Prenatal Imaging of Occipital Encephaloceles

E-Mail [email protected]

Original Paper

Fetal Diagn Ther DOI: 10.1159/000366159

Prenatal Imaging of Occipital Encephaloceles

Gregor J. Kasprian a Michael J. Paldino b, d Amy R. Mehollin-Ray b, d Anil Shetty c, e Jennifer L. Williams b, d Wesley Lee c, e Chris I. Cassady b, d

a Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna, Vienna , Austria; Departments of b Radiology and c Obstetrics and Gynecology, Baylor College of Medicine, d E.B. Singleton Department of Pediatric Radiology, Texas Children’s Hospital, and e Texas Children’s Pavilion for Women, Houston, Tex. , USA

brainstem, white matter pathway and cerebral venous in-volvement and facilitates the detection of specific underly-ing syndromes such as ciliopathies. © 2014 S. Karger AG, Basel

Introduction

Encephaloceles are congenital malformations of the central nervous system characterized by the protrusion of meninges and cerebral tissue through a bony defect of the skull. Although their true embryological etiology re-mains unclear [1] , (meningo-)encephaloceles are cur-rently classified as rare neural tube defects with a preva-lence of 0.8–5 per 10,000 live births [2] . The sociodemo-graphic characteristics of patients with encephaloceles share many commonalities with patients with spinal dys-raphism and anencephaly [3] . In Europe and the USA, encephaloceles are most frequently located occipitally (2/3 cases); frontal, temporal and parietal locations are less common [3] . Associated cerebral and extracentral nervous system anomalies are found in a significant number of cases (20.5–60% depending on the examined patient cohort [2, 4] ).

When encephaloceles are detected prenatally, there is a need for detailed diagnostic assessment and character-ization of a possible underlying syndrome [5] .

The heterogeneity in their morphology and molecular pathology explains the variable outcome of fetuses with oc-

Key Words

Diffusion tensor imaging · Joubert syndrome · Brain malformations · Ciliopathy · Fetal neurology

Abstract

Introduction: This retrospective study aims to describe sys-tematically the fetal cerebral MR morphology in cases with occipital meningoencephaloceles using standard and ad-vanced fetal MRI techniques. Material and Methods: The 1.5-tesla MR examinations (T1- and T2-weighted imaging, echo planar imaging, EPI, diffusion-weighted imaging, DWI) of 14 fetuses with occipital/parietal meningoencephaloceles were retrospectively analyzed for the classification of ana-tomic characteristics. A diffusion tensor sequence was per-formed in 5 cases. Results: In 9/14 cases the occipital lobes were entirely or partially included in the encephalocele sac. Typical features of Chiari III malformation were seen in 6/14 cases. The displaced brain appeared grossly disorganized in 6/14. The brainstem displayed abnormal ‘kinking’/rotation (3/14), a z-shape (1/14) and/or a molar tooth-like configura-tion of the midbrain (3/14). Tractography revealed the pres-ence and position of sensorimotor tracts in 5/5 and the cor-pus callosum in 3/5. DWI was helpful in the identification of a displaced brain (in 8/9). EPI visualized the anatomy of draining cerebral veins in 7/9 cases. Clinical (9/14) and MRI (7/14) follow-up data are presented. Discussion: Encephalo-celes show a wide range of morphological heterogeneity. Fetal MRI serves as an accurate tool in the visualization of

Received: May 5, 2014 Accepted after revision: July 25, 2014 Published online: Octo ber 29, 2014

Gregor Kasprian, MD Department of Biomedical Imaging and Image-Guided Therapy Medical University of Vienna , Währinger Gürtel 18–20AT–1090 Vienna (Austria) E-Mail gregor.kasprian @ meduniwien.ac.at

© 2014 S. Karger AG, Basel1015–3837/14/0000–0000$39.50/0

www.karger.com/fdt

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Kasprian/Paldino/Mehollin-Ray/Shetty/Williams/Lee/Cassady

Fetal Diagn TherDOI: 10.1159/000366159

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cipital and parietal meningoencephaloceles. As a group, half of them will be unable to live and function independently in society [4, 6] . As the presence of associated intracranial pa-thologies, including brain malformations, is predictive for the cognitive outcome [6] , imaging plays an important role in the diagnostic workup of these conditions and often serves as the primary basis for prenatal counseling.

