Anomalies of Midbrain/Hindbrain Development and Related Disabilities: Pontocerebellar Hypoplasia, Congenital Disorders of Glycosylation, and Cerebellar Hemisphere Hypoplasia

Alessandro Gulino; Federica Dierna; Antonio Zanghì; Michele Vecchio; Stefania Salafia; Francesco Marino; Pietro Foti; Giuseppe Belfiore; Antonio Basile; Martino Ruggieri; Agata Polizzi

doi:10.1055/s-0044-1786782

Journal of Pediatric Neurology, Inhaltsverzeichnis

Journal of Pediatric Neurology 2024; 22(05): 396-406
DOI: 10.1055/s-0044-1786782

Review Article

Anomalies of Midbrain/Hindbrain Development and Related Disabilities: Pontocerebellar Hypoplasia, Congenital Disorders of Glycosylation, and Cerebellar Hemisphere Hypoplasia

Alessandro Gulino^*

¹Pediatrics Postgraduate Residency Program, University of Catania, Catania, Italy

,

Federica Dierna^*

¹Pediatrics Postgraduate Residency Program, University of Catania, Catania, Italy

,

Antonio Zanghì^*

²Department of Medical and Surgical Sciences and Advanced Technologies, Research Center for Surgery of Complex Malformation Syndromes of Transition and Adulthood, University of Catania, Catania, Italy

,

Michele Vecchio

³Department of Biomedical and Biotechnological Sciences, Rehabilitation Unit, University of Catania, Catania, Italy

,

Stefania Salafia

⁴Unit of Pediatrics, Lentini Hospital, Lentini, Italy

,

Francesco Marino

⁵Department of Medical Surgical Sciences and Advanced Technologies, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy

,

Pietro Foti

⁶Department of Medical Surgical Sciences and Advanced Technologies, Unit of Radiology 1, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy

,

Giuseppe Belfiore

⁶Department of Medical Surgical Sciences and Advanced Technologies, Unit of Radiology 1, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy

,

Antonio Basile

⁶Department of Medical Surgical Sciences and Advanced Technologies, Unit of Radiology 1, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy

,

Martino Ruggieri

⁷Department of Clinical and Experimental Medicine, Unit of Clinical Pediatrics, University of Catania, Catania, Italy

,

Agata Polizzi

⁸Chair of Pediatrics, Department of Educational Sciences, Chair of Pediatrics, University of Catania, Catania, Italy

› Institutsangaben

Abstract

Recent progress in developmental biology, molecular genetics, and neuroimaging has enabled a more profound comprehension of developmental disorders affecting the embryonic midbrain and hindbrain, which manifest clinically. The purpose of this review is to describe anomalies of the midbrain/hindbrain such as pontocerebellar hypoplasia (PCH), congenital disorders of glycosylation (CDG), cerebellar hemisphere hypoplasia. PCH is a group of disorders that is both clinically and genetically diverse. These disorders are identified by the hypoplasia and degeneration of the cerebellum and ventral pons. A total of 18 distinct clinical subtypes of PCH, each linked to pathogenic variants in 19 different genes, have been documented, like mutations in TSEN54 (coding a subunit of tRNA splicing endonucleases complex) and TBC1D23 which display moderate-to-severe intellectual disability (ID) and microcephaly. CDG represent a set of inherited conditions marked by impaired glycosylation of proteins and lipids. The most prevalent subtype among CDG is PMM2-CDG, inherited in a recessive manner, causing reduced activity of phosphomannomutase. Its phenotype varies from mild to severe, involving the central nervous system and affecting many other organs as well. Patients who are severely affected also exhibit visceral symptoms alongside severe ID and other neurological manifestations. Cerebellar hypoplasia (CH) is characterized by a cerebellum of diminished volume while maintaining its shape. CH exhibits a diverse range of neuroradiologic features, etiologies, clinical characteristics, and neurodevelopmental involvement. Cerebello–oculo–facio–genital syndrome is linked to a recessive MAB21L1 mutation. Jubert's syndrome, associated with a rare autosomal recessive mutation, is identified on magnetic resonance imaging by cerebellar worm hypoplasia and midbrain malformations. The rhombencephalosynapsis, characterized by vermian agenesis or hypogenesis with the fusion of the cerebellar hemispheres, emerges during embryogenesis. It can manifest alone or in conjunction with other and/or extracerebral abnormalities.

