PDF herunterladen
Journal of Pediatric Neurology 2024; 22(05): 377-386
DOI: 10.1055/s-0044-1786788
Review Article

Anomalies of Midbrain/Hindbrain Development: Malformations of Cerebellum: Diagnosis, Classification, and Rehabilitative Hypothesis

Emanuele Liotta‡   *
1   Pediatrics Postgraduate Residency Program, University of Catania, Catania, Italy
,
Federica Dierna‡   *
1   Pediatrics Postgraduate Residency Program, University of Catania, Catania, Italy
,
Antonio Zanghì‡   *
2   Department 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
,
Stefania Salafia
3   Unit of Pediatrics, Lentini Hospital, Lentini, Italy
,
Michele Vecchio
4   Department of Biomedical and Biotechnological Sciences, Rehabilitation Unit, University of Catania, Catania, Italy
,
Rita Chiaramonte
4   Department of Biomedical and Biotechnological Sciences, Rehabilitation Unit, University of Catania, Catania, Italy
,
Giovanna Cancemi
5   Department of Medical Surgical Sciences and Advanced Technologies, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy
,
Giuseppe Belfiore
6   Department of Medical Surgical Sciences and Advanced Technologies, Unit of Radiology 1, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy
,
Antonio Basile
6   Department of Medical Surgical Sciences and Advanced Technologies, Unit of Radiology 1, University Hospital Policlinico “G. Rodolico-San Marco”, Catania, Italy
,
Martino Ruggieri
7   Department of Clinical and Experimental Medicine, Unit of Clinical Pediatrics, University of Catania, Catania, Italy
,
Agata Polizzi
8   Department of Educational Sciences, University of Catania, Catania, Italy
› Institutsangaben
› Weitere Informationen
Auch verfügbar auf
    Lizenzen und Reprints

Abstract

Extensive research has been conducted on the cerebellum, making it one of the most thoroughly investigated regions of the brain. It plays a fundamental role not only in motor control but also in motor learning and cognition. The development of the cerebellum is a lengthy process, beginning during the embryonic period up to the first years of life. This slow and protracted process makes it a vulnerable organ liable to different insults, responsible for many developmental disorders such as Dandy–Walker syndrome, medulloblastoma, dystroglicanopathy, pontocerebellar hypoplasia, thubulinopathies, and Jubert syndrome. Due to several factors, the true prevalence of cerebellar malformations is not known in most cases. The cerebellum undergoes development through following four fundamental stages:

(1) Identification of the cerebellar region at the boundary between the midbrain and hindbrain.

(2) Establishment of two cell proliferation compartments: firstly, Purkinje cells and deep cerebellar nuclei emerge from the ventricular zone of the metencephalic alar plate; secondly, granule cell precursors are generated from a separate proliferation compartment known as the upper rhombic lip.

(3) Migration of granule cells toward the interior: granule precursor cells constitute the external granular layer (EGL), and during the initial postnatal year, granule cells migrate inward to their final position in the internal granular layer.

(4) Formation of cerebellar circuitry and subsequent differentiation.

Based on different types of involvement of the structures detected in the brain magnetic resonance, the classification of brainstem and cerebellar anomalies is divided into three categories: (1) mainly the cerebellum, (2) mainly the brain stem, and (3) both involved. This review will outline the developmental processes of the cerebellum and delve into common developmental disorders associated with it, including the Dandy–Walker syndrome, cerebellar hypoplasia, rhomboencephalosynapsis, lissencephaly, and gray matter heterotopias.

Keywords

cerebellar malformations - cerebellum - cerebellar region/hypoplasia/Dandy–Walker syndrome

* The authors contributed equally to the article.