Up to 80% of meningoencephaloceles can be detected by sonography during the first trimester [7] and, depend-ing on the geographic region, almost all cases are identi-fied after the second-trimester scan [8] . A detailed neuro-sonographic examination offers a depiction of the bony skull defect and the size and morphology of the herniated meningeal and brain tissue. However, due to the extreme divergence from normal brain anatomy in these cases, some morphological findings, such as the presence or ab-sence of neuronal migration disorders (subependymal heterotopia [9] , polymicrogyria and brainstem abnor-malities [10] ) or the position of developing white matter pathways, may be difficult to visualize by ultrasound. Currently, there are very few fetal MRI data available on this subject. Hence, this study aimed to systematically de-scribe the fetal cerebral MR morphology in cases with oc-cipital and parietal meningoencephaloceles using stan-dard and advanced (diffusion-weighted imaging, DWI, diffusion tensor imaging, DTI and susceptibility-weight-ed imaging) fetal MRI techniques.

Material and Methods

This study, which was compliant with the Health Insurance Portability and Accountability Act, was approved by the local in-stitutional review board at Baylor College of Medicine. Patients were identified retrospectively from a search in the existing patient track record database of Texas Children’s hospital. Inclusion cri-teria included the following: (1) fetuses older than 18 gestational weeks (GW; gestational age was verified by biometry during the first sonographic examination and presented as postmenstrual age), (2) referral after abnormal ultrasound screening, (3) prenatal MR examinations between 2004 and 2013 and (4) cranial menin-goceles or meningoencephaloceles in occipital or parietal location.

Imaging Fetal MRI data were retrieved from 2 different 1.5-tesla MR sys-

tems. Examinations before the year 2011 were performed on a Phil-ips Intera and those after 2011 on a Philips Ingenia MRI unit (Phil-ips, Best, The Netherlands). On both systems, T2-weighted se-quences were acquired in 3 orthogonal planes (TR/TE = 1,558/80 ms, resolution 1.09 × 1.1 × 4 mm, FOV = 280 mm). In 9 cases an axial echo planar sequence (echo planar imaging, EPI, TR/TE = 5,290/104 ms, resolution = 1.17 × 1.17 × 3 mm, FOV = 280) and in 10 cases an axial diffusion-weighted sequence (DWI, TR/TE = 2,007/84 ms, resolution = 2 × 2 × 5 mm, b-values of 0 and 700

s/ mm 2 ) was available. In the most recent 5 cases, an axial diffusion tensor sequence (DTI, TR/TE = 2,189/60 ms, b-values of 0 and 700 s/mm 2 , resolution = 2 × 2 × 4 mm, 16 gradient-encoding direc-tions, FOV = 230, scan time = 1 min 12 s) was also performed. Trac-tography was performed by a neuroradiologist with experience in fetal imaging (G.J.K.) using the provider-specific software (Philips Ingenia, version 4.1.2) and a deterministic approach with user-de-fined regions of interest and a linear tractography algorithm (thresholds: minimum angle change = 27°, minimum fractional an-isotropy value = 0.1), as described elsewhere in further detail [11] .

Results

A total of 14 cases with parietal and/or occipital me-ningoencephaloceles were identified – except for 1 case, which appeared to be a meningocele only ( table 1 ; fig. 1–4 ). The mean fetal age at imaging was 26 + 3 GW. Clinical follow-up data is available for 9 patients ( table 2 ).

All cases were detected by prior ultrasound screening examinations. Except for the case with a meningocele only ( fig. 2 , case 13), 13 cases showed a variable degree of brain displacement ( table 1 ). Diffusion-weighted sequences were particularly helpful in the detection of herniated brain tissue, which visualized the displaced brain struc-tures with similar diffusivity to the normal-appearing nondisplaced brain parenchyma in 8/9 cases ( fig. 5 , 6 ).