Keywords

cerebellum - genetics - ponto-cerebellar hypoplasia - congenital disorders of glycosylation - patterning - neurons

Volltext

Referenzen

References
1 Soto-Ares G, Joyes B, Lemaître MP, Vallée L, Pruvo JP. MRI in children with mental retardation. Pediatr Radiol 2003; 33 (05) 334-345
2 Vincent A, Jacobson L, Plested P. et al. Antibodies affecting ion channel function in acquired neuromyotonia, in seropositive and seronegative myasthenia gravis, and in antibody-mediated arthrogryposis multiplex congenita. Ann N Y Acad Sci 1998; 841: 482-496
3 Courchesne E, Pierce K. Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connectivity. Int J Dev Neurosci 2005; 23 (2-3): 153-170
4 Trifiletti RR, Incorpora G, Polizzi A, Cocuzza MD, Bolan EA, Parano E. Aicardi syndrome with multiple tumors: a case report with literature review. Brain Dev 1995; 17 (04) 283-285
5 Barkovich AJ, Millen KJ, Dobyns WB. A developmental and genetic classification for midbrain-hindbrain malformations. Brain 2009; 132 (Pt 12): 3199-3230
6 Nicita F, Ruggieri M, Polizzi A. et al. Seizures and epilepsy in Sotos syndrome: analysis of 19 Caucasian patients with long-term follow-up. Epilepsia 2012; 53 (06) e102-e105
7 Aida N, Yagishita A, Takada K, Katsumata Y. Cerebellar MR in Fukuyama congenital muscular dystrophy: polymicrogyria with cystic lesions. AJNR Am J Neuroradiol 1994; 15 (09) 1755-1759
8 Leuzzi V, Mastrangelo M, Polizzi A. et al. Report of two never treated adult sisters with aromatic L-amino Acid decarboxylase deficiency: a portrait of the natural history of the disease or an expanding phenotype?. JIMD Rep 2015; 15: 39-45
9 Ross ME, Swanson K, Dobyns WB. Lissencephaly with cerebellar hypoplasia (LCH): a heterogeneous group of cortical malformations. Neuropediatrics 2001; 32 (05) 256-263
10 John AM, Ruggieri M, Ferner R, Upadhyaya M. A search for evidence of somatic mutations in the NF1 gene. J Med Genet 2000; 37 (01) 44-49
11 van Reeuwijk J, Maugenre S, van den Elzen C. et al. The expanding phenotype of POMT1 mutations: from Walker-Warburg syndrome to congenital muscular dystrophy, microcephaly, and mental retardation. Hum Mutat 2006; 27 (05) 453-459
12 Ranieri C, Di Tommaso S, Loconte DC. et al. In vitro efficacy of ARQ 092, an allosteric AKT inhibitor, on primary fibroblast cells derived from patients with PIK3CA-related overgrowth spectrum (PROS). Neurogenetics 2018; 19 (02) 77-91
13 Poirier K, Keays DA, Francis F. et al. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A). Hum Mutat 2007; 28 (11) 1055-1064
14 Ruggieri M, Tigano G, Mazzone D, Tiné A, Pavone L. Involvement of the white matter in hypomelanosis of Ito (incontinentia pigmenti achromiens). Neurology 1996; 46 (02) 485-492
15 Jissendi-Tchofo P, Severino M, Nguema-Edzang B, Toure C, Soto Ares G, Barkovich AJ. Update on neuroimaging phenotypes of mid-hindbrain malformations. Neuroradiology 2015; 57 (02) 113-138
16 Ruggieri M, Pavone P, Polizzi A. et al. Ophthalmological manifestations in segmental neurofibromatosis type 1. Br J Ophthalmol 2004; 88 (11) 1429-1433
17 Gleeson JG, Keeler LC, Parisi MA. et al. Molar tooth sign of the midbrain-hindbrain junction: occurrence in multiple distinct syndromes. Am J Med Genet A 2004; 125A (02) 125-134 , discussion 117
