Assessment of risk of ALS conferred by the GGGGCC hexanucleotide repeat expansion in C9orf72 among first-degree relatives of patients with ALS carrying the repeat expansion

References

• Smukowski SN, Maioli H, Latimer CS, Bird TD, Jayadev S, Valdmanis PN. Progress in amyotrophic lateral sclerosis gene discovery: reflecting on classic approaches and leveraging emerging technologies. Neurol Genet. 2022;8:e669.
   PubMed Web of Science ®Google Scholar
• Miller TM, Cudkowicz ME, Genge A, Shaw PJ, Sobue G, Bucelli RC, et al. Trial of antisense oligonucleotide tofersen for SOD1 ALS. N Engl J Med. 2022;387:1099–110.
   PubMed Web of Science ®Google Scholar
• van Es MA, Hardiman O, Chio A, Al-Chalabi A, Pasterkamp RJ, Veldink JH, et al. Amyotrophic lateral sclerosis. Lancet. 2017;390:2084–98.
   PubMed Web of Science ®Google Scholar
• Westeneng H-J, van Veenhuijzen K, van der Spek RA, Peters S, Visser AE, van Rheenen W, et al. Associations between lifestyle and amyotrophic lateral sclerosis stratified by C9orf72 genotype: a longitudinal, population-based, case-control study. Lancet Neurol. 2021;20:373–84.
   PubMed Web of Science ®Google Scholar
• Majounie E, Renton AE, Mok K, Dopper EG, Waite A, Rollinson S, et al. Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol. 2012;11:323–30.
   PubMed Web of Science ®Google Scholar
• Roggenbuck J. C9orf72 and the care of the patient with ALS or FTD: progress and recommendations after 10 years. Neurol Genet. 2021;7:e542.
   PubMed Web of Science ®Google Scholar
• Benatar M, Stanislaw C, Reyes E, Hussain S, Cooley A, Fernandez MC, et al. Presymptomatic ALS genetic counseling and testing: experience and recommendations. Neurology 2016;86:2295–302.
   PubMed Web of Science ®Google Scholar
• Murphy NA, Arthur KC, Tienari PJ, Houlden H, Chiò A, Traynor BJ. Age-related penetrance of the C9orf72 repeat expansion. Sci Rep. 2017;7:2116.
   PubMed Web of Science ®Google Scholar
• Le Ber I, Camuzat A, Guillot-Noel L, Hannequin D, Lacomblez L, Golfier V, et al. C9ORF72 repeat expansions in the frontotemporal dementias spectrum of diseases: a flow-chart for genetic testing. J Alzheimers Dis. 2013;34:485–99.
   PubMed Web of Science ®Google Scholar
• McCann EP, Williams KL, Fifita JA, Tarr IS, O’Connor J, Rowe DB, et al. The genotype-phenotype landscape of familial amyotrophic lateral sclerosis in Australia. Clin Genet. 2017;92:259–66.
   PubMed Web of Science ®Google Scholar
• Williams KL, Fifita JA, Vucic S, Durnall JC, Kiernan MC, Blair IP, et al. Pathophysiological insights into ALS with C9ORF72 expansions. J Neurol Neurosurg Psychiatry. 2013;84:931–5.
   PubMed Web of Science ®Google Scholar
• Dolzhenko E, van Vugt J, Shaw RJ, Bekritsky MA, van Blitterswijk M, Narzisi G, et al. Detection of long repeat expansions from PCR-free whole-genome sequence data. Genome Res. 2017;27:1895–903.
   PubMed Web of Science ®Google Scholar
• Beck J, Poulter M, Hensman D, Rohrer JD, Mahoney CJ, Adamson G, et al. Large C9orf72 hexanucleotide repeat expansions are seen in multiple neurodegenerative syndromes and are more frequent than expected in the UK population. Am J Hum Genet. 2013;92:345–53.
   PubMed Web of Science ®Google Scholar
• Huisman MHB, de Jong SW, van Doormaal PTC, Weinreich SS, Schelhaas HJ, van der Kooi AJ, et al. Population based epidemiology of amyotrophic lateral sclerosis using capture–recapture methodology. J Neurol Neurosurg Psychiatry. 2011;82:1165–70.
   PubMed Web of Science ®Google Scholar
• van Rheenen W, Shatunov A, Dekker AM, McLaughlin RL, Diekstra FP, Pulit SL, et al. Genome-wide association analyses identify new risk variants and the genetic architecture of amyotrophic lateral sclerosis. Nat Genet. 2016;48:1043–8.
   PubMed Web of Science ®Google Scholar
• van Rheenen W, van der Spek RAA, Bakker MK, van Vugt J, Hop PJ, Zwamborn RAJ, et al. Common and rare variant association analyses in amyotrophic lateral sclerosis identify 15 risk loci with distinct genetic architectures and neuron-specific biology. Nat Genet. 2021;53:1636–48.
