Emanuela Caroli, Sandro Carletti

169

Extraneural Metastasis of an Ependymoma: a Rare Occurrence

175

Multisegmental Diffuse Intradural Extramedullary Ependymoma. An Extremely Rare Case

179

Symptomatic Anterior Cerebral Artery Vasospasm after Brainstem Hemangioblastoma Resection

186

Ahmed Alzahrani, Ali Alassiri, Amna Kashgari, Jihad Alrehaili, Hesham Alshaalan, Reem Zakzouk

Gianluigi Guarnieri, Mario Tecame, Roberto Izzo, Fabio Zeccolini, Luigi Genovese, Mario Muto

A Chronic Intracerebral Fluid Hematoma 191

Motohiro Nomura, Katsuyoshi Miyashita, Akira Tamase, Tomoya Kamide, Kentaro Mori, Yoshihisa Kitamura, Shunsuke Seki, Hiroshi Shima, Kunio Yanagimoto

195

Thomas Jose Eluvathingal Muttikkal, Prashant Raghavan

Vascular Flat Panel Angiography Images in the Post-Operative Follow-Up of Surgically Clipped Intracranial Aneurysms

Caterina Budai, Luigi Cirillo, Francesco Patruno, Massimo Dall’Olio, Ciro Princiotta, Marco Leonardi

Rajendra Gajanan Chavan, Ravindra Bhimrao Kamble, Vivek Bonde

Long-Term Treatment Outcomes after Intravascular Ultrasound Evaluation and Stent Placement for Atherosclerotic Subclavian Artery Obstructive Lesions

213

Coexistence of Cavernous Hemangioma and Other Vascular Malformations of the Orbit

223

Takeshi Wada, Katsutoshi Takayama, Toshiaki Taoka, Hiroyuki Nakagawa, Kaoru Myouchin, Toshiteru Miyasaka, Toshiaki Akashi, Masahiko Sakamoto, Kimihiko Kichikawa

Diego Strianese, Manuela Napoli, Carmela Russo, Arianna D’Errico, Nadia Scotti, Gianfranco Puoti, Giulio Bonavolontà, Fausto Tranfa, Francesco Briganti

Pediatric Neuroradiology

Andrea Prontera, Annette Puzzolante, Paolo Carpeggiani, Giacomo Pavesi

Spontaneous Regression and Recurrenc of a Tumefactive Perivascular Space

Endovascular Treatment in an Unusual 207 Case of Direct Carotid Cavernous Fistula

Use of Apparent Diffusion Coefficient Values for Diagnosis of Pediatric Posterior Fossa Tumors

233

Theodore Pierce, Peter G. Kranz, Christopher Roth, Dalun Leong, Peter Wei, James M. Provenzale

Benign External Hydrocephalus in Infants. 245 A Single Centre Experience and Literature Review

Maria Adele Marino, Rosa Morabito, Sergio Vinci, Antonino Germanò, Marilena Briguglio, Concetta Alafaci, Enricomaria Mormina, Marcello Longo, Francesca Granata

203 Information & Congresses

Instructions for Authors

Indexed in: National Library of Medicine’s MEDLINE database (http://www.ncbi.nlm.nih.gov/pubmed/ - Search: neuroradiol j) EMBASE - Scopus (http://www.scopus.com) Google Scholar (http://scholar.google.com) ISSN 1971-4009

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The Strength of Relaxivity MultiHance : significantly improved CNS lesion visualization vs gadobutrol ®

