Benign External Hydrocephalus in Infants A Single Centre Experience and Literature Review
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1 The Neuroradiology Journal 27: , doi: /NRJ Benign External Hydrocephalus in Infants A Single Centre Experience and Literature Review MARIA ADELE MARINO 1, ROSA MORABITO 1, SERGIO VINCI 1, ANTONINO GERMANÒ 2, MARILENA BRIGUGLIO 3, CONCETTA ALAFACI 2, ENRICOMARIA MORMINA 1, MARCELLO LONGO 1, FRANCESCA GRANATA 1 1 Neuroradiology Unit, Department of Biomedical Sciences and Morphologic and Functional Imaging, 2 Department of Neurosciences, Psychiatric and Anaesthesiological Sciences, Neurosurgery Unit, 3 National Research Council of Italy (CNR), Institute of Clinical Physiology (IFC), University of Messina; Messina, Italy Key words: CT, MR imaging, benign macrocephaly, paediatric hydrocephalus SUMMARY External hydrocephalus (EH) is a benign clinical entity in which macrocephaly is associated with an increase in volume of the subarachnoid space, especially overlying both frontal lobes, and a normal or only slight increase in volume of the lateral ventricles. Several pathogenic hypotheses have been proposed but the most accredited theory seems to be delayed maturation of the arachnoid villi. There is a consensus that this is a benign entity, correlated to a familial predisposition and, in some cases, inheritance. CT and MRI are very important to make a diagnosis but also to establish the prognosis in patients who encounter the rare complications such as subdural haematomas. In conclusion, CT and MRI can provide a highly accurate diagnosis in these patients, allowing a preliminary assessment of the prognosis, particularly regarding the enlarged subarachnoid space limits and the cortical vein sign which can predict a further complication. These results are obtained with the same examination performed in a standard CT or MRI study of the brain and no injection of contrast medium is needed. Introduction External hydrocephalus (EH) is a benign clinical entity in which macrocephaly is associated with an increase in volume of the subarachnoid space, especially overlying both frontal lobes, and a normal or only slight increase in volume of the lateral ventricles. Over the years, several terms have been used to describe this condition such as extraventricular hydrocephalus, pseudo-hydrocephalus, benign enlargement of the subarachnoid space, and subdural hygroma, demonstrating the confusion surrounding the entity. Although the most accredited theory seems to be the delayed maturation of arachnoid villi, several other pathogenic hypotheses, such as a valve mechanism created by tearing of the subarachnoid membrane and even hypomagnesaemia, have been proposed. However, there is a general consensus that EH is correlated to a familial predisposition and, in some cases, inheritance. The aim of this work is to describe the neuroradiological aspects of EH and to review the literature dealing with EH and its complications. Materials and Methods We retrospectively reviewed radiologic and clinicopathologic data from a cohort of five children (M:F 2:3; average age: 16 months) with EH. All patients were studied by transfontanellar ultrasound, skull radiograph baseline CT (CT Somatom Definition 64-slices) and MRI (Siemens 1.5-T Magnetom Vision). Retrospective analysis also included a detailed review of the literature, particularly regarding neuroimaging findings and complications. 245
2 Benign External Hydrocephalus in Infants Maria Adele Marino A B Figure 1 A 16-month-old female with BEH. MRI examination with axial T2-weighted image (A) and coronal T1-weighted image (B). Note the mild enlargement of the bifrontal subarachnoid spaces and inter-hemispheric fissure. Figure 2 Main neuroradiological criteria for BEH evaluation: A) inter-hemispheric fissure; B) sino-cortical width; C) cranio-cortical width. Results All children were characterized by macrocephaly radiographically defined as skull circumference more than two standard deviations above the mean. In all patients who underwent CT and MRI, we found bifrontal widening of the subarachnoid space (> 1 cm) and widened inter-hemispheric fissure at the frontal lobe with only mild enlargement of the remaining 246
3 The Neuroradiology Journal 27: , doi: /NRJ 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 months of age
4 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 external hydrocephalus is macrocephaly, radiographically defined as a head circumference two standard deviations above the mean or above the 97 th 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 248
5 The Neuroradiology Journal 27: , doi: /NRJ 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
6 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: doi: /archpedi Maytal J, Alvarez LA, Eikin C, et al. External hydrocephalus: radiologic spectrum and differentiation from cerebral atrophy. Am J Roentgenol. 1987; 148 (6): doi: /ajr Robertson WC Jr, Gomez MR. External hydrocephalus. Early finding in congenital communicating hydrocephalus. Arch Neurol. 1978; 35 (8): doi: / archneur Andersson H, Elfverson J, Svendsen P. External hydrocephalus in infants. Child Brain. 1984; 11 (6): 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): doi: / BF Greenberg MS. Handbook of Neurosurgery. New York: Thieme; p. 174; 7 th Edition. 7 Alvarez LA, Maytal J, Shinnar S. Idiopathic external hydrocephalus: natural history and relationship to benign familial macrocephaly. Pediatric. 1986; 77 (6): Zahl SM, Egge A, Helseth E, et al. Benign external hydrocephalus: a review, with emphasis on management. Neurosurg Rev. 2011; 34 (4): doi: / s Rumboldt Z, Castillo M, Huang B, et al. (eds). Brain imaging with MRI and CT: An image pattern approach. New York: Cambridge University Press; p doi: /CBO Paciorkowski AR, Greenstein RM. When is enlargement of the subarachnoid spaces not benign? A genetic perspective. Pediatr Neurol. 2007; 37 (1): 1-7. doi: /j.pediatrneurol Zahl SM, Egge A, Helseth E, et al. Benign external hydrocephalus: a review, with emphasis on management. Neurosurg Rev. 2011; 34 (4): doi: / s 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): 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): doi: / s 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): 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): doi: / Maria Adele Marino, MD Neuroradiology Unit Department of Biomedical Sciences and Morphologic and Functional Imaging University of Messina Via Consolare Valeria n Messina, Italy mariaadele84@hotmail.com 250
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