Spinal muscular atrophy - insights and challenges in the treatment era.
Journal
Nature reviews. Neurology
ISSN: 1759-4766
Titre abrégé: Nat Rev Neurol
Pays: England
ID NLM: 101500072
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
accepted:
07
09
2020
pubmed:
16
10
2020
medline:
14
1
2022
entrez:
15
10
2020
Statut:
ppublish
Résumé
Spinal muscular atrophy (SMA) is an autosomal recessive motor neuron disease caused by deletion or mutation of SMN1. Four subtypes exist, characterized by different clinical severities. New therapeutic approaches have become available in the past few years, dramatically changing the natural history of all SMA subtypes, including substantial clinical improvement with the severe and advanced SMA type 1 variant. Trials have now demonstrated that phenotypic rescue is even more dramatic when pre-symptomatic patients are treated, and emerging real-world data are demonstrating the benefits of intervention even in the chronic phase of the condition. Here, we critically review how the field is rapidly evolving in response to the new therapies and questions that the new treatments have posed, including the effects of treatment at different ages and stages of disease, new phenotypes and long-term outcomes in patients who would not have survived without treatment, and decisions of who to treat and when. We also discuss how the outcomes associated with different timing of therapeutic intervention are contributing to our understanding of the biology and pathogenesis of SMA.
Identifiants
pubmed: 33057172
doi: 10.1038/s41582-020-00413-4
pii: 10.1038/s41582-020-00413-4
doi:
Substances chimiques
SMN1 protein, human
0
Survival of Motor Neuron 1 Protein
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
706-715Références
Kolb, S. J. & Kissel, J. T. Spinal muscular atrophy: a timely review. Arch. Neurol. 68, 979–984 (2011).
pubmed: 21482919
Sangare, M. et al. Genetics of low spinal muscular atrophy carrier frequency in sub-Saharan Africa. Ann. Neurol. 75, 525–532 (2014).
pubmed: 24515897
pmcid: 4112719
Cusin, V., Clermont, O., Gerard, B., Chantereau, D. & Elion, J. Prevalence of SMN1 deletion and duplication in carrier and normal populations: implication for genetic counselling. J. Med. Genet. 40, e39 (2003).
pubmed: 12676912
pmcid: 1735434
Vorster, E., Essop, F. B., Rodda, J. L. & Krause, A. Spinal muscular atrophy in the Black South African population: a matter of rearrangement? Front. Genet. 11, 54 (2020).
pubmed: 32117462
pmcid: 7033609
Dubowitz, V. Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur. J. Paediatr. Neurol. 3, 49–51 (1999).
pubmed: 10700538
Finkel, R., Bertini, E., Muntoni, F., Mercuri, E. & ENMC SMA Workshop Study Group. 209th ENMC International Workshop: Outcome Measures and Clinical Trial Readiness in Spinal Muscular Atrophy 7–9 November 2014, Heemskerk, The Netherlands. Neuromuscul. Disord. 25, 593–602 (2015).
pubmed: 26045156
Burghes, A. H. & Beattie, C. E. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat. Rev. Neurosci. 10, 597–609 (2009).
pubmed: 19584893
pmcid: 2853768
Feldkotter, M., Schwarzer, V., Wirth, R., Wienker, T. F. & Wirth, B. Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am. J. Hum. Genet. 70, 358–368 (2002).
pubmed: 11791208
Lefebvre, S. et al. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat. Genet. 16, 265–269 (1997).
pubmed: 9207792
Calucho, M. et al. Correlation between SMA type and SMN2 copy number revisited: san analysis of 625 unrelated Spanish patients and a compilation of 2834 reported cases. Neuromuscul. Disord. 28, 208–215 (2018). This large study demonstrates the correlation between SMN2 copy number and clinical outcomes.
pubmed: 29433793
Wirth, B., Karakaya, M., Kye, M. J. & Mendoza-Ferreira, N. Twenty-five years of spinal muscular atrophy research: from phenotype to genotype to therapy, and what comes next. Annu. Rev. Genomics Hum. Genet. 21, 231–261 (2020).