*

1

* Significantly better contrast enhancement, definition of lesion extent, delineation of lesion borders, and depiction of lesion internal morphology; greater enhancement of lesion-brain contrast-to-noise ratio (CNR) and lesion-to-brain ratio. 1. Does Higher Gadolinium Concentration Play a Role in the Morphologic Assessment of Brain Tumors? Results of a Multicenter Intraindividual Crossover Comparison of Gadobutrol versus Gadobenate Dimeglumine (the MERIT study); Seidl et al, AJNR, Published online before print March 1, 2012, doi: 10.3174/ ajnr.A3033, AJNR 2012. 2. Maravilla KR et al. Contrast enhancement of central nervous system lesions: multicenter intraindividual crossover comparative study of two MR contrast agents. Radiology. 2006;240(2):389-400 3. Contrast-Enhanced MR Imaging of Brain Lesions: A Large-Scale Intraindividual Crossover Comparison of Gadobenate Dimeglumine versus Gadodiamide. HA. Rowley, AJNR Am J Neuroradiol. 2008 Jul 3 - MH-130 Please see full Prescribing Information. Before use, please consult the locally approved Summary of Product Characteristics, which will be made available upon request. MULTIHANCE - SUMMARY OF PRODUCT CHARACTERISTICS MultiHance, 0.5 M solution for injection Composition 1 ml of solution for injection contains: gadobenic acid 334 mg (0.5 M) as the dimeglumine salt. [Gadobenate dimeglumine 529 mg = gadobenic acid 334 mg + meglumine 195 mg]. Excipients Water for injections. Therapeutic indications and dosage This medicinal product is for diagnostic use only. MultiHance is a paramagnetic contrast agent for use in diagnostic magnetic resonance imaging (MRI) indicated for: MRI of the brain and spine for patients 2 years and older where it improves the detection of lesions and provides diagnostic information additional to that obtained with unenhanced MRI (0.2 mL/kg); Contrast-enhanced MR-angiography for adult patients where it improves the diagnostic accuracy for detecting clinically significant steno-occlusive vascular disease in patients with suspected or known vascular disease of the abdominal or peripheral arteries (0.2 mL/kg); MRI of the liver for the detection of focal liver lesions in adult patients with known or suspected primary liver cancer (e.g. hepatocellular carcinoma) or metastatic disease (0.1 mL/kg); MRI of the breast, for the detection of malignant lesions in patients where breast cancer is known or suspected on the basis of previous mammography or ultrasound results (0.2 mL/kg) Contra-indications MultiHance is contra-indicated in: patients with hypersensitivity to any of the ingredients; in patients with a history of allergic or adverse reactions to other gadolinium chelates. Special warnings and special precaution for use MultiHance should not be admixed with any other drug; the product should not be frozen, and it should be used immediately after drawing into the syringe. Patients should be kept under close supervision for 15 minutes following the injection as the majority of severe reactions occur at this time. The patient should remain in the hospital environment for one hour after the time of injection. The accepted general safety procedures for Magnetic Resonance Imaging, in particular the exclusion of ferromagnetic objects, for example cardiac pace-makers or aneurysm clips, are also applicable when MultiHance is used. Caution is advised in patients with cardiovascular disease. The use of diagnostic contrast media, such as MultiHance, should be restricted to hospitals or clinics staffed for intensive care emergencies and where cardiopulmonary resuscitation equipment is readily available. Small quantities of benzyl alcohol ( 1 cm) and widened inter-hemispheric fissure at the frontal lobe with only mild enlargement of the remaining

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The Neuroradiology Journal 27: 245-250, 2014 - doi: 10.15274/NRJ-2014-10020

subarachnoid spaces and only a slight increase in ventricular volume. In our experience, only one patient had a subdural spontaneous haematoma as a complication. Discussion History Studies in the pre-CT era suggested that the most frequent cause of macrocephaly was communicating or non-communicating hydrocephalus. According to the literature, the term external hydrocephalus (EH) was first used by Dandy in 1917 to describe the enlargement of the subarachnoid space in the presence of increased intracranial pressure 1. In the post-CT era, Robertson and Gomez reintroduced the term external hydrocephalus to describe a condition in which children with macrocephaly have a CT scan of enlarged subarachnoid spaces with mild to moderate or no ventricular dilation 2,3. In 1984, Andersson et al. performed craniotomies on patients with idiopathic EH and they found enlarged subarachnoid space without other abnormalities demonstrating that this disease should not be treated with a shunt 4. Ordita compared the clinical and radiologic characteristics of subarachnoid widening in macrocephalic children and in normocephalic or microcephalic children and concluded that the term “external hydrocephalus” is inappropriate in the absence of significant ventricular widening and clinical signs of raised intracranial pressure 5. Other terms such as extraventricular hydrocephalus, pseudo-hydrocephalus, benign enlargement of the subarachnoid space, and subdural hygroma were then used by different authors, demonstrating the confusion that surrounds the entity. Today, the good prognosis and benign nature of this condition which can be spontaneously resolved, suggest that benign external hydrocephalus (BEH) is the best expression to be used referring to this disease. Epidemiology BEH accounts for 0.5 to 0.8 per 1000 live and still births and the condition occurs more commonly in boys than in girls, with the same incidence and gender distribution as in hydrocephalus 6. In most cases, there is a positive family history of macrocephaly and this is generally