   PubMed Web of Science ®Google Scholar
• van Blitterswijk M, van Es MA, Hennekam EA, Dooijes D, van Rheenen W, Medic J, et al. Evidence for an oligogenic basis of amyotrophic lateral sclerosis. Hum Mol Genet. 2012;21:3776–84.
   PubMed Web of Science ®Google Scholar
• van Rheenen W, van Blitterswijk M, Huisman MH, Vlam L, van Doormaal PT, Seelen M, et al. Hexanucleotide repeat expansions in C9ORF72 in the spectrum of motor neuron diseases. Neurology 2012;79:878–82.
   PubMed Web of Science ®Google Scholar
• Goutman SA, Hardiman O, Al-Chalabi A, Chió A, Savelieff MG, Kiernan MC, et al. Emerging insights into the complex genetics and pathophysiology of amyotrophic lateral sclerosis. Lancet Neurol. 2022;21:465–79.
   PubMed Web of Science ®Google Scholar
• Fine JP, Gray RJ. A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc. 1999;94:496–509.
   Web of Science ®Google Scholar
• Al-Chalabi A, Lewis CM. Modelling the effects of penetrance and family size on rates of sporadic and familial disease. Hum Hered. 2011;71:281–8.
   PubMed Web of Science ®Google Scholar
• Morisot A, Bessaoud F, Landais P, Rébillard X, Trétarre B, Daurès JP. Prostate cancer: net survival and cause-specific survival rates after multiple imputation. BMC Med Res Methodol. 2015;15:54.
   PubMed Web of Science ®Google Scholar
• Schomaker M, Heumann C. Bootstrap inference when using multiple imputation. Stat Med. 2018;37:2252–66.
   PubMed Web of Science ®Google Scholar
• Brown CA, Lally C, Kupelian V, Flanders WD. Estimated prevalence and incidence of amyotrophic lateral sclerosis and SOD1 and C9orf72 genetic variants. Neuroepidemiology 2021;55:342–53.
   PubMed Web of Science ®Google Scholar
• Zou ZY, Zhou ZR, Che CH, Liu CY, He RL, Huang HP. Genetic epidemiology of amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2017;88:540–9.
   PubMed Web of Science ®Google Scholar
• de Jongh AD, van Eijk RPA, Peters SM, van Es MA, Horemans AMC, van der Kooi AJ, et al. Incidence, prevalence, and geographical clustering of motor neuron disease in the Netherlands. Neurology 2021;96:e1227–e36.
   PubMed Web of Science ®Google Scholar
• van der Zee J, Dillen L, Van Langenhove T, Engelborghs S, Philtjens S, Vandenbulcke M, et al. A Pan-European study of the C9orf72 repeat associated with FTLD: geographic prevalence, genomic instability, and intermediate repeats. Hum Mutat. 2013;34:363–73.
   PubMed Web of Science ®Google Scholar
• Coyle-Gilchrist IT, Dick KM, Patterson K, Vázquez Rodríquez P, Wehmann E, Wilcox A, et al. Prevalence, characteristics, and survival of frontotemporal lobar degeneration syndromes. Neurology 2016;86:1736–43.
   PubMed Web of Science ®Google Scholar
• Spargo TP, Opie-Martin S, Bowles H, Lewis CM, Iacoangeli A, Al-Chalabi A. Calculating variant penetrance from family history of disease and average family size in population-scale data. Genome Med. 2022;14:141.
   PubMed Web of Science ®Google Scholar
• Chiò A, Mazzini L, D Alfonso S, Corrado L, Canosa A, Moglia C, et al. The multistep hypothesis of ALS revisited. Neurology 2018;91:e635-42–e642.
   Web of Science ®Google Scholar
• Ryan M, Heverin M, McLaughlin RL, Hardiman O. Lifetime risk and heritability of amyotrophic lateral sclerosis. JAMA Neurol. 2019;76:1367–74.
   PubMed Web of Science ®Google Scholar
• Greeff JM, Erasmus JC. Three hundred years of low non-paternity in a human population. Heredity (Edinb). 2015;115:396–404.
   PubMed Web of Science ®Google Scholar
• Silverman HE, Goldman JS, Huey ED. Links between the C9orf72 repeat expansion and psychiatric symptoms. Curr Neurol Neurosci Rep. 2019;19:93.
   PubMed Web of Science ®Google Scholar
• Benatar M, Wuu J, Lombardi V, Jeromin A, Bowser R, Andersen PM, et al. Neurofilaments in pre-symptomatic ALS and the impact of genotype. Amyotroph Lateral Scler Frontotemporal Degener. 2019;20:538–48.
   PubMed Web of Science ®Google Scholar