Publikationsverlauf

Eingereicht: 11. Dezember 2023

Angenommen: 03. April 2024

Artikel online veröffentlicht:
11. Mai 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Ten Donkelaar HJ, Lammens M. Development of the human cerebellum and its disorders. Clin Perinatol 2009; 36 (03) 513-530
    CrossrefPubMedGoogle Scholar
  • 2 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
    CrossrefPubMedGoogle Scholar
  • 3 Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 2004; 16 (03) 367-378
    CrossrefPubMedGoogle Scholar
  • 4 Ruggieri M, Milone P, Pavone P. et al. Nevus vascularis mixtus (cutaneous vascular twin nevi) associated with intracranial vascular malformation of the Dyke-Davidoff-Masson type in two patients. Am J Med Genet A 2012; 158A (11) 2870-2880
    CrossrefPubMedGoogle Scholar
  • 5 Calandrelli R, Tuzza L, Romeo DM, Arpaia C, Colosimo C, Pilato F. Extremely preterm infants with a near-total absence of cerebellum: usefulness of quantitative magnetic resonance in predicting the motor outcome. Cerebellum 2024; 23 (03) 981-992
    CrossrefPubMedGoogle Scholar
  • 6 Ruggieri M, Iannetti P, Clementi M. et al. Neurofibromatosis type 1 and infantile spasms. Childs Nerv Syst 2009; 25 (02) 211-216
    CrossrefPubMedGoogle Scholar
  • 7 ten Donkelaar HJ, Lammens M, Wesseling P, Thijssen HO, Renier WO. Development and developmental disorders of the human cerebellum. J Neurol 2003; 250 (09) 1025-1036
    CrossrefPubMedGoogle Scholar
  • 8 Ruggieri M, Pavone P, Polizzi A. et al. Ophthalmological manifestations in segmental neurofibromatosis type 1. Br J Ophthalmol 2004; 88 (11) 1429-1433
    CrossrefPubMedGoogle Scholar
  • 9 Ramaekers VT, Heimann G, Reul J, Thron A, Jaeken J. Genetic disorders and cerebellar structural abnormalities in childhood. Brain 1997; 120 (Pt 10): 1739-1751
    CrossrefPubMedGoogle Scholar
  • 10 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
    CrossrefPubMedGoogle Scholar
  • 11 Abdel Razek AA, Castillo M. Magnetic resonance imaging of malformations of midbrain-hindbrain. J Comput Assist Tomogr 2016; 40 (01) 14-25
    CrossrefPubMedGoogle Scholar
  • 12 Salpietro V, Polizzi A, Di Rosa G. et al. Adrenal disorders and the paediatric brain: pathophysiological considerations and clinical implications. Int J Endocrinol 2014; 2014: 282489
    CrossrefPubMedGoogle Scholar
  • 13 Long A, Moran P, Robson S. Outcome of fetal cerebral posterior fossa anomalies. Prenat Diagn 2006; 26 (08) 707-710
    CrossrefPubMedGoogle Scholar
  • 14 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
    CrossrefPubMedGoogle Scholar
  • 15 Aldinger KA, Doherty D. The genetics of cerebellar malformations. Semin Fetal Neonatal Med 2016; 21 (05) 321-332
    CrossrefPubMedGoogle Scholar
  • 16 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
    CrossrefPubMedGoogle Scholar
  • 17 Accogli A, Addour-Boudrahem N, Srour M. Diagnostic approach to cerebellar hypoplasia. Cerebellum 2021; 20 (04) 631-658
    CrossrefPubMedGoogle Scholar
  • 18 Ruggieri M, Praticò AD, Scuderi A, Sorge G, Polizzi A. The multiple faces of artwork diagnoses. Lancet Neurol 2017; 16 (06) 417-418
    CrossrefPubMedGoogle Scholar
  • 19 Correa GG, Amaral LF, Vedolin LM. Neuroimaging of Dandy-Walker malformation: new concepts. Top Magn Reson Imaging 2011; 22 (06) 303-312
    CrossrefPubMedGoogle Scholar
  • 20 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
    CrossrefPubMedGoogle Scholar
  • 21 Haldipur P, Aldinger KA, Bernardo S. et al. Spatiotemporal expansion of primary progenitor zones in the developing human cerebellum. Science 2019; 366 (6464) 454-460
    CrossrefPubMedGoogle Scholar
  • 22 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
    PubMedGoogle Scholar
  • 23 Patel S, Barkovich AJ. Analysis and classification of cerebellar malformations. AJNR Am J Neuroradiol 2002; 23 (07) 1074-1087
    PubMedGoogle Scholar
