NEXMIF encephalopathy: an X-linked disorder with male and female phenotypic patterns

doi:10.1038/s41436-020-00988-9

. 2021 Feb;23(2):363-373.

doi: 10.1038/s41436-020-00988-9. Epub 2020 Nov 4.

NEXMIF encephalopathy: an X-linked disorder with male and female phenotypic patterns

Hannah Stamberger^#^{1

2}, Trine B Hammer^#^{3

4}, Elena Gardella^{3

5}, Danique R M Vlaskamp^{1

6

7}, Birgitte Bertelsen⁸, Simone Mandelstam^{9

10

11

12

13}, Iris de Lange¹⁴, Jing Zhang¹⁵, Candace T Myers¹⁶, Christina Fenger³, Zaid Afawi¹⁷, Edith P Almanza Fuerte¹⁶, Danielle M Andrade¹⁸, Yunus Balcik¹⁹, Bruria Ben Zeev^{20

21}, Mark F Bennett^{1

22

23}, Samuel F Berkovic¹, Bertrand Isidor²⁴, Arjan Bouman²⁵, Eva Brilstra¹⁴, Øyvind L Busk²⁶, Anita Cairns²⁷, Roseline Caumes²⁸, Nicolas Chatron²⁹, Russell C Dale³⁰, Christa de Geus³¹, Patrick Edery^{29

32}, Deepak Gill³⁰, Jacob Bie Granild-Jensen³³, Lauren Gunderson³⁴, Boudewijn Gunning³⁵, Gali Heimer^{20

21}, Johan R Helle²⁶, Michael S Hildebrand^{1

10}, Georgie Hollingsworth¹, Volodymyr Kharytonov³⁶, Eric W Klee^{34

37}, Bobby P C Koeleman¹⁴, David A Koolen³⁸, Christian Korff³⁹, Sébastien Küry²⁴, Gaetan Lesca²⁹, Dorit Lev^{21

40}, Richard J Leventer^{9

10

11}, Mark T Mackay^{9

10

11}, Erica L Macke³⁷, Meriel McEntagart⁴¹, Shekeeb S Mohammad³⁰, Pauline Monin²⁹, Martino Montomoli⁴², Eva Morava^{34

37}, Sebastien Moutton^{43

44}, Alison M Muir¹⁶, Elena Parrini⁴², Peter Procopis^{30

45}, Emmanuelle Ranza⁴⁶, Laura Reed⁴⁷, Philipp S Reif¹⁹, Felix Rosenow¹⁹, Massimiliano Rossi^{29

32}, Lynette G Sadleir⁴⁸, Tara Sadoway¹⁸, Helenius J Schelhaas³⁵, Amy L Schneider¹, Krati Shah⁴⁹, Ruth Shalev⁵⁰, Sanjay M Sisodiya⁵¹, Thomas Smol⁵², Connie T R M Stumpel⁵³, Kyra Stuurman²⁵, Joseph D Symonds^{54

55}, Frederic Tran Mau-Them^{56

57}, Nienke Verbeek¹⁴, Judith S Verhoeven⁵⁸, Geoffrey Wallace^{27

59}, Keren Yosovich⁶⁰, Yuri A Zarate⁶¹, Ayelet Zerem^{21

62}, Sameer M Zuberi^{54

55}, Renzo Guerrini⁴², Heather C Mefford¹⁶, Chirag Patel⁶³, Yue-Hua Zhang¹⁵, Rikke S Møller^#^{3