An exact anatomical description of displaced brain structures was possible in all cases. In 9/13 cases the oc-cipital lobes were entirely or at least partially included in the encephalocele sac.

In further detail, the displaced brain regions included the following: (1) the occipital poles (3/13), (2) the en-tirety of the occipital lobe (bilaterally 2/13, unilaterally 1/13), (3) both the parietal and occipital lobes (bilaterally 1/13, unilaterally 2/13), (4) the parietal lobe only (1/13) and (5) parts of the brainstem, the cerebellum and the temporal and occipital lobes bilaterally (2/13; table 1 ). In 1 case, only parts of the frontal lobes, medulla and pons were identified intracranially.

The neural tissue of the encephalocele was grossly dis-organized in 9/14 ( fig. 1 , 3 , 4 ) and showed polymicrogyria in 1/14 cases. Hemorrhagic components were found in 3/14 cases. In 6/14 cases histology of the surgically resect-ed encephalocele was available and confirmed the pres-ence of polymicrogyria in 1 case. In 4 cases, histology re-vealed the presence of neuroglial heterotopia as correlate for the gross ‘disorganization’ visible at prenatal MRI ( ta-ble 2 ).

The typical features of the so-called ‘Chiari III malformations’ [12] (crowding of the posterior fossa,

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‘lemon sign’, vermian displacement) were seen in 6/14 cases ( table 1 ), whereas 4/14 cases showed no ‘lemon sign’ but isolated diminution of external CSF spaces.

MRI was able to reveal an exact morphological de-scription of the brainstem configuration, showing an abnormal morphology in 5/14 cases (3/14 showed an

abnormal ‘kinking’/rotation; fig. 1 ). An unequivocal molar tooth sign was seen in 1 case ( fig. 2 ), whereas 2 other cases showed a molar tooth-like configuration of the midbrain ( fig. 5 , 6 ); in 1 of these (case 11, with a z-shaped brainstem) the final diagnosis of Walker-Warburg syndrome was established by gene sequenc-

Table 1. Pre- and postnatal imaging characteristics of encephalocele cases

Patient GWat MRI

Location Extracranial structures

Skull shape Brainstem Exteriorized brain tissue Corpus callosum

Added information by postnatal MRI/CT

1 28+6 Lowoccipital

Pons, midbrain, cerebellum, occipital, temporal lobes

Flat forehead Not assessable Polymicrogyria Not assessable Polymicrogyria confirmed

2 22+4 Occipital Occipital lobes Flat forehead, Chiari III

Kinking/rotation Disorganized, hemorrhage/calcification

Not assessable

3 20+5 Occipital All supratentorial structures, midbrain

Flat forehead, Chiari III

Kinking/rotation Disorganized Not assessable

4 24+3 Occipital Occipital lobes, temporal lobes, midbrain, pons, cerebellum

Flat forehead, Chiari III

Kinking/rotation Relatively organized, not normal

Not assessable

5 19+5 Occipital Occipital pole Normal Posteriorly displaced

Disorganized, hemorrhage/calcification

Complete

6 25+5 Occipital Unilateral parietal and occipital lobe

Normal Normal Disorganized, hemorrhage/calcification

Complete Added: vascular anatomy clarified/confirmed, no calcification

7 28+5 Low occipital

Occipital pole Normal Molar tooth sign, medullary thickening

Meningocele Complete Molar tooth, polymicrogyria confirmed

8 30+5 Occipital Occipital lobes Normal, no eCSF

Normal Disorganized, hemorrhage/calcification

Not assessable

9 27 Parietal Parietal lobe Normal, no eCSF

Normal Disorganized Not assessable Added: exact extent of bony defect

10 18+6 Parietal Unilateral parietal and occipital lobe

Chiari III Normal Disorganized Not assessable Sinus tract, hemorrhagic transformation confirmed; added: normal corpus callosum

11 19+6 Occipital Occipital pole Chiari III Kinking, molar tooth-like midbrain

Disorganized Not fully assessable, anterior there

Added: bilateral polymicrogyria, dysplastic corpus callosum; confirmed: z-shaped brainstem, molar tooth-like midbrain

