Genotype-phenotype characterisation of long survivors with motor neuron disease in Scotland

J Neurol. 2023 Mar;270(3):1702-1712. doi: 10.1007/s00415-022-11505-0. Epub 2022 Dec 14.

Abstract

Background: We investigated the phenotypes and genotypes of a cohort of 'long-surviving' individuals with motor neuron disease (MND) to identify potential targets for prognostication.

Methods: Patients were recruited via the Clinical Audit Research and Evaluation for MND (CARE-MND) platform, which hosts the Scottish MND Register. Long survival was defined as > 8 years from diagnosis. 11 phenotypic variables were analysed. Whole genome sequencing (WGS) was performed and variants within 49 MND-associated genes examined. Each individual was screened for C9orf72 repeat expansions. Data from ancestry-matched Scottish populations (the Lothian Birth Cohorts) were used as controls.

Results: 58 long survivors were identified. Median survival from diagnosis was 15.5 years. Long survivors were significantly younger at onset and diagnosis than incident patients and had a significantly longer diagnostic delay. 42% had the MND subtype of primary lateral sclerosis (PLS). WGS was performed in 46 individuals: 14 (30.4%) had a potentially pathogenic variant. 4 carried the known SOD1 p.(Ile114Thr) variant. Significant variants in FIG4, hnRNPA2B1, SETX, SQSTM1, TAF15, and VAPB were detected. 2 individuals had a variant in the SPAST gene suggesting phenotypic overlap with hereditary spastic paraplegia (HSP). No long survivors had pathogenic C9orf72 repeat expansions.

Conclusions: Long survivors are characterised by younger age at onset, increased prevalence of PLS and longer diagnostic delay. Genetic analysis in this cohort has improved our understanding of the phenotypes associated with the SOD1 variant p.(Ile114Thr). Our findings confirm that pathogenic expansion of C9orf72 is likely a poor prognostic marker. Genetic screening using targeted MND and/or HSP panels should be considered in those with long survival, or early-onset slowly progressive disease, to improve diagnostic accuracy and aid prognostication.

Keywords: Amyotrophic lateral sclerosis; Genetics; Motor neuron disease; Survival.

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • C9orf72 Protein / genetics
  • DNA Helicases / genetics
  • Delayed Diagnosis
  • Genotype
  • Humans
  • Motor Neuron Disease* / epidemiology
  • Motor Neuron Disease* / genetics
  • Multifunctional Enzymes / genetics
  • Phenotype
  • RNA Helicases / genetics
  • Spastic Paraplegia, Hereditary* / genetics
  • Spastin / genetics
  • Superoxide Dismutase-1 / genetics

Substances

  • C9orf72 Protein
  • Superoxide Dismutase-1
  • SPAST protein, human
  • Spastin
  • SETX protein, human
  • DNA Helicases
  • RNA Helicases
  • Multifunctional Enzymes
  • FIG4 protein, human