5}, Ingrid E Scheffer^#^{64

65

66

67

68}

Affiliations

¹ Epilepsy Research Centre, Department of Medicine, Austin Health, University of Melbourne, Melbourne, VIC, Australia.
² Applied and Translational Neurogenomics group, Center for Molecular Neurology, VIB, and Department of Neurology, University Hospital of Antwerp, University of Antwerp, Antwerpen, Belgium.
³ Department of Epilepsy Genetics, Danish Epilepsy Centre Filadelfia, Dianalund, Denmark.
⁴ Clinical Genetic Department, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
⁵ Institute for Regional Health Services Research, University of Southern Denmark, Odense, Denmark.
⁶ University of Groningen, University Medical Center Groningen, Department of Neurology, Groningen, the Netherlands.
⁷ University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, The Netherlands.
⁸ Center for Genomic Medicine, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
⁹ Royal Children's Hospital, Melbourne, VIC, Australia.
¹⁰ Murdoch Children's Research Institute, Melbourne, VIC, Australia.
¹¹ Department of Pediatrics, University of Melbourne, Melbourne, VIC, Australia.
¹² Department of Radiology, University of Melbourne, Melbourne, VIC, Australia.
¹³ Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia.
¹⁴ Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands.
¹⁵ Department of Pediatrics, Peking University First Hospital, Beijing, China.
¹⁶ Division of Genetic Medicine, Department of Pediatrics, University of Washington, Seattle, WA, USA.
¹⁷ Tel Aviv University Medical School, Tel Aviv, Israel.
¹⁸ Division of Neurology, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.
¹⁹ Epilepsy Center Frankfurt Rhine-Main, Center of Neurology and Neurosurgery, University Hospital Frankfurt, and Center for Personalized Translational Epilepsy Research (CePTER), Goethe-University Frankfurt, Frankfurt am Main, Germany.
²⁰ Edmond and Lily Safra Children's Hospital, Pediatric Neurology Unit, Tel-Hashomer, Israel.
²¹ Tel Aviv University, Sackler School of Medicine, Tel Aviv, Israel.
²² The Walter and Eliza Hall Institute of Medical Research, Melbourne, VIC, Australia.
²³ Department of Medical Biology University of Melbourne, Melbourne, VIC, Australia.
²⁴ Service de génétique médicale, CHU Nantes, Nantes, France.
²⁵ Department of Clinical Genetics, Erasmus MC University Medical Center, Rotterdam, The Netherlands.
²⁶ Section for Medical Genetics, Telemark Hospital, Skien, Norway.
²⁷ Department of Neurosciences, Queensland Children's Hospital, Brisbane, QLD, Australia.
²⁸ Service de Neuropédiatrie, Pôle de Médecine et Spécialités Médicales, CHRU de Lille, Lille, France.
²⁹ Lyon University Hospitals, Departments of Genetics, Lyon, France.
³⁰ T.Y. Nelson Department of Neurology and Neurosurgery, The Children's Hospital at Westmead, Faculty of Medicine and Health, University of Sydney, Sydney, Australia.
³¹ University Medical Centre Groningen, Department of Genetics, Groningen, The Netherlands.
³² INSERM U1028, CNRS UMR5292, Centre de Recherche en Neurosciences de Lyon, GENDEV Team, Bron, France.
³³ Child and Youth, Randers Regional Hospital, Randers, Denmark.
³⁴ Department of Clinical Genomics, Mayo Clinic, Rochester, MN, USA.
³⁵ Stichting Epilepsie Instellingen Nederland, Zwolle, The Netherlands.
³⁶ Clinical Hospital "Psychiatry", Kyiv, Ukraine.
³⁷ Center for Individualized Medicine, Mayo Clinic, Rochester, MN, USA.
³⁸ Department of Human Genetics, Donders Institute for Brain, Cognition and Behavior, Radboud University Medical Center, Nijmegen, The Netherlands.
³⁹ Pediatric Neurology Unit, University Hospitals, Geneva, Switzerland.
⁴⁰ Institute of Medical Genetics, Wolfson Medical Center, Holon, Israel.
⁴¹ Medical Genetics, St George's University Hospitals NHS FT, Cranmer Tce, London, United Kingdom.
⁴² Department of Neuroscience, Pharmacology and Child Health, Children's Hospital A. Meyer and University of Florence, Florence, Italy.
⁴³ CPDPN, Pôle mère enfant, Maison de Santé Protestante Bordeaux Bagatelle, Talence, France.
⁴⁴ INSERM UMR1231 GAD, FHU-TRANSLAD, Université de Bourgogne, Dijon, France.
⁴⁵ Discipline of Child and Adolescent Health, Sydney Medical School, University of Sydney, Sydney, NSW, Australia.
⁴⁶ Medigenome, Swiss Institute of Genomic Medicine, Geneva, Switzerland.
⁴⁷ Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK.
⁴⁸ Department of Paediatrics and Child Health, University of Otago Wellington, Wellington, New Zealand.
⁴⁹ One Centre of Genetics, Vadodara, India.
⁵⁰ Neuropaediatric Unit, Shaare Zedek Medical Centre, Hebrew University School of Medicine, Jerusalem, Israel.
⁵¹ Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, United Kingdom and Chalfont Centre for Epilepsy, Bucks, UK.
⁵² Institut de Génétique Médicale, Hopital Jeanne de Flandre, Lille University Hospital, Lille, France.
⁵³ Department of Clinical Genetics and GROW-School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, The Netherlands.
⁵⁴ Paediatric Neurosciences Research Group, Royal Hospital for Children, Glasgow, UK.
⁵⁵ College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.
⁵⁶ UF Innovation en diagnostic genomique des maladies rares, CHU Dijon Bourgogne, Dijon, France.
⁵⁷ INSERM UMR1231 GAD, Dijon, France.
⁵⁸ Academic Center for Epileptology, Kempenhaege, Department of Neurology, Heeze, The Netherlands.
⁵⁹ School of Medicine, University of Queensland, Brisbane, QLD, Australia.
⁶⁰ Molecular Genetics Lab, Wolfson Medical Center, Holon, Israel.
⁶¹ Section of Genetics and Metabolism, Department of Pediatrics, University of Arkansas for Medical Sciences, Arkansas Children's Hospital, Little Rock, AR, USA.
⁶² White Matter Disease Care, Pediatric Neurology Unit, Dana-Dwak Children's Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
⁶³ Genetic Health Queensland, Royal Brisbane and Women's Hospital, Brisbane, QLD, Australia.
⁶⁴ Epilepsy Research Centre, Department of Medicine, Austin Health, University of Melbourne, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁵ Royal Children's Hospital, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁶ Murdoch Children's Research Institute, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁷ Department of Pediatrics, University of Melbourne, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁸ Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.