12 24+1 Low occipital

Occipital lobes Chiari III Kinking, molar tooth-like midbrain

Disorganized Complete Changed: no occipital lobes herniated, cerebellum displaced

13 28+4 Occipital Meningocele Normal Normal No brain tissue Complete

14 27 Occipital Occipital pole Chiari III Normal Disorganized Not assessable

Chiari III configuration includes the following features: hypoplastic posterior fossa, vermian displacement and ‘lemon sign’ [19]. eCSF = External CSF spaces.

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ing. In none of the clinically followed cases did chro-mosomal microarray reveal positive results ( table 2 ).

In addition to conventional DWI, 2 other advanced fetal MR methods were helpful in a more detailed charac-terization of the encephalocele cases: (1) DTI-based tractography revealed the presence and po-

sition of sensorimotor tracts in 5/5 cases ( fig. 1 , 3 ). In 3/5 cases the corpus callosum could be identified by

tractography, whereas conventional sequences failed to visualize this structure unequivocally ( fig. 3 ). In 3/5 cas-es massive fronto-occipitally oriented tracts connected the displaced extracranial with the intracranial brain tis-sue ( fig. 1 , 3 ).

(2) EPI deoxyhemoglobin-sensitive sequences were the only sequences to visualize the detailed vascular anat-omy of the draining cerebral veins in 7/9 cases ( fig. 4 ).

Fig. 3. Tractography depicts anisotropic tissue characteristics (yellow) of the en-cephalocele at 22 GW and posterior distor-tion of the brainstem, which is confirmed by postnatal MRI (patient 2). Note the dys-plastic appearance of the displaced brain tissue. At the age of 4 months, postnatal follow-up showed cortical blindness and reduced reaction to pain/sensory stimuli.

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Fig. 1. Giant occipital encephalocele at 28 GW: DTI tractography displays abnormal corticocerebellar and spinal tract connectivity (green) and part of the corpus callosum (blue).

Fig. 2. Suboccipital meningocele and molar tooth sign (for further details, see tables 1 , 2 ; patient 7).

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Postnatal MRI follow-up data were available in 7/14 cases. In 1/7 cases postnatal MRI confirmed the prenatal findings (confirmation of polymicrogyria) and in 4/7 ad-ditional morphological information was added (vascular anatomy – MRI, exclusion of calcification and extent of bony defect – CCT; fig. 6 ).

Discussion

Although postnatal MRI features of meningoencepha-loceles have been systematically analyzed [12] , prenatal MRI data of these defects are limited to rare case reports [13–22] . Due to the absence of systematically assessed im-aging data, our confidence in predicting the neurological outcome in these cases is generally low. A mainly favorable outcome [23] , in contrast to a major neurological disabil-ity or death, has been reported in more than half of the cases [4] . Therefore, this retrospective study aimed to de-scribe the morphological features of occipital and parietal meningoencephaloceles using ‘standard’ fetal MR se-quences and ‘advanced’ MRI techniques (DWI, EPI and DTI sequences).

All examined cases had a bony skull defect with a vary-ing degree of brain tissue displacement in common. In contradiction to the concept that some degenerative and dysplastic changes mainly occur during postnatal devel-opment, the externalized brain tissue of all prenatally ex-amined cases displayed abnormal cortical folding (‘poly-microgyria’) patterns and/or degenerative changes such as calcification and hemorrhage ( table 2 ; fig. 2 , 4–6 ).

Despite these common features, we also observed a re-markable morphological heterogeneity. First, there was diversity in the grade of involvement of certain brain structures and laterality of the displaced anatomical brain regions. Second, the appearance of the brainstem was found to be different. Third, the shape of the skull and width of external CSF spaces was variable ( table 1 ). Fourth, the morphology of the corpus callosum was het-erogeneous amongst the included cases.

