Hindbrain Herniation and Banana and Lemon Sign After Open Fetal Myelomeningocele Repair – When Do These Signs Disappear and is Shunting Predictable?

Abstract

Purpose The aim was to describe the sonographic follow-up of hindbrain herniation (HH), the banana and lemon sign after fetal myelomeningocele (fMMC) repair, and the time of disappearance of these signs after the intervention, and to investigate any predictive value for the necessity of shunting during the infant’s first year of life. Additionally, the sonographic evolution of the transcerebellar diameter (TCD) before and after fetal intervention was assessed.

Patients and Methods The first 50 patients that underwent fMMC repair at Zurich Center for Fetal Diagnosis and Therapy (www.swissfetus.ch) were included in this study. Sonographic scans performed weekly after fMMC repair focusing on HH and banana and lemon signs were analyzed and compared between the shunted and the non-shunted group. ROC curves were generated for the time intervals of resolution of the signs in order to show their predictive accuracy for the need for shunting until 1 year of age.

Results HH resolved in 48 fetuses (96 %) before delivery. The sonographic disappearance of HH within the first two weeks after fMMC repair was associated with a significantly lower incidence of shunt placement (OR 0.19; 95 % CI 0.4–0.9) during the first year of life (p = 0.03). All fetuses with persistent HH before delivery received a shunt. TCD growth was observed in all fetuses.

Conclusion The reversibility of HH within two weeks after fMMC repair is associated with an 80 % lower incidence of shunt placement during the infant’s first year of life. Moreover, it allows the cerebellum to grow and to normalize its configuration.

Zusammenfassung

Ziel Ziele dieser Studie waren, die sonografische Entwicklung der Kleinhirnherniation (KH) sowie des Bananen- und Zitronenzeichens nach fetalem Myelomeningozelen (fMMC)-Verschluss sowie das Zeitintervall bis zum Verschwinden dieser Zeichen nach der Intervention zu beschreiben und herauszufinden, ob diese Messungen zur Vorhersage der Shunt-Bedürftigkeit im ersten Lebensjahr dieser Kinder verwendet werden können. Zusätzlich wurde der transzerebelläre Durchmesser (TCD) vor und nach der Intervention sonografisch erhoben.

Patienten und Methode Die ersten 50 der am Zürcher Zentrum für Fetale Diagnostik und Therapie (www.swissfetus.ch) operierten Kinder wurden eingeschlossen. Die nach dem fMMC-Verschluss wöchentlich erfassten sonografischen Bilder wurden analysiert und zwischen der geshunteten und nicht geshunteten Gruppe verglichen. Um den Vorhersagewert der Shunt-Bedürftigkeit im ersten Lebensjahr vorherzusagen, wurden ROC-Kurven für die Zeitintervalle bis zum Verschwinden der Zeichen generiert.

Ergebnisse Die KH löste sich bei 48 der Föten (96 %) auf. Die sonografische Reversibilität der KH in den ersten 2 Wochen nach fMMC-Verschluss war mit einer signifikant tieferen Inzidenz der Shunt-Bedürftigkeit im ersten Lebensjahr vergesellschaftet (OR 0,19; 95 %-KI 0,4–0,9; p = 0,03). Alle Föten mit persistierender KH haben einen Shunt bekommen. Ein Wachstum des TCD konnte bei allen Föten beobachtet werden.

Schlussfolgerung Die Reversibilität der KH interhalb der ersten 2 Wochen nach fMMC-Verschluss geht mit einer 80 % niedrigeren Inzidenz der Shunt-Bedürftigkeit im ersten Lebensjahr dieser Kinder einher. Zudem erlaubt sie die Normalisierung des Kleinhirnwachstums und dessen Konfiguration.

Key words

myelomeningozele - fetal surgery - hindbrain herniation - banana sign - lemon sign

