The Fetal Posterior Fossa on Prenatal Ultrasound Imaging: Normal Longitudinal Development and Posterior Fossa Anomalies

Abstract

Fetal neurosonography and the assessment of the posterior fossa have gained in importance during the last 2 decades primarily due to the development of high-resolution ultrasound probes and the introduction of 3 D sonography. The anatomical development of the posterior fossa can be visualized well with the newest ultrasound technologies. This allows better knowledge of the anatomical structures and helps with understanding of the development of malformations of the posterior fossa. In this article the longitudinal development of the posterior fossa structures will be reviewed. The embryologic description will be compared with ultrasound descriptions. These embryologic and anatomic illustrations form the basis for the screening and diagnosis of malformations of the posterior fossa. During the first trimester, screening for open spina bifida as well as cystic malformations of the posterior fossa is possible. In the second and third trimester, malformations of the posterior fossa can be subdivided into 3 groups: fluid accumulation in the posterior fossa (Dandy-Walker malformation, Blake’s pouch cyst, mega cisterna magna, arachnoid cyst, vermian hypoplasia), decreased cerebellar biometrics (volume) (cerebellar hypoplasia, pontocerebellar hypoplasia) and suspicious cerebellar anatomy (Arnold-Chiari malformation, rhombencephalosynapsis, Joubert syndrome). This algorithm, in combination with knowledge of normal development, facilitates the diagnostic workup of malformations of the posterior fossa.

Zusammenfassung

Die fetale Neurosonografie und damit auch die sonografische Beurteilung der Strukturen der Fossa posterior haben in den letzten beiden Jahrzehnten durch den Einsatz hochauflösender Ultraschallsonden und des 3D-Ultraschalls eine besondere Bedeutung erlangt. Durch die neuen Ultraschalltechnologien kann die embryologische Entwicklung der Fossa-posterior-Strukturen nachvollzogen werden. Dies erleichtert die Kenntnis der anatomischen Strukturen und trägt zum Verständnis für die Entstehung von Fehlbildungen der Fossa posterior bei. In der folgenden Übersichtsarbeit wird die longitudinale Entwicklung der Fossa-posterior-Strukturen dargestellt. Dabei wird die embryologische Beschreibung mit der Darstellung im Ultraschall verglichen. Dieses embryologische und anatomische Wissen bildet die Grundlage für das Screening und die Diagnose von Veränderungen und Fehlbildungen der Fossa posterior. Im Ersttrimester ist ein Screening für Spina bifida aperta und zystische Fehlbildungen der Fossa posterior möglich. Im 2. und 3. Trimester können die Fehlbildungen der Fossa posterior in 3 Kategorien unterteilt werden: Fehlbildungen mit vermehrter Flüssigkeit in der Fossa posterior (Dandy-Walker-Malformation, Blakes-pouch-Zyste, Megacisterna magna, Arachnoidalzyste, Vermishypoplasie), Fehlbildungen mit verminderter Biometrie bzw. vermindertem Volumen bei „überwiegend“ normaler Anatomie des Zerebellums (zerebelläre Hypoplasie, pontozerebelläre Hypoplasie) und Fehlbildungen mit strukturell verändertem Zerebellum (Arnold-Chiari-Malformation, Rhombenzephalosynapsis, Joubert-Syndrom). Dieser Algorithmus und das Verständnis der normalen Entwicklung ermöglichen ein systematisches Aufarbeiten der Fehlbildungen der Fossa posterior.

