Newborn screening for spinal muscular atrophy - what have we learned?

References

• Zambon AA, Pini V, Bosco L, et al. Early onset hereditary neuronopathies: an update on non-5q motor neuron diseases. Brain. 2023;146(3):806–822. doi: 10.1093/brain/awac452
   PubMed Web of Science ®Google Scholar
• Aragon-Gawinska K, Mouraux C, Dangouloff T, et al. Spinal muscular atrophy treatment in patients identified by newborn screening-A Systematic review. Genes (Basel). 2023 Jun 29;14(7):1377. doi: 10.3390/genes14071377
   PubMed Web of Science ®Google Scholar
• Kolb SJ, Kissel JT. Spinal muscular atrophy. Neurol Clin. 2015;33(4):831–846. doi: 10.1016/j.ncl.2015.07.004
   PubMed Web of Science ®Google Scholar
• Nicolau S, Waldrop MA, Connolly AM, et al. Spinal muscular atrophy. Semin Pediatr Neurol. 2021;37:100878. doi: 10.1016/j.spen.2021.100878
   PubMed Web of Science ®Google Scholar
• Kolb SJ, Coffey CS, Yankey JW, et al. Natural history of infantile-onset spinal muscular atrophy. Ann Neurol. 2017;82(6):883–891. doi: 10.1002/ana.25101
   PubMed Web of Science ®Google Scholar
• Wijngaarde CA, Stam M, Otto LAM, et al. Population-based analysis of survival in spinal muscular atrophy. Neurology. 2020 14;94(15):e1634–e1644. doi: 10.1212/WNL.0000000000009248
   PubMed Web of Science ®Google Scholar
• Werdnig G. Zwei fruhinfantile hereditare Falle von progressiver Muskelatrophie unter dem Bilde der Dystrophie, aber auf neurotischer Grundlage. Arch Psychiatr Nervenkr. 1891;22:437–480. doi: 10.1007/BF01776636
   Google Scholar
• Hoffmann J. Uber chronische spinale Muskelatrophie im Kindersalter auf familiarer Basis. Deut Zeitsch Nervenheilkd. 1893;3(6):427–470. doi: 10.1007/BF01668496
   Google Scholar
• Lefebvre S, Burglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995 13;80(1):155–165. doi: 10.1016/0092-8674(95)90460-3
   PubMed Web of Science ®Google Scholar
• Wirth B. Spinal muscular atrophy: in the challenge lies a solution. Trends Neurosci. 2021;44(4):306–322. doi: 10.1016/j.tins.2020.11.009
   PubMed Web of Science ®Google Scholar
• Faravelli I, Riboldi GM, Rinchetti P, et al. The SMN complex at the crossroad between RNA metabolism and neurodegeneration. Int J Mol Sci. 2023;24(3):2247. doi: 10.3390/ijms24032247
   PubMed Web of Science ®Google Scholar
• Zilio E, Piano V, Wirth B. Mitochondrial dysfunction in spinal muscular atrophy. Int J Mol Sci. 2022;23(18):10878. doi: 10.3390/ijms231810878
   PubMed Web of Science ®Google Scholar
• Ramos DM, d’Ydewalle C, Gabbeta V, et al. Age-dependent SMN expression in disease-relevant tissue and implications for SMA treatment. J Clin Invest. 2019;129(11):4817–4831. doi: 10.1172/JCI124120
   PubMed Web of Science ®Google Scholar
• Cartegni L, Hastings ML, Calarco JÁ, et al. Determinants of exon 7 splicing in the spinal muscular atrophy genes, SMN1 and SMN2. Am J Hum Genet. 2006;78(1):63–77. doi: 10.1086/498853
   PubMed Web of Science ®Google Scholar
• Alves CRR, Zhang R, Johnstone AJ, et al. Whole blood survival motor neuron protein levels correlate with severity of denervation in spinal muscular atrophy. Muscle Nerve. 2020;62(3):351–357. doi: 10.1002/mus.26995
   PubMed Web of Science ®Google Scholar
• Calucho M, Bernal S, Alías L, et al. Correlation between SMA type and SMN2 copy number revisited: an analysis of 625 unrelated Spanish patients and a compilation of 2834 reported cases. Neuromuscular Disorders. 2018;28(3):208–215. doi: 10.1016/j.nmd.2018.01.003