18 O'Connor KC, Lopez-Amaya C, Gagne D. et al. Anti-myelin antibodies modulate clinical expression of childhood multiple sclerosis. J Neuroimmunol 2010; 223 (1-2): 92-99
19 Parisi MA, Dobyns WB. Human malformations of the midbrain and hindbrain: review and proposed classification scheme. Mol Genet Metab 2003; 80 (1-2): 36-53
20 Ruggieri M, Pavone V, De Luca D, Franzò A, Tiné A, Pavone L. Congenital bone malformations in patients with neurofibromatosis type 1 (Nf1). J Pediatr Orthop 1999; 19 (03) 301-305
21 Patel S, Barkovich AJ. Analysis and classification of cerebellar malformations. AJNR Am J Neuroradiol 2002; 23 (07) 1074-1087
22 Ruggieri M, McShane MA. Parental view of epilepsy in Angelman syndrome: a questionnaire study. Arch Dis Child 1998; 79 (05) 423-426
23 Lumsden A, Krumlauf R. Patterning the vertebrate neuraxis. Science 1996; 274 (5290) 1109-1115
24 Pratico AD, Longo L, Mansueto S. et al. Off-label use of drugs and adverse drug reactions in pediatric units: a prospective, multicenter study. Curr Drug Saf 2018; 13 (03) 200-207
25 Wojcinski A, Morabito M, Lawton AK, Stephen DN, Joyner AL. Genetic deletion of genes in the cerebellar rhombic lip lineage can stimulate compensation through adaptive reprogramming of ventricular zone-derived progenitors. Neural Dev 2019; 14 (01) 4
26 Ruggieri M, Polizzi A. Segmental neurofibromatosis. J Neurosurg 2000; 93 (03) 530-532
27 Haldipur P, Dang D, Millen KJ. Embryology. Handb Clin Neurol 2018; 154: 29-44
28 Ruggieri M. Cutis tricolor: congenital hyper- and hypopigmented lesions in a background of normal skin with and without associated systemic features: further expansion of the phenotype. Eur J Pediatr 2000; 159 (10) 745-749
29 Landsberg RL, Awatramani RB, Hunter NL. et al. Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 2005; 48 (06) 933-947
30 Ruggieri M, Polizzi A, Pavone L, Musumeci S. Thalamic syndrome in children with measles infection and selective, reversible thalamic involvement. Pediatrics 1998; 101 (1 Pt 1): 112-119
31 Partanen J. FGF signalling pathways in development of the midbrain and anterior hindbrain. J Neurochem 2007; 101 (05) 1185-1193
32 Pavone P, Praticò AD, Vitaliti G. et al. Hydranencephaly: cerebral spinal fluid instead of cerebral mantles. Ital J Pediatr 2014; 40: 79
33 Chambers D, Wilson LJ, Alfonsi F. et al. Rhombomere-specific analysis reveals the repertoire of genetic cues expressed across the developing hindbrain. Neural Dev 2009; 4: 6
34 Ruggieri M, Praticò AD, Scuderi A, Sorge G, Polizzi A. The multiple faces of artwork diagnoses. Lancet Neurol 2017; 16 (06) 417-418
35 Doherty D, Millen KJ, Barkovich AJ. Midbrain and hindbrain malformations: advances in clinical diagnosis, imaging, and genetics. Lancet Neurol 2013; 12 (04) 381-393
36 Pavone P, Praticò AD, Pavone V. et al. Ataxia in children: early recognition and clinical evaluation. Ital J Pediatr 2017; 43 (01) 6
37 Ondruskova N, Cechova A, Hansikova H, Honzik T, Jaeken J. Congenital disorders of glycosylation: Still “hot” in 2020. Biochim Biophys Acta, Gen Subj 2021; 1865 (01) 129751
38 Barbagallo M, Ruggieri M, Incorpora G. et al. Infantile spasms in the setting of Sturge-Weber syndrome. Childs Nerv Syst 2009; 25 (01) 111-118
