BCKDK deficiency: a treatable neurodevelopmental disease amenable to newborn screening


Por: Tangeraas T, Ribeiro J, Backe PH, De Oyarzabal-Sanz AL, Neugebauer J, Weinhold N, Boemer F, Debray FG, Ozturk-Hism B, Evren G, Tuba EF, Ummuhan O, Footitt E, Davison J, Martinez C, Bueno C, Machado I, Rodríguez-Pombo P, Al-Sannaa N, de los Santos MM, Muchart-Lopez J, Ozturkmen-Akay H, Karaca M, Tekin M, Pajares S, Ormazabal-Herrero A, Stoway SD, Artuch-Iriberri R, Dixon M, Mørkrid L and Garcia-Cazorla A

Publicada: 3 jul 2023 Ahead of Print: 1 mar 2023
Resumen:
There are few causes of treatable neurodevelopmental diseases described to date. Branched-chain ketoacid dehydrogenase kinase (BCKDK) deficiency causes branched-chain amino acid (BCAA) depletion and is linked to a neurodevelopmental disorder characterized by autism, intellectual disability and microcephaly. We report the largest cohort of patients studied, broadening the phenotypic and genotypic spectrum. Moreover, this is the first study to present newborn screening findings and mid-term clinical outcome. In this cross-sectional study, patients with a diagnosis of BCKDK deficiency were recruited via investigators' practices through a MetabERN initiative. Clinical, biochemical and genetic data were collected. Dried blood spot (DBS) newborn screening (NBS) amino acid profiles were retrieved from collaborating centres and compared to a healthy newborn reference population. Twenty-one patients with BCKDK mutations were included from 13 families. Patients were diagnosed between 8 months and 16 years (mean: 5.8 years, 43% female). At diagnosis, BCAA levels (leucine, valine and isoleucine) were below reference values in plasma and in CSF. All patients had global neurodevelopmental delay; 18/21 had gross motor function (GMF) impairment with GMF III or worse in 5/18, 16/16 intellectual disability, 17/17 language impairment, 12/17 autism spectrum disorder, 9/21 epilepsy, 12/15 clumsiness, 3/21 had sensorineural hearing loss and 4/20 feeding difficulties. No microcephaly was observed at birth, but 17/20 developed microcephaly during follow-up. Regression was reported in six patients. Movement disorder was observed in 3/21 patients: hyperkinetic movements (1), truncal ataxia (1) and dystonia (2). After treatment with a high-protein diet (>= 2 g/kg/day) and BCAA supplementation (100-250 mg/kg/day), plasma BCAA increased significantly (P < 0.001), motor functions and head circumference stabilized/improved in 13/13 and in 11/15 patients, respectively. Among cases with follow-up data, none of the three patients starting treatment before 2 years of age developed autism at follow-up. The patient with the earliest age of treatment initiation (8 months) showed normal development at 3 years of age. NBS in DBS identified BCAA levels significantly lower than those of the normal population. This work highlights the potential benefits of dietetic treatment, in particular early introduction of BCAA. Therefore, it is of utmost importance to increase awareness about this treatable disease and consider it as a candidate for early detection by NBS programmes. Tangeraas et al. describe the largest series of BCKDK deficiency patients to date, including responses to dietetic treatment. Early introduction of BCAA ameliorates the BCKDK deficiency phenotype. This treatable neurodevelopmental disease should be considered for inclusion in newborn screening programmes.

Filiaciones:
Tangeraas T:
 Paediatric and Adolescent Medicine, Oslo University Hospital, 0424, Oslo, Norway

 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

Ribeiro J:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Neurometabolic Unit and Synaptic Metabolism Laboratory, Neurology Department Sant Joan de Déu Hospital, IPR, Barcelona 08950, Spain

 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain

Backe PH:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Department of Medical Biochemistry, Oslo University Hospital-Rikshospitalet, PO Box 4950 Nydalen, OUS HF Rikshospitalet, 0424 Oslo  Norway

 Department of Microbiology, Clinic for Diagnostics and Intervention, Oslo University Hospital, Rikshospitalet, PO Box 4950, Nydalen, N-0424, Oslo, Norway

De Oyarzabal-Sanz AL:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Neurometabolic Unit and Synaptic Metabolism Laboratory, Neurology Department Sant Joan de Déu Hospital, IPR, Barcelona 08950, Spain

 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain

Neugebauer J:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Department of Pediatric Gastroenterology, Nephrology and Metabolic Medicine. Charité - Universitätsmedizin Berlin, Berlin 13353, Germany

 Center for Chronically Sick Children, Charité - Universitätsmedizin Berlin, Berlin 13353, Germany

Weinhold N:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Department of Pediatric Gastroenterology, Nephrology and Metabolic Medicine. Charité - Universitätsmedizin Berlin, Berlin 13353, Germany

