Functional Epicardial Conduction Disturbances Due to a SCN5A Variant Associated With Brugada Syndrome

JACC Clin Electrophysiol. 2023 Aug;9(8 Pt 1):1248-1261. doi: 10.1016/j.jacep.2023.03.009. Epub 2023 May 24.

Abstract

Background: Brugada syndrome is a significant cause of sudden cardiac death (SCD), but the underlying mechanisms remain hypothetical.

Objectives: This study aimed to elucidate this knowledge gap through detailed ex vivo human heart studies.

Methods: A heart was obtained from a 15-year-old adolescent boy with normal electrocardiogram who experienced SCD. Postmortem genotyping was performed, and clinical examinations were done on first-degree relatives. The right ventricle was optically mapped, followed by high-field magnetic resonance imaging and histology. Connexin-43 and NaV1.5 were localized by immunofluorescence, and RNA and protein expression levels were studied. HEK-293 cell surface biotinylation assays were performed to examine NaV1.5 trafficking.

Results: A Brugada-related SCD diagnosis was established for the donor because of a SCN5A Brugada-related variant (p.D356N) inherited from his mother, together with a concomitant NKX2.5 variant of unknown significance. Optical mapping demonstrated a localized epicardial region of impaired conduction near the outflow tract, in the absence of repolarization alterations and microstructural defects, leading to conduction blocks and figure-of-8 patterns. NaV1.5 and connexin-43 localizations were normal in this region, consistent with the finding that the p.D356N variant does not affect the trafficking, nor the expression of NaV1.5. Trends of decreased NaV1.5, connexin-43, and desmoglein-2 protein levels were noted; however, the RT-qPCR results suggested that the NKX2-5 variant was unlikely to be involved.

Conclusions: This study demonstrates for the first time that SCD associated with a Brugada-SCN5A variant can be caused by localized functionally, not structurally, impaired conduction.

Keywords: Brugada syndrome; SCN5A variant; epicardial arrhythmogenic conduction substrate; right ventricle; sudden cardiac death.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Brugada Syndrome*
  • Cardiac Conduction System Disease
  • Connexins
  • Death, Sudden, Cardiac
  • Electrocardiography
  • HEK293 Cells
  • Humans
  • Male

Substances

  • SCN5A protein, human
  • Connexins