Management of seizures in patients with primary mitochondrial diseases: consensus statement from the InterERNs Mitochondrial Working Group.

consensus epilepsy management mitochondrial diseases recommendations

Journal

European journal of neurology
ISSN: 1468-1331
Titre abrégé: Eur J Neurol
Pays: England
ID NLM: 9506311

Informations de publication

Date de publication:
04 Apr 2024
Historique:
revised: 27 02 2024
received: 31 10 2023
accepted: 28 02 2024
medline: 5 4 2024
pubmed: 5 4 2024
entrez: 5 4 2024
Statut: aheadofprint

Résumé

Primary mitochondrial diseases (PMDs) are common inborn errors of energy metabolism, with an estimated prevalence of one in 4300. These disorders typically affect tissues with high energy requirements, including heart, muscle and brain. Epilepsy may be the presenting feature of PMD, can be difficult to treat and often represents a poor prognostic feature. The aim of this study was to develop guidelines and consensus recommendations on safe medication use and seizure management in mitochondrial epilepsy. A panel of 24 experts in mitochondrial medicine, pharmacology and epilepsy management of adults and/or children and two patient representatives from seven countries was established. Experts were members of five different European Reference Networks, known as the Mito InterERN Working Group. A Delphi technique was used to allow the panellists to consider draft recommendations on safe medication use and seizure management in mitochondrial epilepsy, using two rounds with predetermined levels of agreement. A high level of consensus was reached regarding the safety of 14 out of all 25 drugs reviewed, resulting in endorsement of National Institute for Health and Care Excellence guidelines for seizure management, with some modifications. Exceptions including valproic acid in POLG disease, vigabatrin in patients with γ-aminobutyric acid transaminase deficiency and topiramate in patients at risk for renal tubular acidosis were highlighted. These consensus recommendations describe our intent to improve seizure control and reduce the risk of drug-related adverse events in individuals living with PMD-related epilepsy.

Sections du résumé

BACKGROUND AND PURPOSE OBJECTIVE
Primary mitochondrial diseases (PMDs) are common inborn errors of energy metabolism, with an estimated prevalence of one in 4300. These disorders typically affect tissues with high energy requirements, including heart, muscle and brain. Epilepsy may be the presenting feature of PMD, can be difficult to treat and often represents a poor prognostic feature. The aim of this study was to develop guidelines and consensus recommendations on safe medication use and seizure management in mitochondrial epilepsy.
METHODS METHODS
A panel of 24 experts in mitochondrial medicine, pharmacology and epilepsy management of adults and/or children and two patient representatives from seven countries was established. Experts were members of five different European Reference Networks, known as the Mito InterERN Working Group. A Delphi technique was used to allow the panellists to consider draft recommendations on safe medication use and seizure management in mitochondrial epilepsy, using two rounds with predetermined levels of agreement.
RESULTS RESULTS
A high level of consensus was reached regarding the safety of 14 out of all 25 drugs reviewed, resulting in endorsement of National Institute for Health and Care Excellence guidelines for seizure management, with some modifications. Exceptions including valproic acid in POLG disease, vigabatrin in patients with γ-aminobutyric acid transaminase deficiency and topiramate in patients at risk for renal tubular acidosis were highlighted.
CONCLUSIONS CONCLUSIONS
These consensus recommendations describe our intent to improve seizure control and reduce the risk of drug-related adverse events in individuals living with PMD-related epilepsy.

Identifiants

pubmed: 38576261
doi: 10.1111/ene.16275
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e16275

Subventions

Organisme : This project has received funding from the European Joint Programme on Rare Diseases (EJP RD). The EJP RD initiative has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement N°825575

Informations de copyright

© 2024 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.

Références

Ng YS, Bindoff LA, Gorman GS, et al. Mitochondrial disease in adults: recent advances and future promise. Lancet Neurol. 2021;20:573‐584.
Rahman S. Mitochondrial diseases and status epilepticus. Epilepsia. 2018;59(Suppl 2):70‐77.
Lopriore P, Gomes F, Montano V, Siciliano G, Mancuso M. Mitochondrial epilepsy, a challenge for neurologists. Int J Mol Sci. 2022;23:13216.
Bindoff LA, Engelsen BA. Mitochondrial diseases and epilepsy. Epilepsia. 2012;53(Suppl 4):92‐97.
Whittaker RG, Devine HE, Gorman GS, et al. Epilepsy in adults with mitochondrial disease: a cohort study. Ann Neurol. 2015;78:949‐957.
Guerrini R, Balestrini S, Wirrell EC, Walker MC. Monogenic epilepsies: disease mechanisms, clinical phenotypes, and targeted therapies. Neurology. 2021;97:817‐831.
Mancuso M, McFarland R, Klopstock T, Hirano M, consortium on Trial Readiness in Mitochondrial Myopathies. International workshop: outcome measures and clinical trial readiness in primary mitochondrial myopathies in children and adults. Consensus recommendations. 16–18 November 2016, Rome, Italy. Neuromuscul Disord. 2017;27:1126‐1137.
De Vries MC, Brown DA, Allen ME, et al. Safety of drug use in patients with a primary mitochondrial disease: an international Delphi‐based consensus. J Inherit Metab Dis. 2020;43:800‐818. doi:10.1002/jimd.12196
Koene S, van Bon L, Bertini E, et al. Outcome measures for children with mitochondrial disease: consensus recommendations for future studies from a Delphi‐based international workshop. J Inherit Metab Dis. 2018;41:1267‐1273.
Ng YS, Bindoff LA, Gorman GS, et al. Consensus‐based statements for the management of mitochondrial stroke‐like episodes. Wellcome Open Res. 2019;4:201.
Ebihara T, Nagatomo T, Sugiyama Y, et al. Neonatal‐onset mitochondrial disease: clinical features, molecular diagnosis and prognosis. Arch Dis Child Fetal Neonatal Ed. 2022;107:329‐334.
Pressler RM, Abend NS, Auvin S, et al. Treatment of seizures in the neonate: guidelines and consensus‐based recommendations—special report from the ILAE task force on neonatal seizures. Epilepsia. 2023;64:2550‐2570.
de Winter JCF, Dodou D. Five‐point Likert items: t test versus Mann–Whitney–Wilcoxon. Pract Assess Res Eval. 2010;15:1‐10.
Overview | Epilepsies in children, young people and adults | Guidance | NICE. 2022. https://www.nice.org.uk/guidance/ng217.
Minicucci F, Ferlisi M, Brigo F, et al. Management of status epilepticus in adults. Position paper of the Italian League Against Epilepsy. Epilepsy Behav EB. 2020;102:106675.