a condition that resolves spontaneously by two years of age. These findings confirm that idiopathic external hydrocephalus is a relatively benign, self-limited condition that resolves without treatment and which is closely related to benign familial macrocephaly 7. Despite its benignity, BEH can influence psychomotor or motor retardation and behavioural disorders. Several authors describe a transient delay of psychomotor development during childhood. Although most children with external hydrocephalus seem to do well both initially and in the long term, an important number of patients show temporary or permanent psychomotor delay 8. Pathogenesis According to Barkovich, the most favourable pathogenesis hypothesis leading to BEH should be researched in a delayed maturation of the arachnoid villi. Due to immaturity of arachnoid granulations, absorption of CSF may not keep pace with CSF production for a period of time in children under two years of age, resulting in CSF accumulation in the subarachnoid spaces, leaving the ventricles normal or only mildly prominent. BEH may also be caused by amplification of the physiologic imbalance between skull and brain growth in normal infants between three months and one year of age 9. Bhasker et al. described the association between hypomagnesaemia and reversible external hydrocephalus in two siblings as a possible consequence of the derangement of one or more enzymatic functions in magnesium deficiency, even if the precise mechanism responsible for this brain shrinkage is still unknown. Enlargement of the subarachnoid spaces can be an early sign in several genetic disorders or the feature of an associated syndrome that may aid in the underlying diagnosis. Recognizing subarachnoid space enlargement in these circumstances, such as mucopolysaccharidosis, achondroplasia, agenesis of the corpus callosum, Sotos syndrome and glutaric aciduria, requires an understanding of the normal physiology of the subarachnoid space at different time points in a child’s neurodevelopment. This genetic disorder should be considered in patients with enlargement of the subarachnoid spaces who do not fit the expected normal patterns of development, or in those patients where the finding does not resolve after 18-24 months of age 10. 247

Benign External Hydrocephalus in Infants

Maria Adele Marino

Figure 3 A two-year-old male with BEH. MRI examination with axial FLAIR sequence showed a bilateral subdural fluid collection with recent bleeding on the right side.

Neuroimaging Nowadays, neuroimaging performs the most important role in the diagnosis of external hydrocephalus. Thanks to progress, especially in CT and MRI examinations, a detailed analysis of the most prominent features leading to a diagnosis of BEH is possible. Today, BEH is diagnosed either by transfontanellar ultrasound or, more commonly, by CT scanning or MRI. CT and MRI technologies are therefore a central part in the diagnosis, and they are also fundamental in the evaluation of treatment options, follow-up and monitoring of patients. Skull radiography is rarely used and the art of its interpretation is slowly being lost by younger radiologists, but it can still play a role in some cases and could represent the first level approach to a child with an abnormal cranial structure or head shape. The only x-ray sign in benign 248

external hydrocephalus is macrocephaly, radiographically defined as a head circumference two standard deviations above the mean or above the 97th percentile of at least 0.5 cm. The most specific neuroradiological feature in BEH is an extension of the subarachnoid spaces in the frontal lobes with a normal or only slight increase in ventricular volume as can be appreciated by transfontanellar ultrasound, MRI and CT scan. Transfontanellar ultrasonography can easily make the diagnosis of BEH by evaluating the skull-to-cortex distance that in children with this condition is greater than 5 mm 11. Transfontanellar ultrasound is also useful in assessing the presence of ventriculomegaly in infants, especially allowing a differential diagnosis between a benign enlargement of the subarachnoid space and subdural fluid collection caused by meningitis, haemorrhage or trauma. The characteristic CT findings in