   PubMed Web of Science ®Google Scholar
• Wu X, Wang SH, Sun J, et al. A-44G transition in SMN2 intron 6 protects patients with spinal muscular atrophy. Hum Mol Genet. 2017;26(14):2768–2780. doi: 10.1093/hmg/ddx166
   PubMed Web of Science ®Google Scholar
• Prior TW, Krainer AR, Hua Y, et al. A positive modifier of spinal muscular atrophy in the SMN2 gene. Am J Hum Genet. 2009;85(3):408–413. doi: 10.1016/j.ajhg.2009.08.002
   PubMed Web of Science ®Google Scholar
• Cuscó I, Bernal S, Blasco-Pérez L, et al. Practical guidelines to manage discordant situations of SMN2 copy number in patients with spinal muscular atrophy. Neurol Genet. 2020;6(6):e530. doi: 10.1212/NXG.0000000000000530
   PubMed Web of Science ®Google Scholar
• Yener İH, Topaloglu H, Erdem-Özdamar S, et al. Transcript levels of plastin 3 and neuritin 1 modifier genes in spinal muscular atrophy siblings. Pediatr Int. 2017;59(1):53–56. doi: 10.1111/ped.13052
   PubMed Web of Science ®Google Scholar
• Wadman RI, Jansen MD, Curial CAD, et al. Analysis of FUS, PFN2, TDP-43, and PLS3 as potential disease severity modifiers in spinal muscular atrophy. Neurol Genet. 2019 Jan 3;6(1):e386. doi: 10.1212/NXG.0000000000000386
   PubMed Web of Science ®Google Scholar
• Dangouloff T, Boemer F, Dideberg V, et al. Reader response: discrepancy in redetermination of SMN2 copy numbers in children with SMA. Neurology. 2020;95(3):144–145. doi: 10.1212/WNL.0000000000009907
   PubMed Web of Science ®Google Scholar
• Schorling DC, Becker J, Pechmann A, et al. Discrepancy in redetermination of SMN2 copy numbers in children with SMA. Neurology. 2019;93(6):267–269. doi: 10.1212/WNL.0000000000007836
   PubMed Web of Science ®Google Scholar
• Ramdas S, Servais L. New treatments in spinal muscular atrophy: an overview of currently available data. Expert Opin Pharmacother. 2020;21(3):307–315. doi: 10.1080/14656566.2019.1704732
   PubMed Web of Science ®Google Scholar
• Servais L, Baranello G, Scoto M, et al. Therapeutic interventions for spinal muscular atrophy: preclinical and early clinical development opportunities. Expert Opin Investig Drugs. 2021;30(5):519–527. doi: 10.1080/13543784.2021.1904889
   PubMed Web of Science ®Google Scholar
• Drugs.com [Internet]. FDA approves spinraza. Ewing (NJ). [cited 2016 Dec]. Available from: https://www.drugs.com/newdrugs/fda-approves-spinraza-nusinersen-spinal-muscular-atrophy-4469.html
   Google Scholar
• Drugs.com [Internet]. Evrysdi FDA approval history. Ewing (NJ). [cited 2022 May 31]. Available from: https://www.drugs.com/history/evrysdi.html
   Google Scholar
• Drugs.com [Internet]. Zolgensma FDA approval history. Ewing (NJ). [cited 2019 Jul 1]. Available from: https://www.drugs.com/history/zolgensma.html
   Google Scholar
• Crawford TO, Swoboda KJ, De Vivo DC, et al. NURTURE study group. Muscle Nerve. 2023 Aug;68(2):157–170. doi: 10.1002/mus.27853
   PubMedGoogle Scholar
• Finkel R, Farrar M, Vlodavets D, et al. FP.24 RAINBOWFISH: preliminary efficacy and safety data in risdiplam-treated infants with presymptomatic spinal muscular atrophy (SMA). Poster session presented at: Muscular Dystrophy Association Clinical and Scientific Conference. 3–16 Mar 2022. Chicago, IL.