Pathological anatomical heterogeneity of this develop-mental pathology has been reported before. Obviously, the occipital lobes are found to be most frequently dis-placed, whereas the encephalocele rarely includes the pons and medulla [12] . In our series, the herniation of brainstem structures into the encephalocele sac was al-ways associated with the displacement of a major portion of the forebrain (the entire occipital lobes and parts of the temporal lobes; fig. 1 ) and thus indicated the most severe expression of the encephalocele spectrum with generally very limited viability [24] . The commonly used terms ‘gi-ant,’ ‘large’ or ‘massive’ encephalocele [25] exclusively re-fer to the size of the encephalocele sac and not to its con-tent. With regard to the prognostic assessment of these extreme cases, a larger sample size will be needed to show whether brainstem displacement rather than size is the most important marker of lethality.

Our experience supports the concept that the charac-terization of ‘atypical’ brainstem morphologies allows the classification of encephalocele cases ( fig. 2 , 5 , 6 ), espe-cially before 24 GW when associated malformations of cortical (forebrain) development have not yet fully found their morphological expression [26] . Due to the strength of fetal MRI in visualizing the brainstem and cerebellar anatomy, this imaging modality is especially helpful in accomplishing this task [21] . The brainstem was abnor-mally developed in more than one third of our patients. In cases with large herniation, the brainstem was bent posteriorly, leading to an atypical ‘kink’ between the mid-brain and the diencephalon as well as between the me-dulla and the brainstem ( fig. 1 , 3 ). This configuration has to be discriminated from the ‘kinked’ and z-shaped con-figuration of the brainstem, which was found in 1 case

Fig. 4. Parietooccipital encephalocele at 25 GW (patient 6). EPI se-quence depicts aberrant draining vein (postnatal MRI, lower row).

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Fig. 5. Patient 11 with ‘kinking’ and a molar tooth-like configuration of the midbrain at 19 GW. DWI shows diffusion-restricted brain tissue within the encephalocele (arrowheads).

Table 2. Clinical follow-up characteristics of 9 patients with encephaloceles

Patient Age at follow-up

Seizures Shunt Respiratory Other clinical features Genetics Pathology (autopsy/resected specimen)

2 4 months – – Normal Optic nerve hypoplasia, cortically blind, feeding difficulties, developmental delay

Negative CMA n.a.

3 Death at 2 days

Apnea at day 2

Postnatal agonal breathing, acrocyanosis

Negative MaterniT21 results

Autopsy refused

6 2 months + + Normal Hearing loss, hemiplegia, delayed developmental milestones

Negative CMA Oligo v9.1

Mild cortical dysplasia characterized by neuronal dropout, accentuation of the microcolumnar architecture and dyslamination

7 Death at 3 months

Respirator dependent

Panhypopituitarism, suspected Joubert-Boltshauser syndrome


Microcephaly, vermian hypoplasia, dysplastic arcuate nucleus, disorganized spinal cord, occipitocervical encephalocele, polymicrogyria, cortical microdysgenesis

9 7 years + + Normal Speaks in fragmented sentences, abnormal gait


Fairly well-organized brain tissue including a portion of hippocampal tissue, subarachnoid neuroglial heterotopia

10 7 years – + Normal Vision abnormalities, mild optic atrophy, no focal neurological findings

n.a. Well-organized neural parenchyma, leptomeningeal fibrosis and leptomeningeal glioneuronal heterotopia

11 6 months + + Frequent apneas, long-term respirator dependency

Global developmental delay, quadriplegia, persistent hyperplastic primary vitreous

Negative CMA Oligo v9.1; Walker-Warburg syndrome (whole exome sequencing)

Subcutaneous tissue with nodules of neuroglial tissue

12 2 years + + Normal Global developmental delay, retching, inconsistent tracking, no progress


Subcutaneous tissue with dense collagenous tissue containing islands and trabeculae of heterotopic neuroglial and folia of immature cerebellar tissue

14 Intrapartum fetal demise

n.a. n.a.

CMA = Chromosomal microarray; n.a. = not available.

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with genetically proven Walker-Warburg syndrome ( fig. 5 , 6 ; tables 1 , 2 ).