• References

• 1 Meuli M, Meuli-Simmen C, Hutchins GM. et al. In utero surgery rescues neurological function at birth in sheep with spina bifida. Nat Med 1995; 1: 342-347
• 2 McLone DG, Knepper PA. The cause of Chiari II malformation: a unified theory. Pediatr Neurosci 1989; 15: 1-12
• 3 Bell WO, Charney EB, Bruce DA. et al. Symptomatic Arnold-Chiari malformation: review of experience with 22 cases. J Neurosurg 1987; 66: 812-816
• 4 Charney EB, Rorke LB, Sutton LN. et al. Management of Chiari II complications in infants with myelomeningocele. J Pediatr 1987; 111: 364-371
• 5 Bruner JP, Tulipan N, Paschall RL. et al. Fetal surgery for myelomeningocele and the incidence of shunt-dependent hydrocephalus. JAMA 1999; 282: 1819-1825
• 6 Danzer E, Johnson MP, Wilson RD. et al. Fetal head biometry following in-utero repair of myelomeningocele. Ultrasound Obstet Gynecol 2004; 24: 606-611
• 7 Sutton LN, Adzick NS, Bilaniuk LT. et al. Improvement in hindbrain herniation demonstrated by serial fetal magnetic resonance imaging following fetal surgery for myelomeningocele. JAMA 1999; 282: 1826-1831
• 8 Meuli M, Ochsenbein N, Mazzone L. et al Benchmarking the “MOMS-Trial”: Zurich Results of Open Fetal Surgery for Spina Bifida. fetal Diagn Ther 2020; 47: 91-97 . doi:10.1159/000500049
• 9 Adzick NS, Thom EA, Spong CY. et al. A randomized trial of prenatal versus postnatal repair of myelomeningocele. N Engl J Med 2011; 364: 993-1004
• 10 Johnson MP, Sutton LN, Rintoul N. et al. Fetal myelomeningocele repair: short-term clinical outcomes. Am J Obstet Gynecol 2003; 189: 482-487
• 11 Danzer E, Finkel RS, Rintoul NE. et al. Reversal of hindbrain herniation after maternal-fetal surgery for myelomeningocele subsequently impacts on brain stem function. Neuropediatrics 2008; 39: 359-362
• 12 Ochsenbein-Kolble N, Krahenmann F, Husler M. et al Tocolysis for in utero Surgery: Atosiban Performs Distinctly Better than Magnesium Sulfate. Fetal Diagn Ther 2018; 44: 59-64 . doi:10.1159/000478261
• 13 Kahr MK, Winder F, Vonzun L. et al Risk Factors for Preterm Birth following Open Fetal Myelomeningocele Repair: Results from a Prospective Cohort. Fetal Diagn Ther 2020; 47: 15-23 . doi:10.1159/000500048:1-9
• 14 Winder FM, Vonzun L, Meuli M. et al Maternal Complications following Open Fetal Myelomeningocele Repair at the Zurich Center for Fetal Diagnosis and Therapy. Fetal Diagn Ther 2019; 46: 153-158 . doi:10.1159/000494024:1-6
• 15 Vonzun L, Winder FM, Meuli M. et al. Prenatal Sonographic Head Circumference and Cerebral Ventricle Width Measurements Before and After Open Fetal Myelomeningocele Repair – Prediction of Shunting During the First Year of Life. Ultraschall in Med, published online 2018;
• 16 Meuli M, Meuli-Simmen C, Mazzone L. et al In utero Plastic Surgery in Zurich: Successful Use of Distally Pedicled Random Pattern Transposition Flaps for Definitive Skin Closure during Open Fetal Spina Bifida Repair. Fetal Diagn Ther 2018; 44: 173-178 . doi:10.1159/000479926
• 17 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
• 18 Rethmann C, Scheer I, Meuli M. et al. Evolution of posterior fossa and brain morphology after in utero repair of open neural tube defects assessed by MRI. Eur Radiol 2017; 27: 4571-4580
• 19 Nagaraj UD, Bierbrauer KS, Zhang B. et al. Hindbrain Herniation in Chiari II Malformation on Fetal and Postnatal MRI. AJNR Am J Neuroradiol 2017; 38: 1031-1036
• 20 Rethmann C, Scheer I, Meuli M. et al. Evolution of posterior fossa and brain morphology after in utero repair of open neural tube defects assessed by MRI. Eur Radiol 2017; 27: 4571-4580
• 21 Zarutskie A, Guimaraes C, Yepez M. et al. Prenatal brain imaging for predicting need for postnatal hydrocephalus treatment in fetuses that had neural tube defect repair in utero. Ultrasound Obstet Gynecol 2019; 53: 324-334
• 22 Tulipan N, Wellons 3rd JC, Thom EA. et al. Prenatal surgery for myelomeningocele and the need for cerebrospinal fluid shunt placement. J Neurosurg Pediatr 2015; 16: 613-620
• 23 Danzer E, Johnson MP, Bebbington M. et al. Fetal head biometry assessed by fetal magnetic resonance imaging following in utero myelomeningocele repair. Fetal Diagn Ther 2007; 22: 1-6
• 24 Grant RA, Heuer GG, Carrion GM. et al. Morphometric analysis of posterior fossa after in utero myelomeningocele repair. J Neurosurg Pediatr 2011; 7: 362-368