   Google Scholar
• Strauss KA, Farrar MA, Muntoni F, et al. Onasemnogene abeparvovec for presymptomatic infants with two copies of SMN2 at risk for spinal muscular atrophy type 1: the phase III SPR1NT trial. Nat Med. 2022;28(7):1381–1389. doi: 10.1038/s41591-022-01866-4
   PubMed Web of Science ®Google Scholar
• Strauss KA, Farrar MA, Muntoni F, et al. Onasemnogene abeparvovec for presymptomatic infants with three copies of SMN2 at risk for spinal muscular atrophy: the phase III SPR1NT trial. Nat Med. 2022;28(7):1390–1397. doi: 10.1038/s41591-022-01867-3
   PubMed Web of Science ®Google Scholar
• Mercuri E, Darras BT, Chiriboga CA, et al. Nusinersen versus sham control in later-onset spinal muscular atrophy. N Engl J Med. 2018;378(7):625–635. doi: 10.1056/NEJMoa1710504
   PubMed Web of Science ®Google Scholar
• Finkel RS, Mercuri E, Darras BT, et al. Nusinersen versus sham control in infantile-onset spinal muscular atrophy. N Engl J Med. 2017;377(18):1723–1732. doi: 10.1056/NEJMoa1702752
   PubMed Web of Science ®Google Scholar
• Singh NN, Shishimorova M, Cao LC, et al. A short antisense oligonucleotide masking a unique intronic motif prevents skipping of a critical exon in spinal muscular atrophy. RNA Biol. 2009;6(3):341–350. doi: 10.4161/rna.6.3.8723
   PubMed Web of Science ®Google Scholar
• Singh NN, Howell MD, Androphy EJ, et al. How the discovery of ISS-N1 led to the first medical therapy for spinal muscular atrophy. Gene Ther. 2017;24(9):520–526. doi: 10.1038/gt.2017.34
   PubMed Web of Science ®Google Scholar
• Finkel RS, Chiriboga CA, Vajsar J, et al. Treatment of infantile-onset spinal muscular atrophy with nusinersen: a phase 2, open-label, dose-escalation study. Lancet. 2016;388(10063):3017–3026. doi: 10.1016/S0140-6736(16)31408-8
   PubMed Web of Science ®Google Scholar
• Pechmann A, Behrens M, Dörnbrack K, et al. Effect of nusinersen on motor, respiratory and bulbar function in early-onset spinal muscular atrophy. Brain. 2023;146(2):668–677. doi: 10.1093/brain/awac252
   PubMed Web of Science ®Google Scholar
• Pane M, Coratti G, Pera MC, et al. Nusinersen efficacy data for 24-month in type 2 and 3 spinal muscular atrophy. Ann Clin Transl Neurol. 2022;9(3):404–409. doi: 10.1002/acn3.51514
   PubMed Web of Science ®Google Scholar
• Aragon-Gawinska K, Daron A, Ulinici A, et al. Sitting in patients with spinal muscular atrophy type 1 treated with nusinersen. Dev Med Child Neurol. 2020;62(3):310–314. doi: 10.1111/dmcn.14412
   PubMed Web of Science ®Google Scholar
• Finkel RS, Ryan MM, Pascual Pascual SI, et al. Scientific rationale for a higher dose of nusinersen. Ann Clin Transl Neurol. 2022;9(6):819–829. doi: 10.1002/acn3.51562
   PubMed Web of Science ®Google Scholar
• Meyer K, Ferraiuolo L, Schmelzer L, et al. Improving single injection CSF delivery of AAV9-mediated gene therapy for SMA: a dose-response study in mice and nonhuman primates. Mol Ther. 2015;23(3):477–487. doi: 10.1038/mt.2014.210
   PubMed Web of Science ®Google Scholar
• Finkel RS, McDermott MP, Kaufmann P, et al. Observational study of spinal muscular atrophy type I and implications for clinical trials. Neurology. 2014;83(9):810–817. doi: 10.1212/WNL.0000000000000741
   PubMed Web of Science ®Google Scholar
• Mercuri E, Muntoni F, Baranello G, et al. Onasemnogene abeparvovec gene therapy for symptomatic infantile-onset spinal muscular atrophy type 1 (STR1VE-EU): an open-label, single-arm, multicentre, phase 3 trial. Lancet Neurol. 2021;20(10):832–841. doi: 10.1016/S1474-4422(21)00251-9
   PubMed Web of Science ®Google Scholar
• Day JW, Finkel RS, Chiriboga CA, et al. Onasemnogene abeparvovec gene therapy for symptomatic infantile-onset spinal muscular atrophy in patients with two copies of SMN2 (STR1VE): an open-label, single-arm, multicentre, phase 3 trial. Lancet Neurol. 2021;20(4):284–293. doi: 10.1016/S1474-4422(21)00001-6
   PubMed Web of Science ®Google Scholar
• Chien YH, Chiang SC, Weng WC, et al. Presymptomatic diagnosis of spinal muscular atrophy through newborn screening. J Pediatr. 2017;190:124–129.e1.