• References

• 1 Stiles J, Jernigan TL. The Basics of Brain Development. Neuropsychol Rev 2010; 20: 327-348
• 2 Moore K, Persaud TVN, Torchia MG. et al. Embryologie: Entwicklungsstadien – Frühentwicklung – Organogenese – Klinik – mit Zugang zum Elsevier-Portal. 6th. ed. München: Urban & Fischer Verlag/Elsevier GmbH; 2013
• 3 Robinson AJ. Inferior vermian hypoplasia – Preconception, misconception. In: Ultrasound in Obstetrics and Gynecology 2014; 43: 123-136
• 4 Paladini D, Quarantelli M, Pastore G. et al. Abnormal or delayed development of the posterior membranous area of the brain: Anatomy, ultrasound diagnosis, natural history and outcome of Blake’s pouch cyst in the fetus. Ultrasound Obstet Gynecol 2012; 39: 279-287
• 5 Blaas HGK, Eik-Nes SH. Sonoembryology and early prenatal diagnosis of neural anomalies. Prenat Diagn 2009; 29: 312-325
• 6 Altmann R, Scharnreitner I, Scheier T. et al. Sonoembryology of the fetal posterior fossa at 11 + 3 to 13 + 6 gestational weeks on three-dimensional transvaginal ultrasound. Prenat Diagn 2016; 36: 731-737
• 7 Chaoui R, Benoit B, Mitkowska-Wozniak H. et al. Assessment of intracranial translucency (IT) in the detection of spina bifida at the 11–13-week scan. Ultrasound Obstet Gynecol 2009; 34: 249-252
• 8 Hirsch MC. Glossar der Neuroanatomie. Springer-Verlag; 2013
• 9 Liu F, Zhang Z, Lin X. et al. Development of the human fetal cerebellum in the second trimester: a post mortem magnetic resonance imaging evaluation. J Anat 2011; 219: 582-588
• 10 Kapur RP, Mahony BS, Finch L. et al. Normal and abnormal anatomy of the cerebellar vermis in midgestational human fetuses. Birth Defects Res Part A Clin Mol Teratol 2009; 85: 700-709
• 11 Loeser JD, Lemire RJ, Alvord EC. The development of the folia in the human cerebellar vermis. Anat Rec 1972; 173: 109-113
• 12 Barkovich AJ, Millen KJ, Dobyns WB. A developmental and genetic classification for midbrain-hindbrain malformations. Brain 2009; 132: 3199-3230
• 13 Karl K, Kainer F, Heling KS. et al. Fetal neurosonography: extended examination of the CNS in the fetus. Ultraschall in Med 2011; 32: 342-361
• 14 Vinals F, Munoz M, Naveas R. et al. The fetal cerebellar vermis: anatomy and biometric assessment using volume contrast imaging in the C-plane (VCI-C). Ultrasound Obstet Gynecol 2005; 26: 622-627
• 15 Zalel Y, Yagel S, Achiron R. et al. Three-dimensional ultrasonography of the fetal vermis at 18 to 26 weeks’ gestation: time of appearance of the primary fissure. J Ultrasound Med 2009; 28: 1-8
• 16 Verburg BO, Steegers EAP, de Ridder M. et al. New charts for ultrasound dating of pregnancy and assessment of fetal growth: Longitudinal data from a population-based cohort study. Ultrasound Obstet Gynecol 2008; 31: 388-396
• 17 Goldstein I, Reece EA, Pilu G. et al. Cerebellar measurements with ultrasonography in the evaluation of fetal growth and development. Am J Obstet Gynecol 1987; 156: 1065-1069
• 18 Hill LM, Guzick D, Rivello D. et al. The transverse cerebellar diameter cannot be used to assess gestational age in the small for gestational age fetus. Obstet Gynecol 1990; 75: 329-333
• 19 Snijders RJM, de Courcy-Wheeler RHB, Nicolaides KH. Intrauterine growth retardation and fetal transverse cerebellar diameter. Prenat Diagn 1994; 14: 1101-1105
• 20 Chavez MR, Ananth CV, Smulian JC. et al. Fetal transcerebellar diameter measurement with particular emphasis in the third trimester: A reliable predictor of gestational age. Am J Obstet Gynecol 2004; 191: 979-984
• 21 Takano M, Hirata H, Kagawa Y. et al. Ratio of fetal anteroposterior to transverse cerebellar diameter for detection of the cerebellar hypoplasia in the second trimester and comparison with trisomy 18. J Obstet Gynaecol Res 2015; 41: 1757-1761
• 22 Sherer DM, Sokolovski M, Dalloul M. et al. Nomograms of the axial fetal cerebellar hemisphere circumference and area throughout gestation. Ultrasound Obstet Gynecol 2007; 29: 32-37
• 23 Cignini P, Giorlandino M, Brutti P. et al. Reference charts for fetal cerebellar vermis height: A prospective cross-sectional study of 10605 fetuses. PLoS One 2016; 11: e0147528
