Assessing the landscape of STXBP1-related disorders in 534 individuals


Por: Xian J, Parthasarathy S, Ruggiero SM, Balagura G, Fitch E, Helbig K, Gan J, Ganesan S, Kaufman MC, Ellis CA, Lewis-Smith D, Galer P, Cunningham K, O'Brien M, Cosico M, Baker K, Darling A, Veiga de Goes F, El Achkar CM, Doering JH, Furia F, Garcia-Cazorla A, Gardella E, Geertjens L, Klein C, Kolesnik-Taylor A, Lammertse H, Lee J, Mackie A, Misra-Isrie M, Olson H, Sexton E, Sheidley B, Smith L, Sotero L, Stamberger H, Syrbe S, Thalwitzer KM, van Berkel A, van Haelst M, Yuskaitis C, Weckhuysen S, Prosser B, Son Rigby C, Demarest S, Pierce S, Zhang Y, Møller RS, Bruining H, Poduri A, Zara F, Verhage M, Striano P and Helbig I

Publicada: 3 jun 2022 Ahead of Print: 1 feb 2022
Resumen:
Disease-causing variants in STXBP1 are among the most common genetic causes of neurodevelopmental disorders. However, the phenotypic spectrum in STXBP1-related disorders is wide and clear correlations between variant type and clinical features have not been observed so far. Here, we harmonized clinical data across 534 individuals with STXBP1-related disorders and analysed 19 973 derived phenotypic terms, including phenotypes of 253 individuals previously unreported in the scientific literature. The overall phenotypic landscape in STXBP1-related disorders is characterized by neurodevelopmental abnormalities in 95% and seizures in 89% of individuals, including focal-onset seizures as the most common seizure type (47%). More than 88% of individuals with STXBP1-related disorders have seizure onset in the first year of life, including neonatal seizure onset in 47%. Individuals with protein-truncating variants and deletions in STXBP1 (n = 261) were almost twice as likely to present with West syndrome and were more phenotypically similar than expected by chance. Five genetic hotspots with recurrent variants were identified in more than 10 individuals, including p.Arg406Cys/His (n = 40), p.Arg292Cys/His/Leu/Pro (n = 30), p.Arg551Cys/Gly/His/Leu (n = 24), p.Pro139Leu (n = 12), and p.Arg190Trp (n = 11). None of the recurrent variants were significantly associated with distinct electroclinical syndromes, single phenotypic features, or showed overall clinical similarity, indicating that the baseline variability in STXBP1-related disorders is too high for discrete phenotypic subgroups to emerge. We then reconstructed the seizure history in 62 individuals with STXBP1-related disorders in detail, retrospectively assigning seizure type and seizure frequency monthly across 4433 time intervals, and retrieved 251 anti-seizure medication prescriptions from the electronic medical records. We demonstrate a dynamic pattern of seizure control and complex interplay with response to specific medications particularly in the first year of life when seizures in STXBP1-related disorders are the most prominent. Adrenocorticotropic hormone and phenobarbital were more likely to initially reduce seizure frequency in infantile spasms and focal seizures compared to other treatment options, while the ketogenic diet was most effective in maintaining seizure freedom. In summary, we demonstrate how the multidimensional spectrum of phenotypic features in STXBP1-related disorders can be assessed using a computational phenotype framework to facilitate the development of future precision-medicine approaches.

Filiaciones:
Xian J:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

 Neuroscience Program, University of Pennsylvania, Philadelphia, PA 19104, USA

Parthasarathy S:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

 Department of Biology, The College of New Jersey, Ewing Township, NJ 08618, USA

Ruggiero SM:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

Balagura G:
 Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, and Maternal and Child Health, University of Genoa, Genoa, Italy

 Pediatric Neurology and Muscular Diseases Unit, IRCCS 'G. Gaslini' Institute, Genoa, Italy

Fitch E:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

Helbig K:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

Gan J:
 Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, China

 Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Chengdu, China

Ganesan S:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

Kaufman MC:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

Ellis CA:
 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

 Department of Neurology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA

Lewis-Smith D:
 Translational and Clinical Research Institute, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK

 Royal Victoria Infirmary, Newcastle-upon-Tyne NE1 4LP, UK

Galer P:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

 Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, PA 19104, USA

Cunningham K:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

O'Brien M:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Lewis Katz School of Medicine, Temple University, Philadelphia, PA 19140, USA

Cosico M:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

Baker K:
 MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK

Darling A:
 Pediatric Neurology Department, Hospital Sant Joan de Déu, University of Barcelona, Barcelona, Spain

