Fetal Endoscopic Third Ventriculostomy Is Technically Feasible in Prenatally Induced Hydrocephalus Ovine Model.


Journal

Neurosurgery
ISSN: 1524-4040
Titre abrégé: Neurosurgery
Pays: United States
ID NLM: 7802914

Informations de publication

Date de publication:
01 06 2023
Historique:
received: 19 08 2022
accepted: 11 11 2022
pmc-release: 10 02 2024
medline: 17 5 2023
pubmed: 11 2 2023
entrez: 10 2 2023
Statut: ppublish

Résumé

Congenital obstructive hydrocephalus generates progressive irreversible fetal brain damage by ventricular enlargement and incremental brain tissue compression that leads to maldevelopment and poor clinical outcomes. Intrauterine treatments such as ventriculo-amniotic shunting have been unsuccessfully tried in the eighties. To assess if prenatal endoscopic third ventriculostomy (ETV) is feasible in a large animal model and optimize this technique for ventricular decompression and potential arrest of fetal brain damage in fetal lambs. We generated hydrocephalus in 50 fetal lambs by injecting a polymeric agent into the cisterna magna at midgestation (E85). Subsequently, 3 weeks later (E105), fetal ETV was performed using a small rigid fetoscope. The endoscopy entry point was located anterior to the coronal suture, 7 mm from the midline. We obtained clear visualization of the enlarged lateral ventricles by endoscopy in the hydrocephalic fetal lambs. The floor of the third ventricle was bluntly perforated and passed with the scope for a successful ETV. Total success was achieved in 32/50 cases (64%). Causes of failure were blurred vision or third ventricle obliteration by BioGlue in 10/50 (20%) cases, anatomic misdirection of the endoscope in 5 (10%) cases, 2 cases of very narrow foramen of Monro, and 1 case of choroid plexus bleeding. If we exclude the cases artificially blocked by the polymer, we had a successful performance of prenatal-ETV in 80% (32/40) of hydrocephalic fetuses. Despite the inherent difficulties arising from ovine brain anatomy, this study shows that innovative fetal ETV is technically feasible in hydrocephalic fetal lambs.

Sections du résumé

BACKGROUND
Congenital obstructive hydrocephalus generates progressive irreversible fetal brain damage by ventricular enlargement and incremental brain tissue compression that leads to maldevelopment and poor clinical outcomes. Intrauterine treatments such as ventriculo-amniotic shunting have been unsuccessfully tried in the eighties.
OBJECTIVE
To assess if prenatal endoscopic third ventriculostomy (ETV) is feasible in a large animal model and optimize this technique for ventricular decompression and potential arrest of fetal brain damage in fetal lambs.
METHODS
We generated hydrocephalus in 50 fetal lambs by injecting a polymeric agent into the cisterna magna at midgestation (E85). Subsequently, 3 weeks later (E105), fetal ETV was performed using a small rigid fetoscope. The endoscopy entry point was located anterior to the coronal suture, 7 mm from the midline.
RESULTS
We obtained clear visualization of the enlarged lateral ventricles by endoscopy in the hydrocephalic fetal lambs. The floor of the third ventricle was bluntly perforated and passed with the scope for a successful ETV. Total success was achieved in 32/50 cases (64%). Causes of failure were blurred vision or third ventricle obliteration by BioGlue in 10/50 (20%) cases, anatomic misdirection of the endoscope in 5 (10%) cases, 2 cases of very narrow foramen of Monro, and 1 case of choroid plexus bleeding. If we exclude the cases artificially blocked by the polymer, we had a successful performance of prenatal-ETV in 80% (32/40) of hydrocephalic fetuses.
CONCLUSION
Despite the inherent difficulties arising from ovine brain anatomy, this study shows that innovative fetal ETV is technically feasible in hydrocephalic fetal lambs.

Identifiants

pubmed: 36762899
doi: 10.1227/neu.0000000000002361
pii: 00006123-202306000-00024
pmc: PMC10508554
doi:

Types de publication

Clinical Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1303-1311

Informations de copyright

Copyright © 2023 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the Congress of Neurological Surgeons.