 Center for Chronically Sick Children, Charité - Universitätsmedizin Berlin, Berlin 13353, Germany

Boemer F:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Biochemical Genetics Laboratory, Human Genetics, CHU of Liege, University of Liège, Liège, 4000, Belgium

Debray FG:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Department of Human Genetics, CHU of Liege, University of Liège, Liège, 4000, Belgium

Ozturk-Hism B:
 Department of Pediatric Metabolic Diseases, Marmara University School of Medicine, Istanbul 34854, Turkey

Evren G:
 Medical Genetics Department, University of Harran  63000 Sanliurfa, Turkey

Tuba EF:
 Pediatric Metabolism Department, Ankara University School of Medicine, 06100 Ankara, Turkey

Ummuhan O:
 Pediatric Metabolism Department, Ankara University School of Medicine, 06100 Ankara, Turkey

Footitt E:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Metabolic Medicine Department, Great Ormond Street Hospital for Children, London WC1N 3JH, UK

 NIHR Great Ormond Street Hospital Biomedical Research Centre (NIHR GOSH BRC), London WC1N 3JH, UK

Davison J:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Metabolic Medicine Department, Great Ormond Street Hospital for Children, London WC1N 3JH, UK

 NIHR Great Ormond Street Hospital Biomedical Research Centre (NIHR GOSH BRC), London WC1N 3JH, UK

Martinez C:
 Department of Pediatrics and Psychiatry, The Mount Sinai Hospital, New York 1468, USA

Bueno C:
 Neurology Department, Clinical Hospital of the Faculty of Medicine, University of São Paulo, São Paulo 05403-010, Brazil

Machado I:
 Hospital Universitario Clínico San Cecilio, Granada, 18016, Spain

Rodríguez-Pombo P:
 Centro de Diagnóstico de Enfermedades Moleculares, Centro de Biología Molecular Severo Ochoa, CBM-CSIC, Departamento de Biología Molecular, Institute for Molecular Biology-IUBM, Universidad Autónoma Madrid, CIBERER, IDIPAZ, 28049 Madrid, Spain

Al-Sannaa N:
 Pediatric Services Division, Johns Hopkins Aramco Healthcare, Dhahran 34465, Saudi Arabia

de los Santos MM:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain

 Neurometabolic Unit, Gastroenterology and Nutrition Department, Sant Joan de Déu Hospital, Barcelona 08950, Spain

Muchart-Lopez J:
 Institut de Recerca Sant Joan de Déu, Hospital Sant Joan de Déu, Pediatric Radiology Department Esplugues de Llobregat, 08950 Barcelona, Spain

Ozturkmen-Akay H:
 Radiology Department, Baskent University School of Medicine, Ankara 06790, Turkey

Karaca M:
 Pediatric Metabolic Diseases Department, University of Harran, Sanliurfa 63000, Turkey

Tekin M:
 Dr. John T. Macdonald Foundation Department of Human Genetics and John P.Hussman Institute for Human Genomics, University of Miami Miller School of Medicine, Miami 33136, USA

Pajares S:
 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain

 Section of Inborn Errors of Metabolism-IBC, Department of Biochemistry and Molecular Genetics, Hospital Clínic, Barcelona 08036, Spain

Ormazabal-Herrero A:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain

 Clinical Biochemistry Department, Sant Joan de Déu Hospital, Barcelona 08950, Spain

Stoway SD:
 Norwegian National Unit for Newborn Screening, Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo 0424, Norway

 Biochemical Genetics Laboratory, Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester 55905, USA

Artuch-Iriberri R:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain

 Clinical Biochemistry Department, Sant Joan de Déu Hospital, Barcelona 08950, Spain

Dixon M:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Dietetics, Great Ormond Street Hospital for Children, NHS Foundation Trust, London, WC1N, 3JH, UK

Mørkrid L:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Department of Medical Biochemistry, Oslo University Hospital-Rikshospitalet, PO Box 4950 Nydalen, OUS HF Rikshospitalet, 0424 Oslo  Norway

 Institute of Clinical Medicine, University of Oslo, PO Box 4950, Nydalen, N-0424, Norway

Garcia-Cazorla A:
 European Reference Network for Hereditary Metabolic Diseases (MetabERN)

 Neurometabolic Unit and Synaptic Metabolism Laboratory, Neurology Department Sant Joan de Déu Hospital, IPR, Barcelona 08950, Spain

 Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid 28029, Spain
ISSN: 00068950





BRAIN
Editorial
OXFORD UNIV PRESS, GREAT CLARENDON ST, OXFORD OX2 6DP, ENGLAND, Reino Unido
Tipo de documento: Article
Volumen: 146 Número: 7
Páginas: 3003-3013
WOS Id: 000951560400001
ID de PubMed: 36729635
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