Auteurs

Michelangelo Mancuso (M)

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

Maria T Papadopoulou (MT)

Department of Pediatric Clinical Epileptology, Sleep Disorders and Functional Neurology, University Hospital of Lyon, Member of the ERN EpiCARE, Lyon, France.

Yi Shiau Ng (YS)

Wellcome Centre for Mitochondrial Research, Translational and Clinical Research Institute AND National Institute for Health and Care Research (NIHR) Newcastle Biomedical Research Centre (BRC), Newcastle University, Newcastle upon Tyne, UK.
NHS Highly Specialised Service for Rare Mitochondrial Disorders, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

Anna Ardissone (A)

Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Marcello Bellusci (M)

Reference Center for Inherited Metabolic Disorders MetabERN, Mitochondrial Disorders Research Group (imas12), '12 de Octubre' University Hospital, Madrid, Spain.

Enrico Bertini (E)

Research Unit of Neuromuscular Disease, Translational Pediatrics and Clinical Genetics, Bambino Gesu' Children's Research Hospital, IRCCS, Rome, Italy.

Lidia Di Vito (L)

IRCCS Istituto delle Scienze Neurologiche di Bologna, Full Member of the European Reference Network for Rare and Complex Epilepsies (EpiCARE), Bologna, Italy.

Teresinha Evangelista (T)

Department of Neuropathology, Functional Unit of Neuromuscular pathology and Department of Neuromyology, Institute of Myology, EURO-NMD coordination, Pitié-Salpêtrière Hospital, APHP Sorbonne University, Paris, France.

Carmen Fons (C)

Epilepsy and Neurometabolics Units, Pediatric Neurology Department, Hospital Sant Joan de Déu, Institut de Recerca Sant Joan de Déu, Barcelona, Spain.

Omar Hikmat (O)

Department of Paediatrics and Adolescent Medicine, Haukeland University Hospital, Bergen and Department of Clinical Medicine (K1), University of Bergen, Bergen, Norway.

Rita Horvath (R)

Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.

Thomas Klopstock (T)

Department of Neurology, Friedrich-Baur-Institute, LMU University Hospital, Ludwig-Maximilians-Universität München, Munich, Germany.
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Cornelia Kornblum (C)

Department of Neurology, Section of Neuromuscular Diseases, University Hospital Bonn, Bonn, Germany.

Costanza Lamperti (C)

Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Laura Licchetta (L)

IRCCS Istituto delle Scienze Neurologiche di Bologna, Full Member of the European Reference Network for Rare and Complex Epilepsies (EpiCARE), Bologna, Italy.

Maria Judit Molnar (MJ)

Institute of Genomic Medicine and Rare Disorders, Semmelweis University, Budapest, Hungary.

Kristin N Varhaug (KN)

Department of Neurology, Haukeland University Hospital, Bergen, Norway.

Mar O'Callaghan (M)

Epilepsy and Neurometabolics Units, Pediatric Neurology Department, Hospital Sant Joan de Déu, Institut de Recerca Sant Joan de Déu, Barcelona, Spain.

Ronit M Pressler (RM)

UCL Great Ormond Street Institute of Child Health, London, UK.
Great Ormond Street Hospital for Children, London, UK.

Manuel Schiff (M)

Reference Center for Mitochondrial Disorders (CARAMMEL) and Reference Center for Inborn Errors of Metabolism, Department of Pediatrics, Necker-Enfants-Malades Hospital, Assistance Publique-Hôpitaux de Paris, University of Paris-Cité, MetabERN, Paris, France.
INSERM UMRS_1163, Imagine Institute, Paris, France.

Serenella Servidei (S)

Dipartimento di Neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, Rome, Italy.
Dipartimento Di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.

Nora Szabo (N)

Saint John's Hospital, Child Epilepsy Centre, Budapest, Hungary.

Gráinne S Gorman (GS)

Wellcome Centre for Mitochondrial Research, Translational and Clinical Research Institute AND National Institute for Health and Care Research (NIHR) Newcastle Biomedical Research Centre (BRC), Newcastle University, Newcastle upon Tyne, UK.
NHS Highly Specialised Service for Rare Mitochondrial Disorders, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

J Helen Cross (JH)

UCL Great Ormond Street Institute of Child Health, London, UK.
Great Ormond Street Hospital for Children, London, UK.

Shamima Rahman (S)

UCL Great Ormond Street Institute of Child Health, London, UK.
Great Ormond Street Hospital for Children, London, UK.

Classifications MeSH