^# Contributed equally.

PMID: 33144681
DOI: 10.1038/s41436-020-00988-9

Free article

NEXMIF encephalopathy: an X-linked disorder with male and female phenotypic patterns

Hannah Stamberger et al. Genet Med. 2021 Feb.

Free article

. 2021 Feb;23(2):363-373.

doi: 10.1038/s41436-020-00988-9. Epub 2020 Nov 4.

Authors

Affiliations

¹ Epilepsy Research Centre, Department of Medicine, Austin Health, University of Melbourne, Melbourne, VIC, Australia.
² Applied and Translational Neurogenomics group, Center for Molecular Neurology, VIB, and Department of Neurology, University Hospital of Antwerp, University of Antwerp, Antwerpen, Belgium.
³ Department of Epilepsy Genetics, Danish Epilepsy Centre Filadelfia, Dianalund, Denmark.
⁴ Clinical Genetic Department, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
⁵ Institute for Regional Health Services Research, University of Southern Denmark, Odense, Denmark.
⁶ University of Groningen, University Medical Center Groningen, Department of Neurology, Groningen, the Netherlands.
⁷ University of Groningen, University Medical Center Groningen, Department of Genetics, Groningen, The Netherlands.
⁸ Center for Genomic Medicine, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark.
⁹ Royal Children's Hospital, Melbourne, VIC, Australia.
¹⁰ Murdoch Children's Research Institute, Melbourne, VIC, Australia.
¹¹ Department of Pediatrics, University of Melbourne, Melbourne, VIC, Australia.
¹² Department of Radiology, University of Melbourne, Melbourne, VIC, Australia.
¹³ Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia.
¹⁴ Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands.
¹⁵ Department of Pediatrics, Peking University First Hospital, Beijing, China.
¹⁶ Division of Genetic Medicine, Department of Pediatrics, University of Washington, Seattle, WA, USA.
¹⁷ Tel Aviv University Medical School, Tel Aviv, Israel.
¹⁸ Division of Neurology, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.
¹⁹ Epilepsy Center Frankfurt Rhine-Main, Center of Neurology and Neurosurgery, University Hospital Frankfurt, and Center for Personalized Translational Epilepsy Research (CePTER), Goethe-University Frankfurt, Frankfurt am Main, Germany.
²⁰ Edmond and Lily Safra Children's Hospital, Pediatric Neurology Unit, Tel-Hashomer, Israel.
²¹ Tel Aviv University, Sackler School of Medicine, Tel Aviv, Israel.
²² The Walter and Eliza Hall Institute of Medical Research, Melbourne, VIC, Australia.
²³ Department of Medical Biology University of Melbourne, Melbourne, VIC, Australia.
²⁴ Service de génétique médicale, CHU Nantes, Nantes, France.
²⁵ Department of Clinical Genetics, Erasmus MC University Medical Center, Rotterdam, The Netherlands.
²⁶ Section for Medical Genetics, Telemark Hospital, Skien, Norway.
²⁷ Department of Neurosciences, Queensland Children's Hospital, Brisbane, QLD, Australia.
²⁸ Service de Neuropédiatrie, Pôle de Médecine et Spécialités Médicales, CHRU de Lille, Lille, France.
²⁹ Lyon University Hospitals, Departments of Genetics, Lyon, France.
³⁰ T.Y. Nelson Department of Neurology and Neurosurgery, The Children's Hospital at Westmead, Faculty of Medicine and Health, University of Sydney, Sydney, Australia.
³¹ University Medical Centre Groningen, Department of Genetics, Groningen, The Netherlands.
³² INSERM U1028, CNRS UMR5292, Centre de Recherche en Neurosciences de Lyon, GENDEV Team, Bron, France.