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The Neuroradiology Journal 27: 245-250, 2014 - doi: 10.15274/NRJ-2014-10020

BEH are bifrontal widening of the subarachnoid space and widened inter-hemispheric fissure at the frontal lobe with only mild enlargement of the remaining subarachnoid spaces (Figure1). Occasionally, mild to moderate ventriculomegaly is also present. In most cases, the radiological findings could be distinguished from those seen in cerebral atrophy, even without the clinical history of an enlarging head. So far, in agreement with ALARA principles, the examination of choice in children with BEH should be MRI, and CT in children should be considered an option only for patients who cannot be subjected to a MRI study. There is no consensus on the limits of the enlargement of subarachnoid spaces: many inclusion criteria have been tried to study the enlarged subarachnoid space, measuring at the conventional coronal section the level of the interventricular foramen. The defined upper limits of cranio-cortical width range from 3 to 5 mm, but from 4 to 10 mm in infants aged under one year. An enlargement of the inter-hemispheric fissure has been defined as a width upper than 8.5 mm, while the similar spectrum for sinocortical width (the distance from the lateral wall of the superior sagittal sinus to the surface of the cerebral cortex) is 2-10 mm (Figure 2) 12. Enlargement of the basal cisterns and ventricular dilation, when they occur, are later findings. BEH must be differentiated from conditions such as subdural fluid collections and cerebral atrophy, and from a subdural fluid collection. McCluney et al. proposed the so-called “cortical vein sign” defined as the visualization of cortical veins within fluid collections at the cerebral convexities, detectable on both CT scan and MRI examination. A positive sign suggests that the fluid collection is caused by an enlarged subarachnoid space and not by a subdural collection which would compress the subarachnoid space and the veins traversing it. However, the cortical veins lie between the dura and the arachnoid near the sinuses and they can even be seen in patients with subdural hygroma 13. Cerebral atrophy differs from BEH in the global widening of cerebral sulci and not only in the frontal region and there is no evidence of an increasing head circumference. MRI appears essential in the differential diagnosis between benign enlargement of the subarachnoid spaces and subdural collections in infants. The presence of subdural collections is often missed in CT scans, whereas in MRI imaging two separate layers are clearly

differentiated, an outer layer hyperintense on all sequences and an inner layer with the same intensity as the cerebrospinal fluid 14. Sun et al. demonstrated that diffusion tensor imaging can be an important tool in the diagnosis of BEH. They found a significant increase in fractional anisotropy and a decrease in mean diffusivity in children with BEH compared with normal children, so subtle diffusion changes could be taken as preliminary objective radiographic parameters for watchful observation of patients with BEH 15. Complications CT and MRI are also important for evaluating the most common complication associated with BEH. Patients who have benign enlargement of the subarachnoid spaces have been suspected of having an increased propensity for subdural haematomas either spontaneously or as a result of accidental injury (Figure 3). Enlarged subarachnoid spaces represent a risk factor for the development of subdural haematomas following minimal or no trauma. This could be explained by the stretching of the bridging veins in the subdural space due to the enlargement of the CSF spaces. BEH also results in an increased incidence of chronic subdural effusions. Papasian et al. proposed a model of the intracranial space to predict situations where children with BEH will bleed into the extraaxial space when normal infants will not 16. Conclusions This study confirmed the traditional idea that BEH is a benign condition that, in most cases, does not need treatment. Radiological studies are very important to make a diagnosis and also to establish the prognosis in those patients who encounter the rare complications. CT and MRI are able to provide a highly accurate diagnosis in these patients, allowing a preliminary assessment of the prognosis, particularly regarding the enlarged subarachnoid spaces size, course and extent, and to evaluate signs, such as the “cortical vein” sign, which can help the radiologist predict a further complication. These results are obtained with the same examination performed in a standard CT or MRI study of the head and no injection of intravenous contrast is needed. These examinations are easy to perform and are essential for accurate diagnosis and follow-up. 249