Veiga de Goes F:
 Department of Pediatrics and Pediatric Neurology Laboratory, Instituto Fernandes Figueira, Rio de Janeiro 22250-020, Brazil

El Achkar CM:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Doering JH:
 Division of Pediatric Epileptology, Centre for Pediatric and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany

Furia F:
 Department of Clinical Neurophysiology, Danish Epilepsy Center Filadelfia, Dianalund 4293, Denmark

Garcia-Cazorla A:
 Pediatric Neurology Department, Hospital Sant Joan de Déu, University of Barcelona, Barcelona, Spain

Gardella E:
 Department of Clinical Neurophysiology, Danish Epilepsy Center Filadelfia, Dianalund 4293, Denmark

Geertjens L:
 Department of Child and Adolescent Psychiatry, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands

Klein C:
 Departments of Pediatrics and Neurology, Children's Hospital Colorado, Aurora, CO 80045, USA

Kolesnik-Taylor A:
 MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK

Lammertse H:
 Department of Human Genetics, Center for Neurogenomics and Cognitive Research (CNCR), Amsterdam University Medical Center, de Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

Lee J:
 Department of Pediatrics, Samsung Medical Center, School of Medicine, Sungkyunkwan University, Seoul, Republic of Korea

Mackie A:
 Departments of Pediatrics and Neurology, Children's Hospital Colorado, Aurora, CO 80045, USA

Misra-Isrie M:
 Department of Human Genetics, Center for Neurogenomics and Cognitive Research (CNCR), Amsterdam University Medical Center, de Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

Olson H:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Sexton E:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Sheidley B:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Smith L:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Sotero L:
 Department of Pediatrics and Pediatric Neurology Laboratory, Instituto Fernandes Figueira, Rio de Janeiro 22250-020, Brazil

Stamberger H:
 Division of Neurology, University Hospital Antwerp, Antwerp, Belgium

 Applied & Translational Neurogenomics Group, VIB Center for Molecular Neurology, VIB, Antwerp, Belgium

Syrbe S:
 Division of Pediatric Epileptology, Centre for Pediatric and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany

Thalwitzer KM:
 Division of Pediatric Epileptology, Centre for Pediatric and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany

van Berkel A:
 Department of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

van Haelst M:
 Department of Human Genetics, Center for Neurogenomics and Cognitive Research (CNCR), Amsterdam University Medical Center, de Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

Yuskaitis C:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Weckhuysen S:
 Division of Neurology, University Hospital Antwerp, Antwerp, Belgium

 Applied & Translational Neurogenomics Group, VIB Center for Molecular Neurology, VIB, Antwerp, Belgium

 Translational Neurosciences, Faculty of Medicine and Health Science, University of Antwerp, Antwerp, Belgium

Prosser B:
 Department of Physiology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA

Son Rigby C:
 STXBP1 Foundation, Apex, NC 27539, USA

Demarest S:
 Departments of Pediatrics and Neurology, Children's Hospital Colorado, Aurora, CO 80045, USA

Pierce S:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

Zhang Y:
 Department of Pediatrics, Beijing University First Hospital, Beijing, China

Møller RS:
 Department of Clinical Neurophysiology, Danish Epilepsy Center Filadelfia, Dianalund 4293, Denmark

Bruining H:
 Department of Child and Adolescent Psychiatry, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands

Poduri A:
 Division of Epilepsy and Clinical Neurophysiology and Epilepsy Genetics Program, Department of Neurology, Boston Children's Hospital, Boston, MA, USA

Zara F:
 Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, and Maternal and Child Health, University of Genoa, Genoa, Italy

 Unit of Medical Genetics, IRCCS Istituto Giannina Gaslini, Genova, Italy

Verhage M:
 Department of Human Genetics, Center for Neurogenomics and Cognitive Research (CNCR), Amsterdam University Medical Center, de Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

 Department of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands

Striano P:
 Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, and Maternal and Child Health, University of Genoa, Genoa, Italy

 Pediatric Neurology and Muscular Diseases Unit, IRCCS 'G. Gaslini' Institute, Genoa, Italy

Helbig I:
 Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA

 Department of Biomedical and Health Informatics (DBHi), Children's Hospital of Philadelphia, Philadelphia, PA 19146, USA

 Department of Neurology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA 19104, USA
ISSN: 00068950





BRAIN
Editorial
OXFORD UNIV PRESS, GREAT CLARENDON ST, OXFORD OX2 6DP, ENGLAND, Reino Unido
Tipo de documento: Article
Volumen: 145 Número: 5
Páginas: 1668-1683
WOS Id: 000767707300001
ID de PubMed: 35190816
imagen Green Submitted, gold

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