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Expanding the clinical and genetic landscape of (developmental) epileptic encephalopathy with spike-and-wave activation in sleep: results from studies of a Turkish cohort

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Abstract

The terms developmental epileptic encephalopathy with spike-and-wave activation in sleep (DEE-SWAS) and epileptic encephalopathy with spike-and-wave activation in sleep (EE-SWAS) designate a spectrum of conditions that are typified by different combinations of motor, cognitive, language, and behavioral regression linked to robust spike-and-wave activity during sleep. In this study, we aimed at describing the clinical and molecular findings in “(developmental) epileptic encephalopathy with spike-and-wave activation in sleep” (D)EE-SWAS) patients as well as at contributing to the genetic etiologic spectrum of (D)EE-SWAS. Single nucleotide polymorphism (SNP) array and whole-exome sequencing (WES) techniques were used to determine the underlying genetic etiologies. Of the 24 patients included in the study, 8 (33%) were female and 16 (67%) were male. The median age at onset of the first seizure was 4 years and the median age at diagnosis of (D)EE-SWAS was 5 years. Of the 24 cases included in the study, 13 were compatible with the clinical diagnosis of DEE-SWAS and 11 were compatible with the clinical diagnosis of EE-SWAS. Abnormal perinatal history was present in four cases (17%), and two cases (8%) had a family history of epilepsy. Approximately two-thirds (63%) of all patients had abnormalities detected on brain computerized tomography/magnetic resonance (CT/MR) imaging. After SNP array and WES analysis, the genetic etiology was revealed in 7 out of 24 (29%) cases. Three of the variants detected were novel (SLC12A5, DLG4, SLC9A6). This study revealed for the first time that Smith-Magenis syndrome, SCN8A-related DEE type 13 and SLC12A5 gene variation are involved in the genetic etiology of (D)EE-SWAS. (D)EE-SWAS is a genetically diverse disorder with underlying copy number variations and single-gene abnormalities. In the current investigation, rare novel variations in genes known to be related to (D)EE-SWAS and not previously reported genes to be related to (D)EE-SWAS were discovered, adding to the molecular genetic spectrum. Molecular etiology enables the patient and family to receive thorough and accurate genetic counseling as well as a personalized medicine approach.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We want to thank the children and the parents and the clinicians who made this study possible. Some of the data obtained in this study were presented by us as an oral presentation named “Genetic variants in the patients with developmental and/or epileptic encephalopathy with spike-and-wave activation in sleep” at the 15th European Paediatric Neurology Society Congress (Abstract no: EPNS2023-2212).

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Medical Genetics, Karadeniz Technical University Faculty of Medicine, Ortahisar, 61100, Trabzon, Türkiye

    Ayberk Türkyılmaz

  2. Department of Pediatric Neurology, Kartal Dr. Lütfi Kirdar City Hospital, Istanbul, Türkiye

    Safiye Güneş Sağer

  3. Department of Pediatric Neurology, Giresun University Maternity and Children Hospital, Giresun, Türkiye

    Emine Tekin

  4. Department of Medical Biochemistry, Cyprus International University Faculty of Medicine, Nicosia, Cyprus

    Kerem Teralı

  5. Department of Radiology, Kartal Dr. Lütfi Kirdar City Hospital, Istanbul, Türkiye

    Hanife Düzkalır

  6. Department of Medical Genetics, Ümraniye Research and Training Hospital, Istanbul, Türkiye

    Metin Eser

  7. Department of Pediatrics, Kartal Dr. Lütfi Kirdar City Hospital, Istanbul, Türkiye

    Yasemin Akın

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Contributions

AT and KT wrote the main manuscript text and prepared the figures and tables. AT, ET, SGS created the study design. SGS, ET performed the EEG evaluation. SGS, AT, ET, ME, YA, HD gathered and prepared patient data. All authors reviewed, edited, and approved the manuscript.

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Correspondence to Ayberk Türkyılmaz.