  • 24 Pavone P, Praticò AD, Pavone V. et al. Ataxia in children: early recognition and clinical evaluation. Ital J Pediatr 2017; 43 (01) 6
    CrossrefPubMedGoogle Scholar
  • 25 Poretti A, Boltshauser E, Huisman TA. Prenatal cerebellar disruptions: neuroimaging spectrum of findings in correlation with likely mechanisms and etiologies of injury. Neuroimaging Clin N Am 2016; 26 (03) 359-372
    CrossrefPubMedGoogle Scholar
  • 26 Pavone P, Rizzo R, Conti I. et al. Primary headaches in children: clinical findings on the association with other conditions. Int J Immunopathol Pharmacol 2012; 25 (04) 1083-1091
    CrossrefPubMedGoogle Scholar
  • 27 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
    CrossrefPubMedGoogle Scholar
  • 28 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
    CrossrefPubMedGoogle Scholar
  • 29 Maricich SM, Aqeeb KA, Moayedi Y. et al. Pontocerebellar hypoplasia: review of classification and genetics, and exclusion of several genes known to be important for cerebellar development. J Child Neurol 2011; 26 (03) 288-294
    CrossrefPubMedGoogle Scholar
  • 30 Praticò AD, Pavone P, Scuderi MG. et al. Symptomatic hypocalcemia in an epileptic child treated with valproic acid plus lamotrigine: a case report. Cases J 2009; 2: 7394
    PubMedGoogle Scholar
  • 31 Leto K, Arancillo M, Becker EB. et al. Consensus paper: cerebellar development. Cerebellum 2016; 15 (06) 789-828
    CrossrefPubMedGoogle Scholar
  • 32 Pavone P, Praticò AD, Ruggieri M, Falsaperla R. Hypomelanosis of Ito: a round on the frequency and type of epileptic complications. Neurol Sci 2015; 36 (07) 1173-1180
    CrossrefPubMedGoogle Scholar
  • 33 Stambolliu E, Ioakeim-Ioannidou M, Kontokostas K, Dakoutrou M, Kousoulis AA. The most common comorbidities in Dandy-Walker syndrome patients: a systematic review of case reports. J Child Neurol 2017; 32 (10) 886-902
    CrossrefPubMedGoogle Scholar
  • 34 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
    CrossrefPubMedGoogle Scholar
  • 35 Blank MC, Grinberg I, Aryee E. et al. Multiple developmental programs are altered by loss of Zic1 and Zic4 to cause Dandy-Walker malformation cerebellar pathogenesis. Development 2011; 138 (06) 1207-1216
    CrossrefPubMedGoogle Scholar
  • 36 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
    CrossrefPubMedGoogle Scholar
  • 37 Haldipur P, Gillies GS, Janson OK. et al. Foxc1 dependent mesenchymal signalling drives embryonic cerebellar growth. eLife 2014; 3: e03962
    CrossrefPubMedGoogle Scholar
  • 38 Pavone P, Nigro F, Falsaperla R. et al. Hemihydranencephaly: living with half brain dysfunction. Ital J Pediatr 2013; 39: 3
    CrossrefPubMedGoogle Scholar
  • 39 Vertinsky AT, Barnes PD. Macrocephaly, increased intracranial pressure, and hydrocephalus in the infant and young child. Top Magn Reson Imaging 2007; 18 (01) 31-51
    CrossrefPubMedGoogle Scholar
  • 40 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
    CrossrefPubMedGoogle Scholar
  • 41 Deng, F. & Gaillard, F. Blake's pouch cyst. Accessed 12 February, 2023. Radiopaedia.org
    PubMedGoogle Scholar
  • 42 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
    CrossrefPubMedGoogle Scholar
  • 43 Weisbrod LJ, Thorell W. Mega cisterna magna. 2023 May 29. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023
    Google Scholar
  • 44 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
    CrossrefPubMedGoogle Scholar
  • 45 Ishak GE, Dempsey JC, Shaw DW. et al. Rhombencephalosynapsis: a hindbrain malformation associated with incomplete separation of midbrain and forebrain, hydrocephalus and a broad spectrum of severity. Brain 2012; 135 (Pt 5): 1370-1386
    CrossrefPubMedGoogle Scholar
  • 46 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
    CrossrefPubMedGoogle Scholar
  • 47 Fouda MA, Kim TY, Cohen AR. Rhomboencephalosynapsis: review of the literature. World Neurosurg 2022; 159: 48-53
