Tumour risks and genotype-phenotype correlations associated with germline variants in succinate dehydrogenase subunit genes SDHB, SDHC and SDHD

J Med Genet. 2018 Jun;55(6):384-394. doi: 10.1136/jmedgenet-2017-105127. Epub 2018 Jan 31.

Abstract

Background: Germline pathogenic variants in SDHB/SDHC/SDHD are the most frequent causes of inherited phaeochromocytomas/paragangliomas. Insufficient information regarding penetrance and phenotypic variability hinders optimum management of mutation carriers. We estimate penetrance for symptomatic tumours and elucidate genotype-phenotype correlations in a large cohort of SDHB/SDHC/SDHD mutation carriers.

Methods: A retrospective survey of 1832 individuals referred for genetic testing due to a personal or family history of phaeochromocytoma/paraganglioma. 876 patients (401 previously reported) had a germline mutation in SDHB/SDHC/SDHD (n=673/43/160). Tumour risks were correlated with in silico structural prediction analyses.

Results: Tumour risks analysis provided novel penetrance estimates and genotype-phenotype correlations. In addition to tumour type susceptibility differences for individual genes, we confirmed that the SDHD:p.Pro81Leu mutation has a distinct phenotype and identified increased age-related tumour risks with highly destabilising SDHB missense mutations. By Kaplan-Meier analysis, the penetrance (cumulative risk of clinically apparent tumours) in SDHB and (paternally inherited) SDHD mutation-positive non-probands (n=371/67 with detailed clinical information) by age 60 years was 21.8% (95% CI 15.2% to 27.9%) and 43.2% (95% CI 25.4% to 56.7%), respectively. Risk of malignant disease at age 60 years in non-proband SDHB mutation carriers was 4.2%(95% CI 1.1% to 7.2%). With retrospective cohort analysis to adjust for ascertainment, cumulative tumour risks for SDHB mutation carriers at ages 60 years and 80 years were 23.9% (95% CI 20.9% to 27.4%) and 30.6% (95% CI 26.8% to 34.7%).

Conclusions: Overall risks of clinically apparent tumours for SDHB mutation carriers are substantially lower than initially estimated and will improve counselling of affected families. Specific genotype-tumour risk associations provides a basis for novel investigative strategies into succinate dehydrogenase-related mechanisms of tumourigenesis and the development of personalised management for SDHB/SDHC/SDHD mutation carriers.

Keywords: cancer: endocrine; genetic epidemiology; genetics; molecular genetics; oncology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenal Gland Neoplasms / genetics*
  • Adrenal Gland Neoplasms / pathology
  • Age Factors
  • Aged
  • Aged, 80 and over
  • Female
  • Genetic Association Studies
  • Genotype
  • Germ-Line Mutation / genetics
  • Heterozygote
  • Humans
  • Kaplan-Meier Estimate
  • Male
  • Membrane Proteins / genetics*
  • Middle Aged
  • Mutation, Missense / genetics
  • Paraganglioma / genetics*
  • Paraganglioma / pathology
  • Pheochromocytoma / genetics*
  • Pheochromocytoma / pathology
  • Risk Factors
  • Sex Characteristics
  • Succinate Dehydrogenase / genetics*

Substances

  • Membrane Proteins
  • SDHC protein, human
  • SDHD protein, human
  • SDHB protein, human
  • Succinate Dehydrogenase