Moreover, 1 of our presented cases (patient 7) dis-played the characteristic molar tooth sign [26, 27] as a typical morphological feature of Joubert syndrome. The molar tooth sign consists of an abnormally deep cleft in the isthmus of the brainstem (pontomesencephalic junc-tion), thickened and reoriented superior cerebellar pe-duncles and vermian hypoplasia [27] ( fig. 2 ). The fre-quent association of occipital meningoencephaloceles with the Joubert syndrome and its related disorders, such as the Meckel-Gruber syndrome and cases of tectocere-bellar dysraphism [28] , has well been recognized by imag-ing studies [29] and genetic analyses [30] . As the Joubert and Walker-Warburg syndromes have a recurrence risk of 25% [31] , their detection is important for further pa-rental counseling.

Fetal MRI nowadays does not only provide T2-weight-ed structural information – optimized high-resolution fe-tal DWI sequences allowed the detection of small vol-umes of herniated brain tissue within an encephalocele sac. This allows the discrimination between pure menin-goceles and meningoencephaloceles ( fig. 5 , 6 ), which may be difficult by ultrasound [19] and further helps to iden-tify rare cases of atretic encephaloceles [32] .

DTI provides directional information on tissue water motion. This orientational information is used by the technique of tractography to visualize the local geometry of the examined structure in 3D. Due to the vastly altered intracranial anatomy of the forebrain in encephaloceles, the morphology of white matter tracts cannot be ade-quately assessed by conventional T2-weighted sequences. In cases of encephaloceles, DTI allowed the identification of the position of the sensory and motor tracts and the morphology of the corpus callosum in 3D ( fig. 1 , 3 ). Thus, callosal agenesis as a frequently associated pathology could be reliably excluded [33] . Moreover, DTI indirectly

visualized the brainstem in 3D and supported the 2D structural imaging data ( fig. 1 ). Our tractography results of the large ascending and descending tracts resembled previously published postnatal presurgical DTI data in a case of a large occipital encephalocele [34] . However, due to the small dimensions of brainstem white matter tracts, the resolution of prenatal DTI currently does not suffice to reliably identify their functionally important anoma-lies, as postmortem histological analysis has frequently described an absence of the pyramidal tracts in encepha-locele cases [35] .

So far, fetal MRI has been very limited in the visualiza-tion of cerebral blood vessels. However, we were able to demonstrate that the use of deoxyhemoglobin-sensitive EPI sequences [36] allowed a detailed assessment of the commonly abnormal venous vascular anatomy in 7/9 ex-amined cases ( fig. 4 ). Combined MR EPI and duplex ul-trasound may even be more efficient in the visualization of the abnormal persistence of the fetal cerebral vascula-ture/prepontine venous plexus in these conditions [35] .

Despite all of the presented potential benefits of fetal MRI, postnatal brain imaging (MRI or/and CT) was still able to add certain morphological aspects in 4/7 cases. Nonetheless, postnatal imaging revealed different results of clinical significance in only 1/7 cases ( table 1 ). Gener-ally, the imaging data provided by fetal MRI is sufficient to be used as a reliable reference for prenatal neurosurgi-cal counseling in a multidisciplinary setting.

In summary, MRI permits detailed morphological analysis of fetuses with occipital and parietal encephalo-celes, data which are valuable for determining perinatal management. Information gained from fetal MRI is al-most equivalent to postnatal scans. Advanced fetal MRI techniques can provide additional information that may be useful for postnatal surgical planning of these complex pathologies.

Fig. 6. Postnatal brain MRI of patient 11, confirming encephalocele of the occipital pole and the brainstem configuration and addition-ally showing bilateral polymicrogyria of the basal temporal lobes.

References 1 Copp AJ, Stanier P, Greene ND: Neural tube defects: recent advances, unsolved questions, and controversies. Lancet Neurol 2013; 12: 799–810.

2 Siffel C, Wong LY, Olney RS, Correa A: Sur-vival of infants diagnosed with encephalocele in Atlanta, 1979–98. Paediatr Perinat Epide-miol 2003; 17: 40–48.