    CrossrefPubMedGoogle Scholar
  • 48 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
    CrossrefPubMedGoogle Scholar
  • 49 Aldinger KA, Dempsey JC, Tully HM. et al. Rhombencephalosynapsis: fused cerebellum, confused geneticists. Am J Med Genet C Semin Med Genet 2018; 178 (04) 432-439
    CrossrefPubMedGoogle Scholar
  • 50 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
    CrossrefPubMedGoogle Scholar
  • 51 Nakamura H, Katahira T, Matsunaga E, Sato T. Isthmus organizer for midbrain and hindbrain development. Brain Res Brain Res Rev 2005; Sep; 49 (02) 120-126
    CrossrefPubMedGoogle Scholar
  • 52 Palano GM, Praticò AD, Praticò ER. et al. Intossicazione accidentale da alcol etilico in un lattante di 30 giorni. Quadro hombe e follow-up neurologico. Minerva Pediatr 2007; 59 (03) 275-279
    PubMedGoogle Scholar
  • 53 Paprocka J, Jamroz E, Scieszka E, Kluczewska E. Isolated rhomboencephalosynapsis – a rare cerebellar anomaly. Pol J Radiol 2012; 77 (01) 47-49
    CrossrefPubMedGoogle Scholar
  • 54 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
    CrossrefPubMedGoogle Scholar
  • 55 Barkovich AJ, Guerrini R, Kuzniecky RI, Jackson GD, Dobyns WB. A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012; 135 (Pt 5): 1348-1369
    CrossrefPubMedGoogle Scholar
  • 56 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
    CrossrefPubMedGoogle Scholar
  • 57 Sener RN. Unusual MRI findings in hombencephalosynapsis. Comput Med Imaging Graph 2000; 24 (04) 277-282
    CrossrefPubMedGoogle Scholar
  • 58 Praticò AD, Leonardi S. Immunotherapy for food allergies: a myth or a reality?. Immunotherapy 2015; 7 (02) 147-161
    CrossrefPubMedGoogle Scholar
  • 59 Bonnetain MF, Rougeot-Jung C, Sarret C. et al. Normal intellectual skills in patients with Rhombencephalosynapsis. Eur J Paediatr Neurol 2020; 29: 92-100
    CrossrefPubMedGoogle Scholar
  • 60 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
    CrossrefPubMedGoogle Scholar
  • 61 Berquin PC, Giedd JN, Jacobsen LK. et al. Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology 1998; 50 (04) 1087-1093
    CrossrefPubMedGoogle Scholar
  • 62 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
    CrossrefPubMedGoogle Scholar
  • 63 Sellick GS, Barker KT, Stolte-Dijkstra I. et al. Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat Genet 2004; 36 (12) 1301-1305
    CrossrefPubMedGoogle Scholar
  • 64 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
    CrossrefPubMedGoogle Scholar
  • 65 Lerman-Sagie T, Prayer D, Stöcklein S, Malinger G. Fetal cerebellar disorders. Handb Clin Neurol 2018; 155: 3-23
    CrossrefPubMedGoogle Scholar
  • 66 Praticò AD. COVID-19 pandemic for pediatric health care: disadvantages and opportunities. Pediatr Res 2021; 89 (04) 709-710
    CrossrefPubMedGoogle Scholar
  • 67 Poretti A, Boltshauser E, Huisman TA. Congenital brain abnormalities: an update on malformations of cortical development and infratentorial malformations. Semin Neurol 2014; 34 (03) 239-248
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 68 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
    CrossrefPubMedGoogle Scholar
  • 69 Namavar Y, Barth PG, Kasher PR. et al; PCH Consortium. Clinical, neuroradiological and genetic findings in pontocerebellar hypoplasia. Brain 2011; 134 (Pt 1): 143-156
    CrossrefPubMedGoogle Scholar
  • 70 Praticò AD, Polizzi A, Salafia R. et al. Megalencephaly capillary malformation syndrome. J Pediatr Neurol 2018; 16: 328-337
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 71 Hayashi S, Uehara DT, Tanimoto K. et al. Comprehensive investigation of CASK mutations and other genetic etiologies in 41 patients with intellectual disability and microcephaly with pontine and cerebellar hypoplasia (MICPCH). PloS One 2017; 12 (08) e0181791
    CrossrefPubMedGoogle Scholar