³³ Child and Youth, Randers Regional Hospital, Randers, Denmark.
³⁴ Department of Clinical Genomics, Mayo Clinic, Rochester, MN, USA.
³⁵ Stichting Epilepsie Instellingen Nederland, Zwolle, The Netherlands.
³⁶ Clinical Hospital "Psychiatry", Kyiv, Ukraine.
³⁷ Center for Individualized Medicine, Mayo Clinic, Rochester, MN, USA.
³⁸ Department of Human Genetics, Donders Institute for Brain, Cognition and Behavior, Radboud University Medical Center, Nijmegen, The Netherlands.
³⁹ Pediatric Neurology Unit, University Hospitals, Geneva, Switzerland.
⁴⁰ Institute of Medical Genetics, Wolfson Medical Center, Holon, Israel.
⁴¹ Medical Genetics, St George's University Hospitals NHS FT, Cranmer Tce, London, United Kingdom.
⁴² Department of Neuroscience, Pharmacology and Child Health, Children's Hospital A. Meyer and University of Florence, Florence, Italy.
⁴³ CPDPN, Pôle mère enfant, Maison de Santé Protestante Bordeaux Bagatelle, Talence, France.
⁴⁴ INSERM UMR1231 GAD, FHU-TRANSLAD, Université de Bourgogne, Dijon, France.
⁴⁵ Discipline of Child and Adolescent Health, Sydney Medical School, University of Sydney, Sydney, NSW, Australia.
⁴⁶ Medigenome, Swiss Institute of Genomic Medicine, Geneva, Switzerland.
⁴⁷ Great Ormond Street Hospital for Children NHS Foundation Trust, London, UK.
⁴⁸ Department of Paediatrics and Child Health, University of Otago Wellington, Wellington, New Zealand.
⁴⁹ One Centre of Genetics, Vadodara, India.
⁵⁰ Neuropaediatric Unit, Shaare Zedek Medical Centre, Hebrew University School of Medicine, Jerusalem, Israel.
⁵¹ Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, United Kingdom and Chalfont Centre for Epilepsy, Bucks, UK.
⁵² Institut de Génétique Médicale, Hopital Jeanne de Flandre, Lille University Hospital, Lille, France.
⁵³ Department of Clinical Genetics and GROW-School for Oncology and Developmental Biology, Maastricht University Medical Center, Maastricht, The Netherlands.
⁵⁴ Paediatric Neurosciences Research Group, Royal Hospital for Children, Glasgow, UK.
⁵⁵ College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.
⁵⁶ UF Innovation en diagnostic genomique des maladies rares, CHU Dijon Bourgogne, Dijon, France.
⁵⁷ INSERM UMR1231 GAD, Dijon, France.
⁵⁸ Academic Center for Epileptology, Kempenhaege, Department of Neurology, Heeze, The Netherlands.
⁵⁹ School of Medicine, University of Queensland, Brisbane, QLD, Australia.
⁶⁰ Molecular Genetics Lab, Wolfson Medical Center, Holon, Israel.
⁶¹ Section of Genetics and Metabolism, Department of Pediatrics, University of Arkansas for Medical Sciences, Arkansas Children's Hospital, Little Rock, AR, USA.
⁶² White Matter Disease Care, Pediatric Neurology Unit, Dana-Dwak Children's Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
⁶³ Genetic Health Queensland, Royal Brisbane and Women's Hospital, Brisbane, QLD, Australia.
⁶⁴ Epilepsy Research Centre, Department of Medicine, Austin Health, University of Melbourne, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁵ Royal Children's Hospital, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁶ Murdoch Children's Research Institute, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁷ Department of Pediatrics, University of Melbourne, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.
⁶⁸ Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia. i.scheffer@unimelb.edu.au.

^# Contributed equally.

PMID: 33144681
DOI: 10.1038/s41436-020-00988-9

Abstract

Purpose: Pathogenic variants in the X-linked gene NEXMIF (previously KIAA2022) are associated with intellectual disability (ID), autism spectrum disorder, and epilepsy. We aimed to delineate the female and male phenotypic spectrum of NEXMIF encephalopathy.

Methods: Through an international collaboration, we analyzed the phenotypes and genotypes of 87 patients with NEXMIF encephalopathy.

Results: Sixty-three females and 24 males (46 new patients) with NEXMIF encephalopathy were studied, with 30 novel variants. Phenotypic features included developmental delay/ID in 86/87 (99%), seizures in 71/86 (83%) and multiple comorbidities. Generalized seizures predominated including myoclonic seizures and absence seizures (both 46/70, 66%), absence with eyelid myoclonia (17/70, 24%), and atonic seizures (30/70, 43%). Males had more severe developmental impairment; females had epilepsy more frequently, and varied from unaffected to severely affected. All NEXMIF pathogenic variants led to a premature stop codon or were deleterious structural variants. Most arose de novo, although X-linked segregation occurred for both sexes. Somatic mosaicism occurred in two males and a family with suspected parental mosaicism.

Conclusion: NEXMIF encephalopathy is an X-linked, generalized developmental and epileptic encephalopathy characterized by myoclonic-atonic epilepsy overlapping with eyelid myoclonia with absence. Some patients have developmental encephalopathy without epilepsy. Males have more severe developmental impairment. NEXMIF encephalopathy arises due to loss-of-function variants.

Keywords: KIAA2022; NEXMIF; developmental and epileptic encephalopathy; epilepsy; intellectual disability.

PubMed Disclaimer

Cited by

Heterozygous Nexmif female mice demonstrate mosaic NEXMIF expression, autism-like behaviors, and abnormalities in dendritic arborization and synaptogenesis.
O'Connor M, Qiao H, Odamah K, Cerdeira PC, Man HY. O'Connor M, et al. Heliyon. 2024 Jan 24;10(3):e24703. doi: 10.1016/j.heliyon.2024.e24703. eCollection 2024 Feb 15. Heliyon. 2024. PMID: 38322873 Free PMC article.
The autism spectrum disorder risk gene NEXMIF over-synchronizes hippocampal CA1 network and alters neuronal coding.
Mount RA, Athif M, O'Connor M, Saligrama A, Tseng HA, Sridhar S, Zhou C, Bortz E, San Antonio E, Kramer MA, Man HY, Han X. Mount RA, et al. Front Neurosci. 2023 Oct 27;17:1277501. doi: 10.3389/fnins.2023.1277501. eCollection 2023. Front Neurosci. 2023. PMID: 37965217 Free PMC article.
Complexity in Genetic Epilepsies: A Comprehensive Review.
Rastin C, Schenkel LC, Sadikovic B. Rastin C, et al. Int J Mol Sci. 2023 Sep 27;24(19):14606. doi: 10.3390/ijms241914606. Int J Mol Sci. 2023. PMID: 37834053 Free PMC article. Review.
NEXMIF pathogenic variant in a female child with epilepsy and multiple organ failure: a case report.
Wang L, Huang Y, Liu X. Wang L, et al. Transl Pediatr. 2023 Jun 30;12(6):1278-1287. doi: 10.21037/tp-22-435. Epub 2023 May 18. Transl Pediatr. 2023. PMID: 37427056 Free PMC article.
The phenotypic and genotypic spectrum of epilepsy and intellectual disability in adults: Implications for genetic testing.
von Brauchitsch S, Haslinger D, Lindlar S, Thiele H, Bernsen N, Zahnert F, Reif PS, Balcik Y, Au PYB, Josephson CB, Altmüller J, Strzelczyk A, Knake S, Rosenow F, Chiocchetti A, Klein KM. von Brauchitsch S, et al. Epilepsia Open. 2023 Jun;8(2):497-508. doi: 10.1002/epi4.12719. Epub 2023 Mar 17. Epilepsia Open. 2023. PMID: 36896643 Free PMC article.