3 Rowland CA, Correa A, Cragan JD, Alverson CJ: Are encephaloceles neural tube defects? Pediatrics 2006; 118: 916–923.

4 Bui CJ, Tubbs RS, Shannon CN, Acakpo-Satchivi L, Wellons JC 3rd, Blount JP, Oakes WJ: Institutional experience with cranial vault encephaloceles. J Neurosurg 2007; 107: 22–25.

Dow

nloa

ded

by:

Med

ical

Uni

vers

ity V

ienn

a -

Uni

vers

ity L

ibra

ry

149.

148.

228.

148

- 10

/30/

2014

9:5

7:46

AM



8

5 Thompson DN: Postnatal management and outcome for neural tube defects including spi-na bifida and encephalocoeles. Prenat Diagn 2009; 29: 412–419.

6 Lo BW, Kulkarni AV, Rutka JT, Jea A, Drake JM, Lamberti-Pasculli M, Dirks PB, Thabane L: Clinical predictors of developmental out-come in patients with cephaloceles. J Neuro-surg Pediatr 2008; 2: 254–257.

7 Cameron M, Moran P: Prenatal screening and diagnosis of neural tube defects. Prenat Diagn 2009; 29: 402–411.

8 Boyd PA, Wellesley DG, De Walle HE, Ten-coni R, Garcia-Minaur S, Zandwijken GR, Stoll C, Clementi M: Evaluation of the prenatal diagnosis of neural tube defects by fetal ultra-sonographic examination in different centres across Europe. J Med Screen 2000; 7: 169–174.

9 Roelens FA, Barth PG, van der Harten JJ: Sub-ependymal nodular heterotopia in patients with encephalocele. Eur J Paediatr Neurol 1999; 3: 59–63.

10 Glenn OA, Cuneo AA, Barkovich AJ, Hashe-mi Z, Bartha AI, Xu D: Malformations of cor-tical development: diagnostic accuracy of fetal MR imaging. Radiology 2012; 263: 843–855.

11 Kasprian G, Brugger PC, Weber M, Krssak M, Krampl E, Herold C, Prayer D: In utero trac-tography of fetal white matter development. Neuroimage 2008; 43: 213–224.

12 Castillo M, Quencer RM, Dominguez R: Chi-ari III malformation: imaging features. AJNR Am J Neuroradiol 1992; 13: 107–113.

13 Budorick NE, Pretorius DH, McGahan JP, Grafe MR, James HE, Slivka J: Cephalocele detection in utero: sonographic and clinical features. Ultrasound Obstet Gynecol 1995; 5: 77–85.

14 Lee R, Tai KS, Cheng PW, Lui WM, Chan FL: Chiari III malformation: antenatal MRI diag-nosis. Clin Radiol 2002; 57: 759–761.

15 Smith AB, Gupta N, Otto C, Glenn OA: Diag-nosis of Chiari III malformation by second trimester fetal MRI with postnatal MRI and CT correlation. Pediatr Radiol 2007; 37: 1035–1038.

16 Dankovcik R, Vyhnalkova V, Muranska S, Kucera E, Korpova M, Plichtova A, Miklosova M, Ferianec V, Evangelista Jirasek J, Dudas M: Encephalocystocele – uncommon diagnosis in prenatal medicine. Fetal Diagn Ther 2012; 32: 295–298.

17 Ghonge NP, Kanika SS, Poonam B: Familial occipital cephalocele in a fetus at 21 weeks’ gestation: imaging demonstration across 3 generations. J Ultrasound Med 2011; 30: 1747–1751.

18 Peruzzi P, Corbitt RJ, Raffel C: Magnetic reso-nance imaging versus ultrasonography for the in utero evaluation of central nervous system anomalies. J Neurosurg Pediatr 2010; 6: 340–345.

19 Vogel TW, Manjila S, Cohen AR: Novel neu-rodevelopmental disorder in the case of a gi-ant occipitoparietal meningoencephalocele. J Neurosurg Pediatr 2012; 10: 25–29.