   PubMed Web of Science ®Google Scholar
• Elkins K, Wittenauer A, Hagar AF, et al. Georgia state spinal muscular atrophy newborn screening experience: Screening assay performance and early clinical outcomes. Am J Med Genet C Semin Med Genet. 2022;190(2):187–196. doi: 10.1002/ajmg.c.32003
   PubMed Web of Science ®Google Scholar
• Sawada T, Kido J, Sugawara K, et al. Newborn screening for spinal muscular atrophy in Japan: one year of experience. Mol Genet Metab Rep. 2022;32:100908. doi: 10.1016/j.ymgmr.2022.100908
   PubMed Web of Science ®Google Scholar
• Boemer F, Caberg JH, Beckers P, et al. Three years pilot of spinal muscular atrophy newborn screening turned into official program in Southern Belgium. Sci Rep. 2021;11(1):19922. doi: 10.1038/s41598-021-99496-2
   PubMed Web of Science ®Google Scholar
• Vill K, Schwartz O, Blaschek A, et al. Newborn screening for spinal muscular atrophy in Germany: clinical results after 2 years. Orphanet J Rare Dis. 2021;16(1):153. doi: 10.1186/s13023-021-01783-8
   PubMed Web of Science ®Google Scholar
• Kariyawasam DST, Russell JS, Wiley V, et al. The implementation of newborn screening for spinal muscular atrophy: the Australian experience. Genet Med. 2020;22(3):557–565. doi: 10.1038/s41436-019-0673-0
   PubMed Web of Science ®Google Scholar
• Curesma [Internet]. Elk Grove Village (IL): Newborn screening for SMA. [cited 2023 Jun 1]. Available from: https://www.curesma.org/newborn-screening-for-sma/#for-sma
   Google Scholar
• Dangouloff T, Vrščaj E, Servais L, et al. Newborn screening programs for spinal muscular atrophy worldwide: where we stand and where to go. Neuromuscular Disorders. 2021;31(6):574–582. doi: 10.1016/j.nmd.2021.03.007
   PubMed Web of Science ®Google Scholar
• Czibere L, Burggraf S, Fleige T, et al. High-throughput genetic newborn screening for spinal muscular atrophy by rapid nucleic acid extraction from dried blood spots and 384-well qPCR. Eur J Hum Genet. 2020;28(1):23–30. doi: 10.1038/s41431-019-0476-4
   PubMed Web of Science ®Google Scholar
• Dangouloff T, Servais L. Clinical evidence supporting early treatment of patients with spinal muscular atrophy: current perspectives. Ther Clin Risk Manag. 2019;15:1153–1161. doi: 10.2147/TCRM.S172291
   PubMed Web of Science ®Google Scholar
• Alías L, Bernal S, Barceló MJ, et al. Accuracy of marker analysis, quantitative real-time polymerase chain reaction, and multiple ligation-dependent probe amplification to determine SMN2 copy number in patients with spinal muscular atrophy. Genet Test Mol Biomarkers. 2011;15(9):587–594. doi: 10.1089/gtmb.2010.0253
   PubMed Web of Science ®Google Scholar
• Glascock J, Sampson J, Connolly AM, et al. Revised recommendations for the treatment of infants diagnosed with spinal muscular atrophy via newborn screening who have 4 copies of SMN2. J Neuromuscul Dis. 2020;7(2):97–100. doi: 10.3233/JND-190468
   PubMedGoogle Scholar
• Glascock J, Sampson J, Haidet-Phillips A, et al. Treatment algorithm for infants diagnosed with spinal muscular atrophy through newborn screening. J Neuromuscul Dis. 2018;5(2):145–158. doi: 10.3233/JND-180304
   PubMedGoogle Scholar
• Aharoni S, Nevo Y, Orenstein N, et al. Impact of a national population-based carrier-screening program on spinal muscular atrophy births. Neuromuscular Disorders. 2020;30(12):970–974. doi: 10.1016/j.nmd.2020.10.005
   PubMed Web of Science ®Google Scholar
• Robson SJ, Caramins M, Saad M, et al. Socio-economic status and uptake of reproductive carrier screening in Australia. Aust N Z J Obstet Gynaecol. 2020;60(6):976–979. doi: 10.1111/ajo.13206
   PubMed Web of Science ®Google Scholar
• Milligan JN, Blasco-Pérez L, Costa-Roger M, et al. Recommendations for interpreting and reporting silent carrier and disease-modifying variants in SMA testing workflows. Genes (Basel). 2022;13(9):1657. doi: 10.3390/genes13091657
   PubMed Web of Science ®Google Scholar
• Schwab ME, Shao S, Zhang L, et al. Investigating attitudes toward prenatal diagnosis and fetal therapy for spinal muscular atrophy. Prenat Diagn. 2022;42(11):1409–1419. doi: 10.1002/pd.6228
   PubMed Web of Science ®Google Scholar
• Finkel R, Hughes S, Parker J, et al. Selected oral presentation: fetal therapy for spinal muscular atrophy: a case report. Presented at: World Muscle Society; 2022 Oct 11-15; Halifax, NS.
