Phenotype variability and natural history of X-linked myopathy with excessive autophagy

J Neurol. 2024 Jul;271(7):4008-4018. doi: 10.1007/s00415-024-12298-0. Epub 2024 Mar 22.

Abstract

Objective: X-linked myopathy with excessive autophagy (XMEA) linked to the VMA21 gene leads to autophagy failure with progressive vacuolation and atrophy of skeletal muscles. Current knowledge of this rare disease is limited. Our objective was to define the clinical, radiological, and natural history of XMEA.

Methods: We conducted a retrospective study collecting clinical, genetic, muscle imaging, and biopsy data of XMEA patients followed in France and reviewed the literature for additional cases.

Results: Eighteen males had genetically confirmed XMEA in France, carrying four different VMA21 variants. Mean age at disease onset was 9.4 ± 9.9 (range 1-40) years. In 14/18 patients (77.8%), onset occurred during childhood (< 15 years); however in four patients, the disease started in adulthood. Patients had anterior and medial compartment thigh muscle weakness, distal contractures (56.3%), elevated CK levels (1287.9 ± 757.8 U/l) and autophagic vacuoles with sarcolemmal features on muscle histopathology. Muscle MRI (n = 10) showed a characteristic pattern of lower limb muscle involvement. In 11 patients, outcome measures were available for an average follow-up period of 10.6 ± 9.8 years and six of them show disease progression. Mean change of functional outcomes was 0.5 ± 1.2 points for Brooke and 2.2 ± 2.5 points for Vignos score, 7/16 patients (43.8%) needed a walking aid and 3/16 (18.8%) were wheelchair-bound (median age of 40 years old, range 39-48). The variant c.164-7 T > G was associated with a later onset of symptoms. Respiratory insufficiency was common (57.1%) but cardiac involvement rare (12.5%).

Interpretation: XMEA has variable age of onset, but a characteristic clinical, histopathological, and muscle imaging presentation, guiding the diagnosis. Although slowly, motor disability progresses with time, and relevant genotype-phenotype correlations will help design future clinical trials.

Keywords: Muscle MRI; Muscle biopsy; VMA21; X-linked myopathy with excessive autophagy.

MeSH terms

  • Adolescent
  • Adult
  • Child
  • Child, Preschool
  • Disease Progression
  • France
  • Genetic Diseases, X-Linked* / diagnostic imaging
  • Genetic Diseases, X-Linked* / genetics
  • Genetic Diseases, X-Linked* / pathology
  • Genetic Diseases, X-Linked* / physiopathology
  • Humans
  • Infant
  • Male
  • Middle Aged
  • Muscle, Skeletal* / diagnostic imaging
  • Muscle, Skeletal* / pathology
  • Muscle, Skeletal* / physiopathology
  • Muscular Diseases
  • Phenotype*
  • Retrospective Studies
  • Vacuolar Proton-Translocating ATPases
  • Young Adult

Substances

  • VMA21 protein, human
  • Vacuolar Proton-Translocating ATPases

Supplementary concepts

  • Myopathy, X-Linked, with Excessive Autophagy