  • 72 Pratico AD, Salafia S, Barone P, La Rosa M, Leonardi S, Type II. Type II autoimmune hepatitis and small duct sclerosing cholangitis in a seven years old child: an overlap syndrome?. Hepat Mon 2013; 13 (12) e14452
    CrossrefPubMedGoogle Scholar
  • 73 Hong SE, Shugart YY, Huang DT. et al. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 2000; 26 (01) 93-96
    CrossrefPubMedGoogle Scholar
  • 74 Pavone P, Falsaperla R, Ruggieri M, Praticò AD, Pavone L. West syndrome treatment: new roads for an old syndrome. Front Neurol 2013; 4: 113
    CrossrefPubMedGoogle Scholar
  • 75 Poretti A, Boltshauser E, Huisman TA. Cerebellar and brainstem malformations. Neuroimaging Clin N Am 2016; 26 (03) 341-357
    CrossrefPubMedGoogle Scholar
  • 76 Barth PG, Majoie CB, Caan MW. et al. Pontine tegmental cap dysplasia: a novel brain malformation with a defect in axonal guidance. Brain 2007; 130 (Pt 9): 2258-2266
    CrossrefPubMedGoogle Scholar
  • 77 Jen JC, Chan WM, Bosley TM. et al. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 2004; 304 (5676) 1509-1513
    CrossrefPubMedGoogle Scholar
  • 78 Poretti A, Boltshauser E, Plecko B. Brainstem disconnection: case report and review of the literature. Neuropediatrics 2007; 38 (04) 210-212
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 79 Severino M, Righini A, Tortora D. et al. MR imaging diagnosis of diencephalic-mesencephalic junction dysplasia in fetuses with developmental ventriculomegaly. AJNR Am J Neuroradiol 2017; 38 (08) 1643-1646
    CrossrefPubMedGoogle Scholar
  • 80 Zaki MS, Saleem SN, Dobyns WB. et al. Diencephalic-mesencephalic junction dysplasia: a novel recessive brain malformation. Brain 2012; 135 (Pt 8): 2416-2427
    CrossrefPubMedGoogle Scholar
  • 81 Bertholdo D, de Carvalho Neto A, Castillo M. Posterior fossa malformation associated with cerebral anomalies: genetic and imaging features. Top Magn Reson Imaging 2011; 22 (06) 295-302
    CrossrefPubMedGoogle Scholar
  • 82 Hewitt JE. Abnormal glycosylation of dystroglycan in human genetic disease. Biochim Biophys Acta 2009; 1792 (09) 853-861
    CrossrefPubMedGoogle Scholar
  • 83 Clement E, Mercuri E, Godfrey C. et al. Brain involvement in muscular dystrophies with defective dystroglycan glycosylation. Ann Neurol 2008; 64 (05) 573-582
    CrossrefPubMedGoogle Scholar
  • 84 González G, Vedolin L, Barry B, Poduri A, Walsh C, Barkovich AJ. Location of periventricular nodular heterotopia is related to the malformation phenotype on MRI. AJNR Am J Neuroradiol 2013; 34 (04) 877-883
    CrossrefPubMedGoogle Scholar
  • 85 Jissendi-Tchofo P, Kara S, Barkovich AJ. Midbrain-hindbrain involvement in lissencephalies. Neurology 2009; 72 (05) 410-418
    CrossrefPubMedGoogle Scholar
  • 86 Lecourtois M, Poirier K, Friocourt G. et al. Human lissencephaly with cerebellar hypoplasia due to mutations in TUBA1A: expansion of the foetal neuropathological phenotype. Acta Neuropathol 2010; 119 (06) 779-789
    CrossrefPubMedGoogle Scholar
  • 87 Chiaramonte R, Pavone P, Vecchio M. Speech rehabilitation in dysarthria after stroke: a systematic review of the studies. Eur J Phys Rehabil Med 2020; 56 (05) 547-562
    CrossrefPubMedGoogle Scholar
  • 88 Chiaramonte R, Vecchio M. A systematic review of measures of dysarthria severity in stroke patients. PM R 2021; 13 (03) 314-324
    CrossrefPubMedGoogle Scholar
  • 89 Vecchio M, Gracies JM, Panza F. et al. Change in coefficient of fatigability following rapid, repetitive movement training in post-stroke spastic paresis: a prospective open-label observational study. J Stroke Cerebrovasc Dis 2017; 26 (11) 2536-2540
    CrossrefPubMedGoogle Scholar
  • 90 Santamato A, Ranieri M, Solfrizzi V. et al. High doses of incobotulinumtoxinA for the treatment of post-stroke spasticity: are they safe and effective?. Expert Opin Drug Metab Toxicol 2016; 12 (08) 843-846
    CrossrefPubMedGoogle Scholar