   Google Scholar
• Proud CM, Mercuri E, Finkel RS, et al. Combination disease-modifying treatment in spinal muscular atrophy: a proposed classification. Ann Clin Transl Neurol. 2023. In press.
   PubMed Web of Science ®Google Scholar
• Grotto S, Cuisset JM, Marret S, et al. Type 0 spinal muscular atrophy: further delineation of prenatal and postnatal features in 16 patients. J Neuromuscul Dis. 2016;3(4):487–495. doi: 10.3233/JND-160177
   PubMedGoogle Scholar
• Matesanz SE, Curry C, Gross B, et al. Clinical course in a patient with spinal muscular atrophy type 0 treated with nusinersen and Onasemnogene abeparvovec. J Child Neurol. 2020;35(11):717–723. doi: 10.1177/0883073820928784
   PubMed Web of Science ®Google Scholar
• Ajjarapu A, Mathews DK, Ramachandra D The use of Onasemnogene-abeparvovec at 33 weeks’ gestation in spinal muscular atrophy with one copy of SMN2. Poster session presented at: 2023 Annual Meeting of the American Academy of Neurology; 2023 Apr 22-27: Boston, MA.
   Google Scholar
• Blaschek A, Kölbel H, Schwartz O, et al. Newborn screening for SMA - Can a wait-and-see strategy be responsibly justified in patients with four SMN2 copies? J Neuromuscul Dis. 2022;9(5):597–605. doi: 10.3233/JND-221510
   PubMedGoogle Scholar
• Dangouloff T, Botty C, Beaudart C, et al. Systematic literature review of the economic burden of spinal muscular atrophy and economic evaluations of treatments. Orphanet J Rare Dis. 2021;16(1):47. doi: 10.1186/s13023-021-01695-7
   PubMed Web of Science ®Google Scholar
• Dangouloff T, Hiligsmann M, Deconinck N, et al. Financial cost and quality of life of patients with spinal muscular atrophy identified by symptoms or newborn screening. Dev Med Child Neurol. 2023;65(1):67–77. doi: 10.1111/dmcn.15286
   PubMed Web of Science ®Google Scholar
• Weidlich D, Servais L, Kausar I, et al. Cost-effectiveness of newborn screening for spinal muscular atrophy in England. Neurol Ther. 2023;12(4):1205–1220. doi: 10.1007/s40120-023-00489-2
   PubMed Web of Science ®Google Scholar
• Shih STF, Keller E, Wiley V, et al. Modelling the cost-effectiveness and budget impact of a newborn screening program for spinal muscular atrophy and severe combined immunodeficiency. Int J Neonatal Screen. 2022;8(3):45. doi: 10.3390/ijns8030045
   PubMed Web of Science ®Google Scholar
• Velikanova R, van der Schans S, Bischof M, et al. Cost-effectiveness of newborn screening for spinal muscular atrophy in the Netherlands. Value Health. 2022;25(10):1696–1704. doi: 10.1016/j.jval.2022.06.010
   PubMed Web of Science ®Google Scholar
• Pane M, Berti B, Capasso A, et al. Onasemnogene abeparvovec in spinal muscular atrophy: predictors of efficacy and safety in naïve patients with spinal muscular atrophy and following switch from other therapies. EClinicalMedicine. 2023;59:101997. doi: 10.1016/j.eclinm.2023.101997
   PubMedGoogle Scholar
• Olkhovych N, Gorovenko N, Servais L. Universal newborn screening for spinal muscular atrophy in Ukraine. Lancet. 2023 Jul 22;402(10398):288–289. doi: 10.1016/S0140-6736(23)01281-3
   PubMed Web of Science ®Google Scholar