pubmed: 32004094
Bernal, S. et al. The c.859G>C variant in the SMN2 gene is associated with types II and III SMA and originates from a common ancestor. J. Med. Genet. 47, 640–642 (2010).
pubmed: 20577007
Riessland, M. et al. Neurocalcin δ suppression protects against spinal muscular atrophy in humans and across species by restoring impaired endocytosis. Am. J. Hum. Genet. 100, 297–315 (2017).
pubmed: 28132687
pmcid: 5294679
Hosseinibarkooie, S., Schneider, S. & Wirth, B. Advances in understanding the role of disease-associated proteins in spinal muscular atrophy. Expert Rev. Proteom. 14, 581–592 (2017).
Hosseinibarkooie, S. et al. The power of human protective modifiers: PLS3 and CORO1C unravel impaired endocytosis in spinal muscular atrophy and rescue SMA phenotype. Am. J. Hum. Genet. 99, 647–665 (2016). This study identifies genes that can modify SMA disease severity in preclinical models.
pubmed: 27499521
pmcid: 5011078
Finkel, R. S. et al. Diagnosis and management of spinal muscular atrophy: Part 2: pulmonary and acute care; medications, supplements and immunizations; other organ systems; and ethics. Neuromuscul. Disord. 28, 197–207 (2018).
pubmed: 29305137
Mercuri, E. et al. Diagnosis and management of spinal muscular atrophy: Part 1: recommendations for diagnosis, rehabilitation, orthopedic and nutritional care. Neuromuscul. Disord. 28, 103–115 (2018).
pubmed: 29290580
Farrar, M. A. et al. Emerging therapies and challenges in spinal muscular atrophy. Ann. Neurol. 81, 355–368 (2017).
pubmed: 28026041
pmcid: 5396275
Sumner, C. J. & Crawford, T. O. Two breakthrough gene-targeted treatments for spinal muscular atrophy: challenges remain. J. Clin. Invest. 128, 3219–3227 (2018).
pubmed: 29985170
pmcid: 6063504
Passini, M. A. et al. Antisense oligonucleotides delivered to the mouse CNS ameliorate symptoms of severe spinal muscular atrophy. Sci. Transl Med. 3, 72ra18 (2011).
pubmed: 21368223
pmcid: 3140425
Hua, Y. et al. Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev. 24, 1634–1644 (2010).
pubmed: 20624852
pmcid: 2912561
Finkel, R. S. et al. Nusinersen versus sham control in infantile-onset spinal muscular atrophy. N. Engl. J. Med. 377, 1723–1732 (2017). This paper presents a seminal phase III trial of the antisense oligonucleotide nusinersen in infants with SMA-I.
pubmed: 29091570
Mercuri, E. et al. Nusinersen versus sham control in later-onset spinal muscular atrophy. N. Engl. J. Med. 378, 625–635 (2018). This paper presents a seminal phase III trial of nusinersen in children with chronic forms of SMA-II and SMA-III.
pubmed: 29443664
Darras, B. T. et al. Nusinersen in later-onset spinal muscular atrophy: long-term results from the phase 1/2 studies. Neurology 92, e2492–e2506 (2019).
pubmed: 31019106
pmcid: 6541434
De Vivo, D. C. et al. Nusinersen initiated in infants during the presymptomatic stage of spinal muscular atrophy: interim efficacy and safety results from the phase 2 NURTURE study. Neuromuscul. Disord. 29, 842–856 (2019). This paper presents the first study of nusinersen in pre-symptomatic infants with SMA-I and SMA-II who were identified through family studies or newborn screening.
pubmed: 31704158
pmcid: 7127286
Sivaramakrishnan, M. et al. Binding to SMN2 pre-mRNA–protein complex elicits specificity for small molecule splicing modifiers. Nat. Commun. 8, 1476 (2017). This paper presents the identification of a small molecule that can selectively induce SMN2 exon 7 retention in the mRNA.
pubmed: 29133793
pmcid: 5684323
Poirier, A. et al. Risdiplam distributes and increases SMN protein in both the central nervous system and peripheral organs. Pharmacol. Res. Perspect. 6, e00447 (2018). This paper presents the first-in-human study of an AAV replacement therapy for infants with SMA-I.
pubmed: 30519476
pmcid: 6262736
Ratni, H. et al. Discovery of risdiplam, a selective survival of motor neuron-2 (SMN2) gene splicing modifier for the treatment of spinal muscular atrophy (SMA). J. Med. Chem. 61, 6501–6517 (2018).
pubmed: 30044619
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT02913482 (2020).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT02908685 (2020).
Baranello, G. et al. FIREFISH Part 1: early clinical results following a significant increase of SMN protein in SMA type 1 babies treated with RG7916. INeuromuscular Disord. 28, S109 (2018).
Mercuri, E. M. et al. SUNFISH Part 1: RG7916 treatment results in a sustained increase of SMN protein levels and the first clinical efficacy results in patients with type 2 or 3 SMA. Neuromuscul. Disord. 28, S108 (2018).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03779334 (2020).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03032172 (2020).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT02268552 (2020).
Foust, K. D. et al. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol. 228, 271–274 (2010).
Mendell, J. R. et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N. Engl. J. Med. 377, 1713–1722 (2017).
pubmed: 29091557
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03306277 (2020).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03461289 (2020).
Day, J. W. et al. Onasemnogene abeparvovec-xioi gene-replacement therapy for spinal muscular atrophy type 1 (SMA1): phase 3 US study (STR1VE) update (1828). Neurology 94, 1828 (2020).
Strauss, K. A. et al. Onasemnogene abeparvovec-xioi gene-replacement therapy in presymptomatic spinal muscular atrophy: SPR1NT study update (2384). Neurology 94, 2384 (2020).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03505099 (2020).
European Medicines Agency. Zolgensma summary of product characteristics https://www.ema.europa.eu/en/documents/product-information/zolgensma-epar-product-information_en.pdf (2020).
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03381729 (2020).
Novartis. Novartis announces AVXS-101 intrathecal study update https://www.novartis.com/news/media-releases/novartis-announces-avxs-101-intrathecal-study-update (2019).
Mendell, J. R. et al. Gene-replacement therapy in spinal muscular atrophy type 1: long-term follow-up from the onasemnogene abeparvovec-xioi phase 1/2a clinical trial (1808). Neurology 94, 1808 (2020).
Ronzitti, G. et al. Human, immune responses to adeno-associated virus (AAV) vectors. Front. Immunol. 11, 670 (2020).
pubmed: 32362898
pmcid: 7181373
Mariot, V. et al. Downregulation of myostatin pathway in neuromuscular diseases may explain challenges of anti-myostatin therapeutic approaches. Nat. Commun. 8, 1859 (2017).
pubmed: 29192144
pmcid: 5709430
Zhou, H. et al. Myostatin inhibition in combination with antisense oligonucleotide therapy improves outcomes in spinal muscular atrophy. J. Cachexia Sarcopenia Muscle 11, 768–782 (2020).
pubmed: 32031328
pmcid: 7296258
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT03819660 (2020).
Harding, B. N. et al. Spectrum of neuropathophysiology in spinal muscular atrophy type I. J. Neuropathol. Exp. Neurol. 74, 15–24 (2015).
pubmed: 25470343
pmcid: 4350580
Finkel, R. S. Electrophysiological and motor function scale association in a pre-symptomatic infant with spinal muscular atrophy type I. Neuromuscul. Disord. 23, 112–115 (2013).
pubmed: 23146148
Swoboda, K. J. et al. Natural history of denervation in SMA: relation to age, SMN2 copy number, and function. Ann. Neurol. 57, 704–712 (2005).
pubmed: 15852397
pmcid: 4334582
Swoboda, K. J. et al. SMA CARNI-VAL trial part I: double-blind, randomized, placebo-controlled trial of L-carnitine and valproic acid in spinal muscular atrophy. PLoS ONE 5, e12140 (2010).
pubmed: 20808854
pmcid: 2924376
Kang, P. B. et al. The motor neuron response to SMN1 deficiency in spinal muscular atrophy. Muscle Nerve 49, 636–644 (2014).
pubmed: 23893312
pmcid: 4090017
Kolb, S. J. et al. Baseline results of the NeuroNEXT spinal muscular atrophy infant biomarker study. Ann. Clin. Transl Neurol. 3, 132–145 (2016).
pubmed: 26900585
pmcid: 4748311
Kolb, S. J. et al. Natural history of infantile-onset spinal muscular atrophy. Ann. Neurol. 82, 883–891 (2017).
pubmed: 29149772
pmcid: 5776712
Pane, M. et al. Longitudinal assessments in discordant twins with SMA. Neuromuscul. Disord. 27, 890–893 (2017).
pubmed: 28797588
Ramos, D. M. et al. Age-dependent SMN expression in disease-relevant tissue and implications for SMA treatment. J. Clin. Invest. 129, 4817–4831 (2019). This study demonstrates developmental expression of SMN with implications for disease pathogenesis and response to SMN augmentation therapies.
pubmed: 31589162
pmcid: 6819103
Cifuentes-Diaz, C. et al. Neurofilament accumulation at the motor endplate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum. Mol. Genet. 11, 1439–1447 (2002).
pubmed: 12023986
Kariya, S. et al. Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum. Mol. Genet. 17, 2552–2569 (2008).
pubmed: 18492800
pmcid: 2722888
Murray, L. M. et al. Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum. Mol. Genet. 17, 949–962 (2008).
pubmed: 18065780
Kong, L. et al. Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J. Neurosci. 29, 842–851 (2009).
pubmed: 19158308
pmcid: 2746673
Braun, S., Croizat, B., Lagrange, M. C., Warter, J. M. & Poindron, P. Constitutive muscular abnormalities in culture in spinal muscular atrophy. Lancet 345, 694–695 (1995).
pubmed: 7741893
Arnold, A. S. et al. Reduced expression of nicotinic AChRs in myotubes from spinal muscular atrophy I patients. Lab. Invest. 84, 1271–1278 (2004).
pubmed: 15322565
Wishart, T. M. et al. Dysregulation of ubiquitin homeostasis and β-catenin signaling promote spinal muscular atrophy. J. Clin. Invest. 124, 1821–1834 (2014).
pubmed: 24590288
pmcid: 3973095
Martinez-Hernandez, R. et al. Synaptic defects in type I spinal muscular atrophy in human development. J. Pathol. 229, 49–61 (2013).
pubmed: 22847626
Wadman, R. I., Vrancken, A. F., van den Berg, L. H. & van der Pol, W. L. Dysfunction of the neuromuscular junction in spinal muscular atrophy types 2 and 3. Neurology 79, 2050–2055 (2012).
pubmed: 23115209
Pera, M. C. et al. 6MWT can identify type 3 SMA patients with neuromuscular junction dysfunction. Neuromuscul. Disord. 27, 879–882 (2017).
pubmed: 28803817
Montes, J. et al. A randomized, controlled clinical trial of exercise in patients with spinal muscular atrophy: methods and baseline characteristics. J. Neuromuscul. Dis. 1, 151–161 (2014).
pubmed: 27858768
Montes, J. et al. Six-minute walk test demonstrates motor fatigue in spinal muscular atrophy. Neurology 74, 833–838 (2010).
pubmed: 20211907
pmcid: 2839195
Montes, J. et al. Leg muscle function and fatigue during walking in spinal muscular atrophy type 3. Muscle Nerve 50, 34–39 (2014).