39 Van Schaftingen E, Jaeken J. Phosphomannomutase deficiency is a cause of carbohydrate-deficient glycoprotein syndrome type I. FEBS Lett 1995; 377 (03) 318-320
40 Pavone P, Briuglia S, Falsaperla R. et al. Wide spectrum of congenital anomalies including choanal atresia, malformed extremities, and brain and spinal malformations in a girl with a de novo 5.6-Mb deletion of 13q12.11-13q12.13. Am J Med Genet A 2014; 164A (07) 1734-1743
41 Hagberg BA, Blennow G, Kristiansson B, Stibler H. Carbohydrate-deficient glycoprotein syndromes: peculiar group of new disorders. Pediatr Neurol 1993; 9 (04) 255-262
42 Pavone P, Praticò AD, Falsaperla R. et al. Congenital generalized hypertrichosis: the skin as a clue to complex malformation syndromes. Ital J Pediatr 2015; 41: 55
43 Westphal V, Kjaergaard S, Davis JA, Peterson SM, Skovby F, Freeze HH. Genetic and metabolic analysis of the first adult with congenital disorder of glycosylation type Ib: long-term outcome and effects of mannose supplementation. Mol Genet Metab 2001; 73 (01) 77-85
44 Pavone P, Praticò AD, Ruggieri M. et al. Acquired peripheral neuropathy: a report on 20 children. Int J Immunopathol Pharmacol 2012; 25 (02) 513-517
45 Drouin-Garraud V, Belgrand M, Grünewald S. et al. Neurological presentation of a congenital disorder of glycosylation CDG-Ia: implications for diagnosis and genetic counseling. Am J Med Genet 2001; 101 (01) 46-49
46 Pratico AD, Ruggieri M, Falsaperla R, Pavone P. A probable topiramate-induced limbs paraesthesia and rigid fingers flexion. Curr Drug Saf 2018; 13 (02) 131-136
47 Barone R, Fiumara A, Jaeken J. Congenital disorders of glycosylation with emphasis on cerebellar involvement. Semin Neurol 2014; 34 (03) 357-366
48 Pavone P, Falsaperla R, Ruggieri M. et al. Clinical course of N-methyl-D-aspartate receptor encephalitis and the effectiveness of cyclophosphamide treatment. J Pediatr Neurol 2017; 15: 84-49
49 Giurgea I, Michel A, Le Merrer M, Seta N, de Lonlay P. Underdiagnosis of mild congenital disorders of glycosylation type Ia. Pediatr Neurol 2005; 32 (02) 121-123
50 Pavone P, Nigro F, Falsaperla R. et al. Hemihydranencephaly: living with half brain dysfunction. Ital J Pediatr 2013; 39: 3
51 Mader I, Döbler-Neumann M, Küker W, Stibler H, Krägeloh-Mann I. Congenital disorder of glycosylation type Ia: benign clinical course in a new genetic variant. Childs Nerv Syst 2002; 18 (1-2): 77-80
52 Pavone P, Praticò AD, Gentile G. et al. A neurocutaneous phenotype with paired hypo- and hyperpigmented macules, microcephaly and stunted growth as prominent features. Eur J Med Genet 2016; 59 (05) 283-289
53 Vermeer S, Kremer HP, Leijten QH. et al. Cerebellar ataxia and congenital disorder of glycosylation Ia (CDG-Ia) with normal routine CDG screening. J Neurol 2007; 254 (10) 1356-1358
54 Pavone P, Falsaperla R, Ruggieri M, Praticò AD, Pavone L. West syndrome treatment: new roads for an old syndrome. Front Neurol 2013; 4: 113
55 Scott K, Gadomski T, Kozicz T, Morava E. Congenital disorders of glycosylation: new defects and still counting. J Inherit Metab Dis 2014; 37 (04) 609-617
