Radiological Features of Joubert's Syndrome

Giovanni Stroscio; Caterina Cuppari; Maria Domenica Ceravolo; Annamaria Salpietro; Francesco Battaglia; Alessia Sallemi; Monica Fusco; Antonio Ceravolo; Giulia Iapadre; Elisa Calì; Daniela Impollonia; Francesca Granata

doi:10.1055/s-0042-1760241

Journal of Pediatric Neurology, Inhaltsverzeichnis

Journal of Pediatric Neurology 2023; 21(01): 073-077
DOI: 10.1055/s-0042-1760241

Review Article

Radiological Features of Joubert's Syndrome

Giovanni Stroscio

¹Unit of Radiology, Department of Human Pathology in Adulthood and Childhood “G. Barresi,” University Hospital of Messina, Messina, Italy

,

Caterina Cuppari

²Unit of Pediatric Emergency, Department of Human Pathology of the Adult and Developmental Age “Gaetano Barresi,” University of Messina, Messina, Italy

,

Maria Domenica Ceravolo

²Unit of Pediatric Emergency, Department of Human Pathology of the Adult and Developmental Age “Gaetano Barresi,” University of Messina, Messina, Italy

,

Annamaria Salpietro

³ASST-Spedali Civili of Brescia, Pediatrics Clinic, Brescia, Italy

,

Francesco Battaglia

⁴Orthopaedic and Traumatology Department, “S. Anna” Hospital, University of Ferrara, Ferrara, Italy

,

Alessia Sallemi

²Unit of Pediatric Emergency, Department of Human Pathology of the Adult and Developmental Age “Gaetano Barresi,” University of Messina, Messina, Italy

,

Monica Fusco

²Unit of Pediatric Emergency, Department of Human Pathology of the Adult and Developmental Age “Gaetano Barresi,” University of Messina, Messina, Italy

,

Antonio Ceravolo

⁵Department of Pediatrics, Cinquefrondi, Reggio Calabria, Italy

,

Giulia Iapadre

⁶Department of Pediatrics, University of L'Aquila, L'Aquila, Italy

,

Elisa Calì

⁷Department of Neuromuscular Diseases, UCL Queen Square Institute of Neurology, London, United Kingdom

,

Daniela Impollonia

¹Unit of Radiology, Department of Human Pathology in Adulthood and Childhood “G. Barresi,” University Hospital of Messina, Messina, Italy

,

Francesca Granata

¹Unit of Radiology, Department of Human Pathology in Adulthood and Childhood “G. Barresi,” University Hospital of Messina, Messina, Italy

› Institutsangaben

Abstract

Joubert syndrome (JS) is a rare autosomal recessive disorder. All patients affected by this syndrome presented a characteristic picture of cranial fossa malformations, called “molar tooth sign.” This sign is defined by the presence in axial section at the level of a deck/midbrain, of hypo/dysplasia of the cerebellar vermis, abnormally deep interpeduncular fossa and horizontalized thickened and elongated superior cerebellar peduncles. Although “molar tooth sign” is peculiar of JS, other radiological findings have been also reported in these patients. Here, the authors briefly assumed the principal magnetic resonance imaging findings of JS.

Keywords

Joubert syndrome - radiological findings - “molar tooth sign”

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Referenzen

References
1 Brancati F, Dallapiccola B, Valente EM. Joubert syndrome and related disorders. Orphanet J Rare Dis 2010; 5: 20
2 Salpietro CD, Briuglia S, Rigoli L, Merlino MV, Dallapiccola B. Confirmation of Nablus mask-like facial syndrome. Am J Med Genet A 2003; 121A (03) 283-285
3 Salpietro V, Phadke R, Saggar A. et al. Zellweger syndrome and secondary mitochondrial myopathy. Eur J Pediatr 2015; 174 (04) 557-563
4 Salpietro V, Zollo M, Vandrovcova J. et al; SYNAPS Study Group. The phenotypic and molecular spectrum of PEHO syndrome and PEHO-like disorders. Brain 2017; 140 (08) e49
5 Damiano Salpietro C, Briuglia S, Valeria Merlino M, Piraino B, Valenzise M, Dallapiccola B. Hallerman-Streiff syndrome: patient with decreased GH and insulin-like growth factor-1. Am J Med Genet A 2004; 125A (02) 216-218
6 Lacquaniti A, Chirico V, Donato V. et al. NGAL as an early biomarker of kidney disease in Joubert syndrome: three brothers compared. Ren Fail 2012; 34 (04) 495-498
7 Travaglini L, Brancati F, Attie-Bitach T. et al; International JSRD Study Group. Expanding CEP290 mutational spectrum in ciliopathies. Am J Med Genet A 2009; 149A (10) 2173-2180
8 Travaglini L, Brancati F, Silhavy J. et al; International JSRD Study Group. Phenotypic spectrum and prevalence of INPP5E mutations in Joubert syndrome and related disorders. Eur J Hum Genet 2013; 21 (10) 1074-1078
9 Valente EM, Salpietro DC, Brancati F. et al. Description, nomenclature, and mapping of a novel cerebello-renal syndrome with the molar tooth malformation. Am J Hum Genet 2003; 73 (03) 663-670
10 Poretti A, Snow J, Summers AC. et al; NISC Comparative Sequencing Program. Joubert syndrome: neuroimaging findings in 110 patients in correlation with cognitive function and genetic cause. J Med Genet 2017; 54 (08) 521-529
11 Molinari E, Srivastava S, Sayer JA, Ramsbottom SA. From disease modelling to personalised therapy in patients with CEP290 mutations. F1000 Res 2017; 6: 669
12 Manole A, Jaunmuktane Z, Hargreaves I. et al. Clinical, pathological and functional characterization of riboflavin-responsive neuropathy. Brain 2017; 140 (11) 2820-2837
13 Leu C, Stevelink R, Smith AW. et al; Epi25 Consortium. Polygenic burden in focal and generalized epilepsies. Brain 2019; 142 (11) 3473-3481
14 Bruno L, Ceravolo G, Ceravolo MD. et al. Genetic cardiac channelopathies and SIDS. J Biol Regul Homeost Agents 2020; 34 (4, suppl. 2): 55-58
15 Piard J, Umanah GKE, Harms FL. et al. A homozygous ATAD1 mutation impairs postsynaptic AMPA receptor trafficking and causes a lethal encephalopathy. Brain 2018; 141 (03) 651-661
16 Chelban V, Wilson MP, Warman Chardon J. et al; Care4Rare Canada Consortium and the SYNaPS Study Group. PDXK mutations cause polyneuropathy responsive to pyridoxal 5′-phosphate supplementation. Ann Neurol 2019; 86 (02) 225-240
17 Pellerin D, Ellezam B, Korathanakhun P. et al. Multisystem proteinopathy associated with a VCP G156S mutation in a French Canadian Family. Can J Neurol Sci 2020; 47 (03) 412-415
18 Nascimben F, Peri FM, Impellizzeri P. et al. Role of oxidative stress in the pathogenesis of congenital cardiopathies. J Biol Regul Homeost Agents 2020; 34 (4, suppl 2): 85-90
19 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
20 Carotenuto M, Roccella M, Pisani F. et al. Polysomnographic findings in fragile X syndrome children with EEG abnormalities. Behav Neurol 2019; 2019: 5202808
21 Coleman J, Jouannot O, Ramakrishnan SK. et al. PRRT2 regulates synaptic fusion by directly modulating SNARE complex assembly. Cell Rep 2018; 22 (03) 820-831
22 Salpietro V, Lin W, Delle Vedove A. et al; SYNAPS Study Group. Homozygous mutations in VAMP1 cause a presynaptic congenital myasthenic syndrome. Ann Neurol 2017; 81 (04) 597-603
23 Giacobbe A, Granese R, Grasso R. et al. Association between maternal serum high mobility group box 1 levels and pregnancy complicated by gestational diabetes mellitus. Nutr Metab Cardiovasc Dis 2016; 26 (05) 414-418
24 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
25 Efthymiou S, Salpietro V, Malintan N. et al; SYNAPS Study Group. Biallelic mutations in neurofascin cause neurodevelopmental impairment and peripheral demyelination. Brain 2019; 142 (10) 2948-2964
26 Cuppari C, Amatruda M, Ceravolo G. et al. Myocarditis in children – from infection to autoimmunity. J Biol Regul Homeost Agents 2020; 34 (4, suppl 2): 37-41
27 Steel D, Salpietro V, Phadke R. et al. Whole exome sequencing reveals a MLL de novo mutation associated with mild developmental delay and without ‘hairy elbows’: expanding the phenotype of Wiedemann-Steiner syndrome. J Genet 2015; 94 (04) 755-758
28 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
29 Toldo I, Brunello F, Morao V. et al. First attack and clinical presentation of hemiplegic migraine in pediatric age: a multicenter retrospective study and literature review. Front Neurol 2019; 10: 1079
30 Chimenz R, Chirico V, Cuppari C. et al. Fabry disease and kidney involvement: starting from childhood to understand the future. Pediatr Nephrol 2022; 37 (01) 95-103
31 Greco M, Ferrara P, Farello G, Striano P, Verrotti A. Electroclinical features of epilepsy associated with 1p36 deletion syndrome: a review. Epilepsy Res 2018; 139: 92-101
32 Bell S, Rousseau J, Peng H. et al. Mutations in ACTL6B cause neurodevelopmental deficits and epilepsy and lead to loss of dendrites in human neurons. Am J Hum Genet 2019; 104 (05) 815-834
33 Papandreou A, Schneider RB, Augustine EF. et al. Delineation of the movement disorders associated with FOXG1 mutations. Neurology 2016; 86 (19) 1794-1800
34 Chirico V, Rigoli L, Lacquaniti A. et al. Endocrinopathies, metabolic disorders, and iron overload in major and intermedia thalassemia: serum ferritin as diagnostic and predictive marker associated with liver and cardiac T2* MRI assessment. Eur J Haematol 2015; 94 (05) 404-412
35 Sestito S, Roppa K, Parisi F. et al. The heart in Anderson-Fabry disease. J Biol Regul Homeost Agents 2020; 34 (4, suppl 2): 63-69
36 Ghosh SG, Becker K, Huang H. et al. Biallelic mutations in ADPRHL2, encoding ADP-ribosylhydrolase 3, lead to a degenerative pediatric stress-induced epileptic ataxia syndrome. Am J Hum Genet 2018; 103 (03) 431-439
37 Granata F, Morabito R, Mormina E. et al. 3T double inversion recovery magnetic resonance imaging: diagnostic advantages in the evaluation of cortical development anomalies. Eur J Radiol 2016; 85 (05) 906-914
38 Chimenz R, Manti S, Fede C. et al. Primary nocturnal enuresis in children with allergic rhinitis and severe adenotonsillar hypertrophy: a single center pilot study. J Biol Regul Homeost Agents 2015; 29 (2, suppl 1): 73-79
39 Accogli A, Iacomino M, Pinto F. et al. Novel AMPD2 mutation in pontocerebellar hypoplasia, dysmorphisms, and teeth abnormalities. Neurol Genet 2017; 3 (05) e179
40 Sheldon CA, Paley GL, Xiao R. et al. Pediatric idiopathic intracranial hypertension: age, gender, and anthropometric features at diagnosis in a large, retrospective, multisite cohort. Ophthalmology 2016; 123 (11) 2424-2431
41 Riva A, Gambadauro A, Dipasquale V. et al. Biallelic variants in KIF17 associated with microphthalmia and coloboma spectrum. Int J Mol Sci 2021; 22 (09) 4471
42 Ruggieri M, Polizzi A, Strano S. et al. Mixed vascular nevus syndrome: a report of four new cases and a literature review. Quant Imaging Med Surg 2016; 6 (05) 515-524
43 Salpietro V, Ruggieri M. Pseudotumor cerebri pathophysiology: the likely role of aldosterone. Headache 2014; 54 (07) 1229
44 Casto C, Dipasquale V, Ceravolo I. et al. Prominent and regressive brain developmental disorders associated with Nance-Horan syndrome. Brain Sci 2021; 11 (09) 1150
45 Pavlidou E, Salpietro V, Phadke R. et al. Pontocerebellar hypoplasia type 2D and optic nerve atrophy further expand the spectrum associated with selenoprotein biosynthesis deficiency. Eur J Paediatr Neurol 2016; 20 (03) 483-488
46 Salpietro V, Efthymiou S, Manole A. et al. A loss-of-function homozygous mutation in DDX59 implicates a conserved DEAD-box RNA helicase in nervous system development and function. Hum Mutat 2018; 39 (02) 187-192
47 Shaheen R, Mark P, Prevost CT. et al. Biallelic variants in CTU2 cause DREAM-PL syndrome and impair thiolation of tRNA wobble U34. Hum Mutat 2019; 40 (11) 2108-2120
48 Tassano E, Accogli A, Pavanello M. et al. Interstitial 9p24.3 deletion involving only DOCK8 and KANK1 genes in two patients with non-overlapping phenotypic traits. Eur J Med Genet 2016; 59 (01) 20-25
49 Pedullà M, Miraglia Del Giudice M, Fierro V. et al. Atopy as a risk factor for thyroid autoimmunity in children. J Biol Regul Homeost Agents 2012; 26 (Suppl. 01) S9-S14
50 Niccolini F, Mencacci NE, Yousaf T. et al. PDE10A and ADCY5 mutations linked to molecular and microstructural basal ganglia pathology. Mov Disord 2018; 33 (12) 1961-1965
51 Gramaglia SMC, Cuppari C, Salpietro C. et al. Congenital heart disease in Down syndrome. J Biol Regul Homeost Agents 2020; 34 (4, suppl 2): 31-35
52 Salpietro V, Ruggieri M, Sancetta F. et al. New insights on the relationship between pseudotumor cerebri and secondary hyperaldosteronism in children. J Hypertens 2012; 30 (03) 629-630
53 Mitsumoto H, Turner MR, Ajroud-Driss S. et al; all Delegates of the PLS Conference. Preface: promoting research in PLS: current knowledge and future challenges. Amyotroph Lateral Scler Frontotemporal Degener 2020; 21 (Suppl. 01) 1-2
54 Ruggieri M, Polizzi A, Schepis C. et al. Cutis tricolor: a literature review and report of five new cases. Quant Imaging Med Surg 2016; 6 (05) 525-534
55 Chirico V, Lacquaniti A, Salpietro V, Buemi M, Salpietro C, Arrigo T. Central precocious puberty: from physiopathological mechanisms to treatment. J Biol Regul Homeost Agents 2014; 28 (03) 367-375
56 Loddo I, Cutrupi MC, Concolino D. et al. Cardiac defects in RASopathies: a review of genotype- phenotype correlations. J Biol Regul Homeost Agents 2020; 34 (4, suppl 2): 23-30
57 Valente EM, Marsh SE, Castori M. et al. Distinguishing the four genetic causes of Jouberts syndrome-related disorders. Ann Neurol 2005; 57 (04) 513-519
58 Valente EM, Brancati F, Silhavy JL. et al; International JSRD Study Group. AHI1 gene mutations cause specific forms of Joubert syndrome-related disorders. Ann Neurol 2006; 59 (03) 527-534
59 Valente EM, Logan CV, Mougou-Zerelli S. et al. Mutations in TMEM216 perturb ciliogenesis and cause Joubert, Meckel and related syndromes. Nat Genet 2010; 42 (07) 619-625
60 Brancati F, Barrano G, Silhavy JL. et al; International JSRD Study Group. CEP290 mutations are frequently identified in the oculo-renal form of Joubert syndrome-related disorders. Am J Hum Genet 2007; 81 (01) 104-113
61 Brancati F, Travaglini L, Zablocka D. et al; International JSRD Study Group. RPGRIP1L mutations are mainly associated with the cerebello-renal phenotype of Joubert syndrome-related disorders. Clin Genet 2008; 74 (02) 164-170
62 Brancati F, Iannicelli M, Travaglini L. et al; International JSRD Study Group. MKS3/TMEM67 mutations are a major cause of COACH Syndrome, a Joubert Syndrome related disorder with liver involvement. Hum Mutat 2009; 30 (02) E432-E442
63 Briguglio M, Pinelli L, Giordano L. et al; CBCD Study Group. Pontine tegmental cap dysplasia: developmental and cognitive outcome in three adolescent patients. Orphanet J Rare Dis 2011; 6: 36
64 Arrigoni F, Romaniello R, Peruzzo D. et al. Anterior mesencephalic cap dysplasia: novel brain stem malformative features associated with Joubert syndrome. AJNR Am J Neuroradiol 2017; 38 (12) 2385-2390
65 Enokizono M, Aida N, Niwa T. et al. Neuroimaging findings in Joubert syndrome with C5orf42 gene mutations: a milder form of molar tooth sign and Vermian hypoplasia. J Neurol Sci 2017; 376: 7-12
66 Seylanian Toosi F, Boloursaz S, Abbasi B, Hekmat R, Mortazavi Ardestani R, Mohajerzadeh M. Joubert syndrome; misleading presentation of two cases as pseudo-tumor cerebri and literature review. J Renal Inj Prev 2016; 6 (02) 76-79
67 Hsu CC, Kwan GN, Bhuta S. High-resolution diffusion tensor imaging and tractography in Joubert syndrome: beyond molar tooth sign. Pediatr Neurol 2015; 53 (01) 47-52
68 Accogli A, Addour-Boudrahem N, Srour M. Neurogenesis, neuronal migration, and axon guidance. Handb Clin Neurol 2020; 173: 25-42
69 Manley AT, Maertens PM. The Shepherd's Crook sign: a new neuroimaging pareidolia in Joubert syndrome. J Neuroimaging 2015; 25 (03) 510-512
70 Pugash D, Oh T, Godwin K. et al. Sonographic ‘molar tooth’ sign in the diagnosis of Joubert syndrome. Ultrasound Obstet Gynecol 2011; 38 (05) 598-602
71 Quarello E, Molho M, Garel C. et al. Prenatal abnormal features of the fourth ventricle in Joubert syndrome and related disorders. Ultrasound Obstet Gynecol 2014; 43 (02) 227-232
72 Accogli A, Addour-Boudrahem N, Srour M. Diagnostic approach to cerebellar hypoplasia. Cerebellum 2021; 20 (04) 631-658