Benign External Hydrocephalus in Infants

Maria Adele Marino

References 1 Dandy WE, Blackfan KD. Internal hydrocephalus: an experimental clinical and pathological study. Am J Dis Child. 1914; 8: 406-482. doi: 10.1001/archpedi.1914.02180010416002. 2 Maytal J, Alvarez LA, Eikin C, et al. External hydrocephalus: radiologic spectrum and differentiation from cerebral atrophy. Am J Roentgenol. 1987; 148 (6): 1223-1230. doi: 10.2214/ajr.148.6.1223. 3 Robertson WC Jr, Gomez MR. External hydrocephalus. Early finding in congenital communicating hydrocephalus. Arch Neurol. 1978; 35 (8): 541-544. doi: 10.1001/ archneur.1978.00500320061014. 4 Andersson H, Elfverson J, Svendsen P. External hydrocephalus in infants. Child Brain. 1984; 11 (6): 398-402. 5 Ordita JC. The widened frontal subarachnoid space. A CT comparative study between macrocephalic, microcephalic, and normocephalic infants and children. Childs Nerv Syst. 1992; 8 (1): 36-39. doi: 10.1007/ BF00316560. 6 Greenberg MS. Handbook of Neurosurgery. New York: Thieme; 2010. p. 174; 7th Edition. 7 Alvarez LA, Maytal J, Shinnar S. Idiopathic external hydrocephalus: natural history and relationship to benign familial macrocephaly. Pediatric. 1986; 77 (6): 901-907. 8 Zahl SM, Egge A, Helseth E, et al. Benign external hydrocephalus: a review, with emphasis on management. Neurosurg Rev. 2011; 34 (4): 417-432. doi: 10.1007/ s10143-011-0327-4. 9 Rumboldt Z, Castillo M, Huang B, et al. (eds). Brain imaging with MRI and CT: An image pattern approach. New York: Cambridge University Press; 2012. p. 387-388. doi: 10.1017/CBO9781139030854. 10 Paciorkowski AR, Greenstein RM. When is enlargement of the subarachnoid spaces not benign? A genetic perspective. Pediatr Neurol. 2007; 37 (1): 1-7. doi: 10.1016/j.pediatrneurol.2007.04.001. 11 Zahl SM, Egge A, Helseth E, et al. Benign external hydrocephalus: a review, with emphasis on management.

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Neurosurg Rev. 2011; 34 (4): 417-432. doi: 10.1007/ s10143-011-0327-4. Jang U-J, Lee K-S, Shim J-J, et al. Diagnostic value of the cortical vein sign: unreliable index of atrophy on MR image. J Kor Neurotraumatol Soc. 2006; 2 (1): 13-17. Sun M, Yuan W, Hertzler DA, et al. Diffusion tensor imaging findings in young children with benign external hydrocephalus differ from the normal population. Childs Nerv Syst. 2012; 28 (2): 199-208. doi: 10.1007/ s00381-011-1651-2. Wilms G, Vanderschueren G, Demaerel PH, et al. CT and MR in infants with pericerebral collections and macrocephaly: benign enlargement of the subarachnoid spaces versus subdural collections. Am J Neuroradiol. 1993; 14 (4): 855-860. Papasian NC, Frim DM. A theoretical model of benign external hydrocephalus that predicts a predisposition towards extra-axial hemorrhage after minor head trauma. Pediatr Neurosurg. 2000; 33 (4): 188-193. doi: 10.1159/000055951.

Maria Adele Marino, MD Neuroradiology Unit Department of Biomedical Sciences and Morphologic and Functional Imaging University of Messina Via Consolare Valeria n°1 98125 Messina, Italy E-mail: [email protected]

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