56 Ruggieri M, Praticò AD, Caltabiano R, Polizzi A. Rediagnosing one of Smith's patients (John McCann) with “neuromas tumours” (1849). Neurol Sci 2017; 38 (03) 493-499
57 Barone R, Carrozzi M, Parini R. et al. A nationwide survey of PMM2-CDG in Italy: high frequency of a mild neurological variant associated with the L32R mutation. J Neurol 2015; 262 (01) 154-164
58 Ruggieri M, Polizzi A, Marceca GP, Catanzaro S, Praticò AD, Di Rocco C. Introduction to phacomatoses (neurocutaneous disorders) in childhood. Childs Nerv Syst 2020; 36 (10) 2229-2268
59 Aebi M, Helenius A, Schenk B. et al. Carbohydrate-deficient glycoprotein syndromes become congenital disorders of glycosylation: an updated nomenclature for CDG. First International Workshop on CDGS. Glycoconj J 1999; 16 (11) 669-671
60 Incorpora G, Pavone P, Castellano-Chiodo D, Praticò AD, Ruggieri M, Pavone L. Gelastic seizures due to hypothalamic hamartoma: rapid resolution after endoscopic tumor disconnection. Neurocase 2013; 19 (05) 458-461
61 Grünewald S, Schollen E, Van Schaftingen E, Jaeken J, Matthijs G. High residual activity of PMM2 in patients' fibroblasts: possible pitfall in the diagnosis of CDG-Ia (phosphomannomutase deficiency). Am J Hum Genet 2001; 68 (02) 347-354
62 Vitaliti G, Praticò AD, Cimino C. et al. Hepatitis B vaccine in celiac disease: yesterday, today and tomorrow. World J Gastroenterol 2013; 19 (06) 838-845
63 Matthijs G, Schollen E, Pardon E. et al. Mutations in PMM2, a phosphomannomutase gene on chromosome 16p13, in carbohydrate-deficient glycoprotein type I syndrome (Jaeken syndrome). Nat Genet 1997; 16 (01) 88-92
64 Leonardi S, Praticò AD, Lionetti E, Spina M, Vitaliti G, La Rosa M. Intramuscular vs intradermal route for hepatitis B booster vaccine in celiac children. World J Gastroenterol 2012; 18 (40) 5729-5733
65 Aronica E, van Kempen AA, van der Heide M. et al. Congenital disorder of glycosylation type Ia: a clinicopathological report of a newborn infant with cerebellar pathology. Acta Neuropathol 2005; 109 (04) 433-442
66 Palano GM, Praticò AD, Praticò ER. et al. Intossicazione accidentale da alcol etilico in un lattante di 30 giorni. Quadro clinico e follow-up neurologico. Minerva Pediatr 2007; 59 (03) 275-279
67 Fernlund E, Andersson O, Ellegård R. et al. The congenital disorder of glycosylation in PGM1 (PGM1-CDG) can cause severe cardiomyopathy and unexpected sudden cardiac death in childhood. Forensic Sci Int Genet 2019; 43: 102111
68 Fiumara A, Lanzafame G, Arena A. et al. COVID-19 pandemic outbreak and its psychological impact on patients with rare lysosomal diseases. J Clin Med 2020; 9 (09) 2716
69 Monin ML, Mignot C, De Lonlay P. et al. 29 French adult patients with PMM2-congenital disorder of glycosylation: outcome of the classical pediatric phenotype and depiction of a late-onset phenotype. Orphanet J Rare Dis 2014; 9: 207
70 Sapuppo A, Pavone P, Praticò AD, Ruggieri M, Bertino G, Fiumara A. Genotype-phenotype variable correlation in Wilson disease: clinical history of two sisters with the similar genotype. BMC Med Genet 2020; 21 (01) 128
71 Stefanits H, Konstantopoulou V, Kuess M, Milenkovic I, Matula C. Initial diagnosis of the congenital disorder of glycosylation PMM2-CDG (CDG1a) in a 4-year-old girl after neurosurgical intervention for cerebral hemorrhage. J Neurosurg Pediatr 2014; 14 (05) 546-549