Références

Rekate H. Hydrocephalus in children. In: Winn HR, Youmans JR, eds. Youmans Neurological Surgery. Sanders; 2003:3387-3404.
Laurence KM, Coates S. The natural history of hydrocephalus. Detailed analysis of 182 unoperated cases. Arch Dis Child. 1962;37(194):345-362.
Cinalli G, Spennato P, Nastro A, et al. Hydrocephalus in aqueductal stenosis. Childs Nerv Syst. 2011;27(10):1621-1642.
Kandasamy J, Jenkinson MD, Mallucci CL. Contemporary management and recent advances in paediatric hydrocephalus. BMJ. 2011;343(7815):d4191.
Varela MF, Miyabe MM, Oria M. Fetal brain damage in congenital hydrocephalus. Childs Nerv Syst. 2020;36(8):1661-1668.
McAllister JP II, Chovan P. Neonatal hydrocephalus. Mechanisms and consequences. Neurosurg Clin N Am. 1998;9(1):73-93.
Birnholz JC, Frigoletto FD. Antenatal treatment of hydrocephalus. N Engl J Med. 1981;304(17):1021-1023.
Frigoletto FD, Birnholz JC, Greene NF. Antenatal treatment of hydrocephalus by ventriculoamniotic shunting. JAMA. 1982;248(19):2496-2497.
Clewell WH, Johnson ML, Meier PR, et al. A surgical approach to the treatment of fetal hydrocephalus. N Engl J Med. 1982;306(22):1320-1325.
Clewell WH, Manco-Johnson ML, Manchester DK. Diagnosis and management of fetal hydrocephalus. Clin Obstet Gynecol. 1986;29(3):514-522.
Glick PL, Harrison MR, Nakayama DK, et al. Management of ventriculomegaly in the fetus. J Pediatr. 1984;105(1):97-105.
Glick PL, Harrison MR, Halks-Miller M, et al. Correction of congenital hydrocephalus in utero. II. Efficacy of in utero shunting. J Pediatr Surg. 1984;19(6):870-881.
Peiro JL, Fabbro MD. Fetal therapy for congenital hydrocephalus—where we came from and where we are going. Childs Nerv Syst. 2020;36(8):1697-1712.
Duru S, Peiro JL, Oria M, et al. Successful endoscopic third ventriculostomy in children depends on age and etiology of hydrocephalus: outcome analysis in 51 pediatric patients. Childs Nerv Syst. 2018;34(8):1521-1528.
Von Koch CS, Gupta N, Sutton LN, Sun PP. In utero surgery for hydrocephalus. Childs Nerv Syst. 2003;19(7-8):574-586.
Oria M, Duru S, Scorletti F, et al. A novel model employing fetal intracisternal BioGlue injection recapitulates obstructive congenital hydrocephalus without additional chemical-induced neuroinflammation. J Neurosurg Pediatr. 2019;(24):1-11.
Di Rocco C, Pettorossi VE, Caldarelli M, et al. Communicating hydrocephalus induced by mechanically increased amplitude of the intraventricular cerebrospinal fluid pressure: experimental studies. Exp Neurol. 1978;59(1):40-52.
Nakayama DK, Harrison MR, Berger MS, Chinn DH, Halks-Miller M, Edwards MS. Correction of congenital hydrocephalus in utero. I. The model: intracisternal kaolin produces hydrocephalus in fetal lambs and rhesus monkeys. J Pediatr Surg. 1983;18(4):331-338.
Michejda M, Hodgen GD. In utero diagnosis and treatment of non-human primate fetal skeletal anomalies. JAMA. 1981;246(10):1093-1097.
Michejda M. Neurobehavioral development of in utero treated hydrocephalic monkeys. Z Kinderchir. 1989;44(suppl 1):52.
Michejda M, Bayne K, Schneider M, Suomi S. Functional and structural recovery of the brain in in utero treated hydrocephalic monkeys: follow-up of neurobehavioral development. Contrib Gynecol Obstet. 1991;18:157-176.
Cambria S, Gambardella G, Cardia E, Cambria M. Experimental endouterine hydrocephalus in foetal sheep and surgical treatment by ventriculo-amniotic shunt. Acta Neurochir (Wien). 1984;72(3-4):235-240.
Garzetti GG, Rosati P, Angelozzi P, Exacoustos C, Mancuso S. Proposal of an experimental model of fetal hydrocephalus. J Neurosurg Sci. 1988;32(3):93-97.
De Keersmaecker B, Vloeberghs M, Ville Y. Fetal hydrocephalus and intrauterine cerebral ventriculoscopy: an animal model. Fetal Diagn Ther. 2005;20(5):445-449.
Warf BC. Comparison of endoscopic third ventriculostomy alone and combined with choroid plexus cauterization in infants younger than 1 year of age: a prospective study in 550 African children. J Neurosurg. 2005;103(6 suppl):475-481.
Kulkarni AV, Riva-Cambrin J, Browd SR, et al. Endoscopic third ventriculostomy and choroid plexus cauterization in infants with hydrocephalus: a retrospective Hydrocephalus Clinical Research Network study. J Neurosurg Pediatr. 2014;14(3):224-229.
Kulkarni AV, Riva-Cambrin J, Rozzelle CJ, et al. Endoscopic third ventriculostomy and choroid plexus cauterization in infant hydrocephalus: a prospective study by the Hydrocephalus Clinical Research Network. J Neurosurg Pediatr. 2018;21(3):214-223.
Li D, Ravindra VM, Lam SK. Rigid versus flexible neuroendoscopy: a systematic review and meta-analysis of endoscopic third ventriculostomy for the management of pediatric hydrocephalus. J Neurosurg Pediatr. 2021;28(4):439-449.

Auteurs

Jose L Peiro (JL)

Center for Fetal and Placental Research, Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center (CCHMC), Cincinnati, Ohio, USA.
University of Cincinnati, College of Medicine, Cincinnati, Ohio, USA.

Soner Duru (S)

Center for Fetal and Placental Research, Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center (CCHMC), Cincinnati, Ohio, USA.

Blanca Fernandez-Tome (B)

Jesus Uson Minimally Invasive Surgery Centre (JUMISC), Caceres, Spain.

Lucas Peiro (L)

Center for Fetal and Placental Research, Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center (CCHMC), Cincinnati, Ohio, USA.
University of Cincinnati, College of Medicine, Cincinnati, Ohio, USA.

Jose L Encinas (JL)

Department of Pediatric Surgery, Hospital La Paz, Madrid, Spain.

Francisco M Sanchez-Margallo (FM)

Jesus Uson Minimally Invasive Surgery Centre (JUMISC), Caceres, Spain.

Marc Oria (M)

Center for Fetal and Placental Research, Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center (CCHMC), Cincinnati, Ohio, USA.
University of Cincinnati, College of Medicine, Cincinnati, Ohio, USA.

Articles similaires

1.00
Humans Yoga Low Back Pain Female Male
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH