Large genotype-phenotype study in carriers of D4Z4 borderline alleles provides guidance for facioscapulohumeral muscular dystrophy diagnosis.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
10 12 2020
Historique:
received: 10 08 2020
accepted: 18 11 2020
entrez: 11 12 2020
pubmed: 12 12 2020
medline: 21 5 2021
Statut: epublish

Résumé

Facioscapulohumeral muscular dystrophy (FSHD) is a myopathy with prevalence of 1 in 20,000. Almost all patients affected by FSHD carry deletions of an integral number of tandem 3.3 kilobase repeats, termed D4Z4, located on chromosome 4q35. Assessment of size of D4Z4 alleles is commonly used for FSHD diagnosis. However, the extended molecular testing has expanded the spectrum of clinical phenotypes. In particular, D4Z4 alleles with 9-10 repeat have been found in healthy individuals, in subjects with FSHD or affected by other myopathies. These findings weakened the strict relationship between observed phenotypes and their underlying genotypes, complicating the interpretation of molecular findings for diagnosis and genetic counseling. In light of the wide clinical variability detected in carriers of D4Z4 alleles with 9-10 repeats, we applied a standardized methodology, the Comprehensive Clinical Evaluation Form (CCEF), to describe and characterize the phenotype of 244 individuals carrying D4Z4 alleles with 9-10 repeats (134 index cases and 110 relatives). The study shows that 54.5% of index cases display a classical FSHD phenotype with typical facial and scapular muscle weakness, whereas 20.1% present incomplete phenotype with facial weakness or scapular girdle weakness, 6.7% display minor signs such as winged scapula or hyperCKemia, without functional motor impairment, and 18.7% of index cases show more complex phenotypes with atypical clinical features. Family studies revealed that 70.9% of relatives carrying 9-10 D4Z4 reduced alleles has no motor impairment, whereas a few relatives (10.0%) display a classical FSHD phenotype. Importantly all relatives of index cases with no FSHD phenotype were healthy carriers. These data establish the low penetrance of D4Z4 alleles with 9-10 repeats. We recommend the use of CCEF for the standardized clinical assessment integrated by family studies and further molecular investigation for appropriate diagnosis and genetic counseling. Especially in presence of atypical phenotypes and/or sporadic cases with all healthy relatives is not possible to perform conclusive diagnosis of FSHD, but all these cases need further studies for a proper diagnosis, to search novel causative genetic defects or investigate environmental factors or co-morbidities that may trigger the pathogenic process. These evidences are also fundamental for the stratification of patients eligible for clinical trials. Our work reinforces the value of large genotype-phenotype studies to define criteria for clinical practice and genetic counseling in rare diseases.

Identifiants

pubmed: 33303865
doi: 10.1038/s41598-020-78578-7
pii: 10.1038/s41598-020-78578-7
pmc: PMC7730397
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

21648

Subventions

Organisme : Telethon
ID : GUP13012
Pays : Italy

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Auteurs

Giulia Ricci (G)

Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy.
Department of Clinical and Experimental Medicine, Neurological Clinic, University of Pisa, Pisa, Italy.

Fabiano Mele (F)

Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Monica Govi (M)

Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Lucia Ruggiero (L)

Department of Neurosciences, Reproductive and Odontostomatological Sciences, University Federico II of Naples, Naples, Italy.

Francesco Sera (F)

Department of Statistics, Computer Science and Applications "G. Parenti", University of Florence, Florence, Italy.

Liliana Vercelli (L)

Department of Neuroscience, Center for Neuromuscular Diseases, University of Turin, Turin, Italy.

Cinzia Bettio (C)

Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Via G. Campi 287, 41125, Modena, Italy.
Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy.

Lucio Santoro (L)

Department of Neurosciences, Reproductive and Odontostomatological Sciences, University Federico II of Naples, Naples, Italy.

Tiziana Mongini (T)

Department of Neuroscience, Center for Neuromuscular Diseases, University of Turin, Turin, Italy.

Luisa Villa (L)

Neuromuscular Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Dino Ferrari Center, University of Milan, Milan, Italy.

Maurizio Moggio (M)

Neuromuscular Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Dino Ferrari Center, University of Milan, Milan, Italy.

Massimiliano Filosto (M)

Neurology Clinic, Spedali Civili Hospital, Brescia, Italy.

Marina Scarlato (M)

INSPE and Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Stefano C Previtali (SC)

INSPE and Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy.

Silvia Maria Tripodi (SM)

Department of Neurosciences, University of Padua, Padua, Italy.

Elena Pegoraro (E)

Department of Neurosciences, University of Padua, Padua, Italy.

Roberta Telese (R)

Center for Neuromuscular Disease, CeSI, University "G. D'Annunzio", Chieti, Italy.

Antonio Di Muzio (A)

Center for Neuromuscular Disease, CeSI, University "G. D'Annunzio", Chieti, Italy.

Carmelo Rodolico (C)

Department of Neurosciences, Policlinico "G. Martino", University of Messina, Messina, Italy.

Elisabetta Bucci (E)

Department of Neuroscience, Mental Health and Sensory Organs, S. Andrea Hospital, University of Rome "La Sapienza", Rome, Italy.

Giovanni Antonini (G)

Department of Neuroscience, Mental Health and Sensory Organs, S. Andrea Hospital, University of Rome "La Sapienza", Rome, Italy.

Maria Grazia D'Angelo (MG)

Department of Neurorehabilitation, IRCCS Eugenio Medea, Bosisio Parini, Italy.

Angela Berardinelli (A)

Unit of Child Neurology and Psychiatry, IRCCS "C. Mondino" Foundation, Pavia, Italy.

Lorenzo Maggi (L)

IRCCS Foundation, C. Besta Neurological Institute, Milan, Italy.

Rachele Piras (R)

ASL8, Centro Sclerosi Multipla, Cagliari, Italy.

Maria Antonietta Maioli (MA)

ASL8, Centro Sclerosi Multipla, Cagliari, Italy.

Gabriele Siciliano (G)

Department of Clinical and Experimental Medicine, Neurological Clinic, University of Pisa, Pisa, Italy.

Giuliano Tomelleri (G)

Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Via G. Campi 287, 41125, Modena, Italy.
Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy.

Corrado Angelini (C)

IRCCS San Camillo, Venice, Italy.

Rossella Tupler (R)

Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy. rossella.tupler@unimore.it.
Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Via G. Campi 287, 41125, Modena, Italy. rossella.tupler@unimore.it.
Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy. rossella.tupler@unimore.it.
Department of Molecular Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, USA. rossella.tupler@unimore.it.
Li Weibo Institute for Rare Diseases Research at the University of Massachusetts Medical School, Worcester, USA. rossella.tupler@unimore.it.

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