20 Ramdurg SR, Gubbi S, Odugoudar A, Kadeli V: A rare case of split pons with double en-cephalocoele, dermal sinus tract, and lipom-eningomyelocele: a case report and review of literature. Childs Nerv Syst 2014; 30: 173–176.

21 Saleem SN, Zaki MS: Role of MR imaging in prenatal diagnosis of pregnancies at risk for Joubert syndrome and related cerebellar dis-orders. AJNR Am J Neuroradiol 2010; 31: 424–429.

22 Papadias A, Miller C, Martin WL, Kilby MD, Sgouros S: Comparison of prenatal and post-natal MRI findings in the evaluation of intra-uterine CNS anomalies requiring postnatal neurosurgical treatment. Childs Nerv Syst 2008; 24: 185–192.

23 Date I, Yagyu Y, Asari S, Ohmoto T: Long-term outcome in surgically treated encepha-locele. Surg Neurol 1993; 40: 125–130.

24 Shams Amiri R, Faghih Jouibari M, Nejat F, El Khashab M: Iniencephaly: Clinical, radio-logical and surgical findings. Pediatr Neuro-surg 2010; 46: 290–293.

25 Mahapatra AK: Giant encephalocele: a study of 14 patients. Pediatr Neurosurg 2011; 47: 406–411.

26 Pugash D, Oh T, Godwin K, Robinson AJ, By-rne A, Van Allen MI, Osiovich H: Sonograph-ic ‘molar tooth’ sign in the diagnosis of Jou-bert syndrome. Ultrasound Obstet Gynecol 2011; 38: 598–602.

27 Maria BL, Hoang KB, Tusa RJ, Mancuso AA, Hamed LM, Quisling RG, Hove MT, Fennell EB, Booth-Jones M, Ringdahl DM, Yachnis AT, Creel G, Frerking B: ‘Joubert syndrome’ revisited: key ocular motor signs with mag-netic resonance imaging correlation. J Child Neurol 1997; 12: 423–430.

28 Friede RL: Uncommon syndromes of cerebel-lar vermis aplasia. II. Tecto-cerebellar dys-raphia with occipital encephalocele. Dev Med Child Neurol 1978; 20: 764–772.

29 Poretti A, Singhi S, Huisman TA, Meoded A, Jallo G, Ozturk A, Boltshauser E, Tekes A: Tecto-cerebellar dysraphism with occipital encephalocele: not a distinct disorder, but part of the Joubert syndrome spectrum? Neu-ropediatrics 2011; 42: 170–174.

30 Abdelhamed ZA, Wheway G, Szymanska K, Natarajan S, Toomes C, Inglehearn C, John-son CA: Variable expressivity of ciliopathy neurological phenotypes that encompass Meckel-Gruber syndrome and Joubert syn-drome is caused by complex de-regulated cil-iogenesis, SHH and WNT signalling defects. Hum Mol Genet 2013; 22: 1358–1372.

31 Parisi MA: Clinical and molecular features of Joubert syndrome and related disorders. Am J Med Genet C Semin Med Genet 2009; 151C:326–340.

32 Yamazaki T, Enomoto T, Iguchi M, Nose T: Atretic cephalocele – report of two cases with special reference to embryology. Childs Nerv Syst 2001; 17: 674–678.

33 Kasprian G, Brugger PC, Schopf V, Mitter C, Weber M, Hainfellner JA, Prayer D: Assessing prenatal white matter connectivity in com-missural agenesis. Brain 2013; 136: 168–179.

34 Zolal A, Vachata P, Hejcl A, Malucelli A, Bar-tos R, Sames M: Identification of the large de-scending tracts using diffusion tensor imag-ing in Chiari III malformation. Childs Nerv Syst 2010; 26: 867–870.

35 Karch SB, Urich H: Occipital encephalocele: a morphological study. J Neurol Sci 1972; 15: 89–112.

36 Brugger PC, Stuhr F, Lindner C, Prayer D: Methods of fetal MR: beyond T2-weighted imaging. Eur J Radiol 2006; 57: 172–181.

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Prenatal Imaging of Occipital Encephaloceles

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