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Supplementary Information

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Supplementary Fig. 1

Electrical status epileptic during sleep presenting as bilateral spikes and waves activated in sleep in patient 8, 12, 13, 16, 17 respectively. "(Calibration: vertical bar = 70 μV, horizontal bar = 1000 msec; Bandpass 0.5–70 Hz). (PDF 372 kb)

Supplementary Fig. 2

Electrical status epileptic during sleep presenting as bilateral spikes and waves activated in sleep in patient 8, 12, 13, 16, 17 respectively. "(Calibration: vertical bar = 70 μV, horizontal bar = 1000 msec; Bandpass 0.5–70 Hz). (PDF 362 kb)

Supplementary Fig. 3

Electrical status epileptic during sleep presenting as bilateral spikes and waves activated in sleep in patient 8, 12, 13, 16, 17 respectively. "(Calibration: vertical bar = 70 μV, horizontal bar = 1000 msec; Bandpass 0.5–70 Hz). (PDF 726 kb)

Supplementary Fig. 4

Electrical status epileptic during sleep presenting as bilateral spikes and waves activated in sleep in patient 8, 12, 13, 16, 17 respectively. "(Calibration: vertical bar = 70 μV, horizontal bar = 1000 msec; Bandpass 0.5–70 Hz). (PDF 478 kb)

Supplementary Fig. 5

Electrical status epileptic during sleep presenting as bilateral spikes and waves activated in sleep in patient 8, 12, 13, 16, 17 respectively. "(Calibration: vertical bar = 70 μV, horizontal bar = 1000 msec; Bandpass 0.5–70 Hz). (PDF 434 kb)

Supplementary Fig. 6

Computational biochemical analysis of the human NaV1.6 Gly1626Leu mutant. (A) Cartoon representation of the wild-type NaV1.6 α-subunit complexed with the auxiliary β1-subunit (PDB ID: 8FHD). The structurally homologous domains I to IV are colored pale green, pale yellow, light blue and light pink, respectively. Visible portion of the NaV1.6 N-terminal domain is colored cherry red, and visible portion of the NaV1.6 C-terminal domain is colored olive green. The cytoplasmic interdomain linkers are colored black. Dashed lines indicate the invisible regions of the channel. (B) Combined cartoon and stick representation of a part of the wild-type NaV1.6 VSDIV. R1–R5 and K6 correspond to the gating charges, An1 and An2 correspond to the anionic centers, and HSC corresponds to the hydrophobic constriction site. (C) Combined cartoon and stick representation of a part of the mutant NaV1.6 VSDIV. The in silico introduced mutant Leu1626 residue is colored gray. All images were rendered with the PyMOL Molecular Graphics System, v18 (Schrödinger LLC, Portland, OR, USA). (PNG 6108 kb)

High resolution image (TIF 8890 kb)

Supplementary Fig. 7

Computational biochemical analysis of the human KCC2 Gly549Ala (Gly526Ala) mutant. (A) Cartoon representation of the wild-type KCC2 homodimer complexed with the K+ and Cl– ions (PDB ID: 6M23). The two monomers (A and B) are colored pale cyan and wheat yellow, respectively. Dashed lines indicate the invisible regions of the cotransporter. (B) Combined cartoon and stick representation of a part of the mutant KCC2 intracellular loop interconnecting TM8 and TM9. The in silico introduced mutant Ala549 (Ala526) residue is colored gray. Both images were rendered with the PyMOL Molecular Graphics System, v18 (Schrödinger LLC, Portland, OR, USA). (C) Multiple sequence alignment of known electroneutral cation-coupled chloride cotransporters of the human SLC12 family (except CCC9). Uppercase letters denote identity, and lowercase letters denote a consensus level of greater than 0.5. The position of the affected glycine residue is marked by an arrow. The graphically enhanced alignment was prepared with ESPript 3.0. (PNG 6689 kb)

High resolution image (TIF 9713 kb)

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Türkyılmaz, A., Sağer, S.G., Tekin, E. et al. Expanding the clinical and genetic landscape of (developmental) epileptic encephalopathy with spike-and-wave activation in sleep: results from studies of a Turkish cohort. Neurogenetics (2024). https://doi.org/10.1007/s10048-024-00751-1

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