• 24 Katorza E, Bertucci E, Perlman S. et al. Development of the fetal vermis: New biometry reference data and comparison of 3 diagnostic modalities-3d ultrasound, 2d ultrasound, and mr imaging. Am J Neuroradiol 2016; 37: 1359-1366
• 25 Ghi T, Contro E, de Musso F. et al. Normal morphometry of fetal posterior fossa at midtrimester: Brainstem-tentorium angle and brainstem-vermis angle. Prenat Diagn 2012; 32: 440-443
• 26 Volpe P, Contro E, de Musso F. et al. Brainstem-vermis and brainstem-tentorium angles allow accurate categorization of fetal upward rotation of cerebellar vermis. Ultrasound Obstet Gynecol 2012; 39: 632-635
• 27 Spinelli M, die Meglio L, Mosimann B. et al. The Vermian-Crest Angle: A New Method to Assess Fetal Vermis Position within the Posterior Fossa Using 3-Dimensional Multiplanar Sonography. Fetal Diagn Ther 2018;
• 28 Leibovitz Z, Shkolnik C, Haratz KK. et al. Assessment of fetal midbrain and hindbrain in mid-sagittal cranial plane by three-dimensional multiplanar sonography. Part 1: Comparison of new and established nomograms. Ultrasound Obstet Gynecol 2014; 44: 575-580
• 29 Ginath S, Lerman-Sagie T, Haratz KK. et al. The Fetal vermis, pons and brainstem: Normal longitudinal development as shown by dedicated neurosonography. J Matern Neonatal Med 2013; 26: 757-762
• 30 Haratz KK, Shulevitz SL, Leibovitz Z. et al. The fourth ventricle index – a sonographic marker for severe fetal vermian dysgenesis/agenesis. Ultrasound Obstet Gynecol 2019; 53: 390-395
• 31 Guibaud L, des Portes V. Plea for an anatomical approach to abnormalities of the posterior fossa in prenatal diagnosis. Ultrasound Obstet Gynecol 2006; 27: 477-481
• 32 Mahony BS, Callen PW, Filly RA. et al. The fetal cisterna magna. Radiology United States 1984; 153: 773-776
• 33 Brown RN. Reassessment of the normal fetal cisterna magna during gestation and an alternative approach to the definition of cisterna magna dilatation. Fetal Diagn Ther 2013; 34: 44-49
• 34 Passos AP, Araujo E, Bruns RF. et al. Reference ranges of fetal cisterna magna length and area measurements by 3-dimensional ultrasonography using the multiplanar mode. J Child Neurol 2015; 30: 209-215
• 35 Araujo Júnior E, Passos AP, Bruns RF. et al. Reference range of fetal cisterna magna volume by three-dimensional ultrasonography using the VOCAL method. J Matern Neonatal Med 2014; 27: 1023-1028
• 36 Lachmann R, Chaoui R, Moratalla J. et al. Posterior brain in fetuses with open spina bifida at 11 to 13 weeks. Prenat Diagn 2011; 31: 103-106
• 37 Chen FCK, Gerhardt J, Entezami M. et al. Detection of Spina Bifida by First Trimester Screening – Results of the Prospective Multicenter Berlin IT-Study. Ultraschall in Med 2017; 38: 151-157
• 38 Garcia-Posada R, Eixarch E, Sanz M. et al. Cisterna magna width at 11–13 weeks in the detection of posterior fossa anomalies. Ultrasound Obstet Gynecol 2013; 41: 515-520
• 39 Kavalakis I, Souka AP, Pilalis A. et al. Assessment of the posterior brain at 11–14 weeks for the prediction of open neural tube defects. Prenat Diagn 2012; 32: 1143-1146
• 40 Mangione R, Dhombres F, Lelong N. et al. Screening for fetal spina bifida at the 11–13-week scan using three anatomical features of the posterior brain. Ultrasound Obstet Gynecol 2013; 42: 416-420
• 41 Scheier M, Lachmann R, Petros M. et al. Three-dimensional sonography of the posterior fossa in fetuses with open spina bifida at 11–13 weeks’ gestation. Ultrasound Obstet Gynecol 2011; 38: 625-629
• 42 Finn M, Sutton D, Atkinson S. et al. The aqueduct of Sylvius: a sonographic landmark for neural tube defects in the first trimester. Ultrasound Obstet Gynecol 2011; 38: 640-645
• 43 Bornstein E, Goncalves Rodriguez JL, Alvarez Pavon EC. et al. First-trimester sonographic findings associated with a Dandy-Walker malformation and inferior vermian hypoplasia. J Ultrasound Med 2013; 32: 1863-1868
• 44 Volpe P, Contro E, Fanelli T. et al. Appearance of fetal posterior fossa at 11–14 weeks in fetuses with Dandy-Walker malformation or chromosomal anomalies. Ultrasound Obstet Gynecol 2016; 47: 720-725