See all "Cited by" articles

References

1. Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512–521. - DOI
1. Howell KB, Eggers S, Dalziel K, et al. A population-based cost-effectiveness study of early genetic testing in severe epilepsies of infancy. Epilepsia. 2018;59:1177–1187. - DOI
1. Heyne HO, Singh T, Stamberger H, et al. De novo variants in neurodevelopmental disorders with epilepsy. Nat Genet. 2018;50:1048–1053. - DOI
1. Dibbens LM, Tarpey PS, Hynes K, et al. X-linked protocadherin 19 mutations cause female-limited epilepsy and cognitive impairment. Nat Genet. 2008;40:776–781. - DOI
1. Mignot C, McMahon AC, Bar C, et al. IQSEC2-related encephalopathy in males and females: a comparative study including 37 novel patients. Genet Med. 2019;21:837–849. - DOI

Publication types

Actions
Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions
Actions

Grants and funding

R01 NS069605/NS/NINDS NIH HHS/United States

LinkOut - more resources

Full Text Sources
- Elsevier Science
Medical
- MedlinePlus Consumer Health Information
- MedlinePlus Health Information
Molecular Biology Databases
- GlyGen glycoinformatics resource

[1] Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512–521. - DOI

[2] Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512–521. - DOI

[3] Howell KB, Eggers S, Dalziel K, et al. A population-based cost-effectiveness study of early genetic testing in severe epilepsies of infancy. Epilepsia. 2018;59:1177–1187. - DOI

[4] Howell KB, Eggers S, Dalziel K, et al. A population-based cost-effectiveness study of early genetic testing in severe epilepsies of infancy. Epilepsia. 2018;59:1177–1187. - DOI

[5] Heyne HO, Singh T, Stamberger H, et al. De novo variants in neurodevelopmental disorders with epilepsy. Nat Genet. 2018;50:1048–1053. - DOI

[6] Heyne HO, Singh T, Stamberger H, et al. De novo variants in neurodevelopmental disorders with epilepsy. Nat Genet. 2018;50:1048–1053. - DOI

[7] Dibbens LM, Tarpey PS, Hynes K, et al. X-linked protocadherin 19 mutations cause female-limited epilepsy and cognitive impairment. Nat Genet. 2008;40:776–781. - DOI

[8] Dibbens LM, Tarpey PS, Hynes K, et al. X-linked protocadherin 19 mutations cause female-limited epilepsy and cognitive impairment. Nat Genet. 2008;40:776–781. - DOI

[9] Mignot C, McMahon AC, Bar C, et al. IQSEC2-related encephalopathy in males and females: a comparative study including 37 novel patients. Genet Med. 2019;21:837–849. - DOI

[10] Mignot C, McMahon AC, Bar C, et al. IQSEC2-related encephalopathy in males and females: a comparative study including 37 novel patients. Genet Med. 2019;21:837–849. - DOI

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

NEXMIF encephalopathy: an X-linked disorder with male and female phenotypic patterns

Affiliations

NEXMIF encephalopathy: an X-linked disorder with male and female phenotypic patterns

Authors

Affiliations

Abstract

Similar articles

Cited by

References

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Molecular Biology Databases

Abstract

Similar articles

Cited by

References

Publication types

MeSH terms

Substances

Related information

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Molecular Biology Databases