72 Praticò AD, Leonardi S. Immunotherapy for food allergies: a myth or a reality?. Immunotherapy 2015; 7 (02) 147-161
73 Linssen M, Mohamed M, Wevers RA, Lefeber DJ, Morava E. Thrombotic complications in patients with PMM2-CDG. Mol Genet Metab 2013; 109 (01) 107-111
74 Salafia S, Praticò AD, Pizzo E, Greco F, Di Bella D. Hemiconvulsion-hemiplegia-epilepsy syndrome. Magnetic resonance findings in a 3-year-old boy. Neurol Neurochir Pol 2013; 47 (06) 584-589
75 Mohamed M, Theodore M, Claahsen-van der Grinten H. et al. Thyroid function in PMM2-CDG: diagnostic approach and proposed management. Mol Genet Metab 2012; 105 (04) 681-683
76 Praticò AD, Ruggieri M. COVID-19 vaccination for children: may be necessary for the full eradication of the disease. Pediatr Res 2021; 90 (06) 1102-1103
77 Jaeken J. Congenital disorders of glycosylation. Handb Clin Neurol 2013; 113: 1737-1743
78 Praticò AD, Mistrello G, La Rosa M. et al. Immunotherapy: a new horizon for egg allergy?. Expert Rev Clin Immunol 2014; 10 (05) 677-686
79 Moosavi A, Kanekar S. Congenital malformations of cerebellum. Clin Perinatol 2022; 49 (03) 603-621
80 Praticò AD. COVID-19 pandemic for pediatric health care: disadvantages and opportunities. Pediatr Res 2021; 89 (04) 709-710
81 Pinchefsky EF, Accogli A, Shevell MI, Saint-Martin C, Srour M. Developmental outcomes in children with congenital cerebellar malformations. Dev Med Child Neurol 2019; 61 (03) 350-358
82 Praticò AD, Giallongo A, Arrabito M. et al. SCN2A and its related epileptic phenotypes. J Pediatr Neurol 2023; 21: 173-185
83 Aldinger KA, Timms AE, Thomson Z. et al. Redefining the etiologic landscape of cerebellar malformations. Am J Hum Genet 2019; 105 (03) 606-615
84 Praticò AD, Falsaperla R, Comella M, Belfiore G, Polizzi A, Ruggieri M. Case report: a gain-of-function of hamartin may lead to a distinct “inverse TSC1-hamartin” phenotype characterized by reduced cell growth. Front Pediatr 2023; 11: 1101026
85 Bar C, Kuchenbuch M, Barcia G. et al. Developmental and epilepsy spectrum of KCNB1 encephalopathy with long-term outcome. Epilepsia 2020; 61 (11) 2461-2473
86 Stegeman R, Sprong MCA, Breur JMPJ. et al; CHD LifeSpan Study Group Utrecht. Early motor outcomes in infants with critical congenital heart disease are related to neonatal brain development and brain injury. Dev Med Child Neurol 2022; 64 (02) 192-199
87 Ivanova EL, Mau-Them FT, Riazuddin S. et al. Homozygous truncating variants in TBC1D23 cause pontocerebellar hypoplasia and alter cortical development. Am J Hum Genet 2017; 101 (03) 428-440
88 Laugwitz L, Buchert R, Groeschel S. et al. Pontocerebellar hypoplasia type 11: does the genetic defect determine timing of cerebellar pathology?. Eur J Med Genet 2020; 63 (07) 103938
89 Leibovitz Z, Lerman-Sagie T, Haddad L. Fetal brain development: regulating processes and related malformations. Life (Basel) 2022; 12 (06) 809
90 Lerman-Sagie T, Pogledic I, Leibovitz Z, Malinger G. A practical approach to prenatal diagnosis of malformations of cortical development. Eur J Paediatr Neurol 2021; 34: 50-61
91 Adamaszek M, D'Agata F, Ferrucci R. et al. Consensus paper: cerebellum and emotion. Cerebellum 2017; 16 (02) 552-576
92 Wafik M, Taylor J, Lester T, Gibbons RJ, Shears DJ. 2 new cases of pontocerebellar hypoplasia type 10 identified by whole exome sequencing in a Turkish family. Eur J Med Genet 2018; 61 (05) 273-279
93 Marin-Valencia I, Gerondopoulos A, Zaki MS. et al. Homozygous mutations in TBC1D23 lead to a non-degenerative form of pontocerebellar hypoplasia. Am J Hum Genet 2017; 101 (03) 441-450
94 Malinger G, Ginath S, Lerman-Sagie T, Watemberg N, Lev D, Glezerman M. The fetal cerebellar vermis: normal development as shown by transvaginal ultrasound. Prenat Diagn 2001; 21 (08) 687-692
95 Leibovitz Z, Shkolnik C, Haratz KK, Malinger G, Shapiro I, Lerman-Sagie T. 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 (05) 575-580
96 Expanded Journal of Maternal-Fetal & Neonatal Medicine. Expanded Journal of Maternal-Fetal & Neonatal Medicine. J Matern Fetal Neonatal Med 2012; 25 (06) 551
97 Guimaraes CVA, Dahmoush HM. Fetal brain anatomy. Neuroimaging Clin N Am 2022; 32 (03) 663-681
98 Guibaud L. Fetal cerebral ventricular measurement and ventriculomegaly: time for procedure standardization. Ultrasound Obstet Gynecol 2009; 34 (02) 127-130
99 Levine D, Cavazos C, Kazan-Tannus JF. et al. Evaluation of real-time single-shot fast spin-echo MRI for visualization of the fetal midline corpus callosum and secondary palate. AJR Am J Roentgenol 2006; 187 (06) 1505-1511
100 Tocchio S, Kline-Fath B, Kanal E, Schmithorst VJ, Panigrahy A. MRI evaluation and safety in the developing brain. Semin Perinatol 2015; 39 (02) 73-104
101 Triulzi F, Parazzini C, Righini A. MRI of fetal and neonatal cerebellar development. Semin Fetal Neonatal Med 2005; 10 (05) 411-420
102 Fame RM, MacDonald JL, Macklis JD. Development, specification, and diversity of callosal projection neurons. Trends Neurosci 2011; 34 (01) 41-50
103 Sullo F. et al. Cerebellotrigeminal dermal dysplasia (Gómez-López-Hernández syndrome). J Pediatr Neurol 2018; 16: 362-368
104 Saugier-Veber P, Marguet F, Vezain M. et al. Pontocerebellar hypoplasia with rhombencephalosynapsis and microlissencephaly expands the spectrum of PCH type 1B. Eur J Med Genet 2020; 63 (04) 103814
105 Mariani M, Corradi A, Baldessari D. et al. Mab21, the mouse homolog of a C. elegans cell-fate specification gene, participates in cerebellar, midbrain and eye development. Mech Dev 1998; 79 (1-2): 131-135
106 Bruel AL, Masurel-Paulet A, Rivière JB. et al. Autosomal recessive truncating MAB21L1 mutation associated with a syndromic scrotal agenesis. Clin Genet 2017; 91 (02) 333-338
107 Rad A, Altunoglu U, Miller R. et al. MAB21L1 loss of function causes a syndromic neurodevelopmental disorder with distinctive cerebellar, ocular, craniofacial and genital features (COFG syndrome). J Med Genet 2019; 56 (05) 332-339
108 Dehghani M, Mojarad M, Ghayoor Karimiani E. et al. A common ancestral Asn242Ser mutation in TMEM67 identified in multiple Iranian families with Joubert syndrome. Public Health Genomics 2017; 20 (03) 188-193
109 Tavano A, Borgatti R. Evidence for a link among cognition, language and emotion in cerebellar malformations. Cortex 2010; 46 (07) 907-918