• 45 Contro E, Volpe P, de Musso F. et al. Open fourth ventricle prior to 20 weeks’ gestation: A benign finding?. Ultrasound Obstet Gynecol 2014; 43: 154-158
• 46 Pertl B, Karpf E, Juch H. et al. A case of a transient enlargement of the intracranial translucency. In: Prenatal Diagnosis 2012; 32: 1324-1325
• 47 Hoopmann M, Kagan KO. The Fetal Profile – More Than Just NT. Ultraschall in Med 2017; 38: 611-618
• 48 Martinez-Ten P, Illescas T, Adiego B. et al. Non-visualization of choroid plexus of fourth ventricle as first-trimester predictor of posterior fossa anomalies and chromosomal defects. Ultrasound Obstet Gynecol 2018; 51: 199-207
• 49 Garel C, Fallet-Bianco C, Guibaud L. The fetal cerebellum: development and common malformations. J Child Neurol 2011; 26: 1483-1492
• 50 Lerman-Sagie T, Prayer D, Stocklein S. et al. Fetal cerebellar disorders. Handb Clin Neurol Netherlands 2018; 155: 3-23
• 51 Malinger G, Lev D, Lerman-Sagie T. The fetal cerebellum. Pitfalls in diagnosis and management. Prenat Diagn 2009; 29: 372-380
• 52 Prayer D, Malinger G, Brugger PC. et al. ISUOG Practice Guidelines: performance of fetal magnetic resonance imaging. Ultrasound Obstet Gynecol 2017; 49: 671-680
• 53 Poretti A, Boltshauser E, Huisman TAGM. Pre- and Postnatal Neuroimaging of Congenital Cerebellar Abnormalities. Cerebellum 2016; 15: 5-9
• 54 D’Antonio F, Khalil A, Garel C. et al. Systematic review and meta-analysis of isolated posterior fossa malformations on prenatal imaging (part 2): neurodevelopmental outcome. Ultrasound Obstet Gynecol 2016; 48: 28-37
• 55 Lei T, Feng JL, Xie YJ. et al. Chromosomal aneuploidies and copy number variations in posterior fossa abnormalities diagnosed by prenatal ultrasonography. Prenat Diagn 2017; 37: 1160-1168
• 56 Zou Z, Huang L, Lin S. et al. Prenatal diagnosis of posterior fossa anomalies: Additional value of chromosomal microarray analysis in fetuses with cerebellar hypoplasia. Prenat Diagn 2018; 38: 91-98
• 57 Gandolfi Colleoni G, Contro E, Carletti A. et al. Prenatal diagnosis and outcome of fetal posterior fossa fluid collections. Ultrasound Obstet Gynecol 2012; 39: 625-631
• 58 Takeshige N, Eto T, Nakashima S. et al. Rare case of a rapidly enlarging symptomatic arachnoid cyst of the posterior fossa in an infant: A case report and review of the literature. In: Surgical neurology international. India 2018
• 59 Qin X, Wang Y, Xu S. et al. Familial arachnoid cysts: a review of 35 families. Childs Nerv Syst 2019; 35: 607-612
• 60 Pinchefsky EF, Accogli A, Shevell MI. et al. Developmental outcomes in children with congenital cerebellar malformations. Dev Med Child Neurol 2019; 61: 350-358
• 61 Rudnik-Schoneborn S, Barth PG, Zerres K. Pontocerebellar hypoplasia. Am J Med Genet C Semin Med Genet 2014; 166C: 173-183
• 62 van Dijk T, Baas F, Barth PG. et al. What’s new in pontocerebellar hypoplasia? An update on genes and subtypes. Orphanet J Rare Dis 2018; 13: 92
• 63 van den Hof MC, Nicolaides KH, Campbell J. et al. Evaluation of the lemon and banana signs in one hundred thirty fetuses with open spina bifida. Am J Obstet Gynecol 1990; 162: 322-327
• 64 Bahlmann F, Reinhard I, Schramm T. et al. Cranial and cerebral signs in the diagnosis of spina bifida between 18 and 22 weeks of gestation: a German multicentre study. Prenat Diagn 2015; 35: 228-235
• 65 Kennedy D, Chitayat D, Winsor EJ. et al. Prenatally diagnosed neural tube defects: ultrasound, chromosome, and autopsy or postnatal findings in 212 cases. Am J Med Genet 1998; 77: 317-321
• 66 Ishak GE, Dempsey JC, Shaw DWW. et al. Rhombenzephalosynapsis: a hindbrain malformation associated with incomplete separation of midbrain and forebrain, hydrocephalus and a broad spectrum of severity. Brain 2012; 135: 1370-1386
• 67 Aldinger KA, Dempsey JC, Tully HM. et al. Rhombencephalosynapsis: Fused cerebellum, confused geneticists. Am J Med Genet C Semin Med Genet 2018; 178: 432-439
• 68 Parisi M, Glass I. Joubert Syndrome. In: Adam MP, Ardinger HH, Pagon RA. et al. (Eds.). Seattle (WA). 1993