pubmed: 24122959
Mazzone, E. et al. Six minute walk test in type III spinal muscular atrophy: a 12-month longitudinal study. Neuromuscul. Disord. 23, 624–628 (2013).
pubmed: 23809874
Montes, J. et al. Nusinersen improves walking distance and reduces fatigue in later-onset spinal muscular atrophy. Muscle Nerve 60, 409–414 (2019).
pubmed: 31298747
pmcid: 6771553
Ghazanfari, N., Morsch, M., Tse, N., Reddel, S. W. & Phillips, W. D. Effects of the β2-adrenoceptor agonist, albuterol, in a mouse model of anti-MuSK myasthenia gravis. PLoS ONE 9, e87840 (2014).
pubmed: 24505322
pmcid: 3914858
Kinali, M. et al. Pilot trial of albuterol in spinal muscular atrophy. Neurology 59, 609–610 (2002).
pubmed: 12196659
Pane, M. et al. Daily salbutamol in young patients with SMA type II. Neuromuscul. Disord. 18, 536–540 (2008).
pubmed: 18579379
Khirani, S. et al. Effect of salbutamol on respiratory muscle strength in spinal muscular atrophy. Pediatr. Neurol. 73, 78–87 (2017).
pubmed: 28668232
Pera, M. C. et al. Does albuterol have an effect on neuromuscular junction dysfunction in spinal muscular atrophy? Neuromuscul. Disord. 28, 863–864 (2018).
pubmed: 30177455
Stam, M. et al. Protocol for a phase II, monocentre, double-blind, placebo-controlled, cross-over trial to assess efficacy of pyridostigmine in patients with spinal muscular atrophy types 2–4 (SPACE trial). BMJ Open 8, e019932 (2018).
pubmed: 30061431
pmcid: 6067401
Messina, S. et al. Expanded access program with nusinersen in SMA type I in Italy: strengths and pitfalls of a successful experience. Neuromuscul. Disord. 27, 1084–1086 (2017).
pubmed: 29132728
Walter, M. C. et al. Safety and treatment effects of nusinersen in longstanding adult 5q-SMA type 3—a prospective observational study. J. Neuromuscul. Dis. 6, 453–465 (2019).
pubmed: 31594243
pmcid: 6918909
Pane, M. et al. Nusinersen in type 1 spinal muscular atrophy: twelve-month real-world data. Ann. Neurol. 86, 443–451 (2019).
pubmed: 31228281
Aragon-Gawinska, K. et al. Sitting in patients with spinal muscular atrophy type 1 treated with nusinersen. Dev. Med. Child. Neurol. 62, 310–314 (2020).
pubmed: 31799720
Pechmann, A. et al. Evaluation of children with SMA type 1 under treatment with nusinersen within the expanded access program in Germany. J. Neuromuscul. Dis. 5, 135–143 (2018).
pubmed: 29689734
pmcid: 6004898
Pechmann, A., Langer, T., Wider, S. & Kirschner, J. Single-center experience with intrathecal administration of nusinersen in children with spinal muscular atrophy type 1. Eur. J. Paediatr. Neurol. 22, 122–127 (2018).
pubmed: 29208343
Sansone, V. A. et al. Respiratory needs in patients with type 1 spinal muscular atrophy treated with nusinersen. J. Pediatr. 219, 223–228 (2020).
pubmed: 32035635
LoMauro, A. et al. Effect of nusinersen on respiratory muscle function in different subtypes of type 1 spinal muscular atrophy. Am. J. Respir. Crit. Care Med. 200, 1547–1550 (2019).
pubmed: 31433957
Hagenacker, T. et al. Nusinersen in adults with 5q spinal muscular atrophy: a non-interventional, multicentre, observational cohort study. Lancet Neurol. 19, 317–325 (2020).
pubmed: 32199097
Mercuri, E. & Sansone, V. Nusinersen in adults with spinal muscular atrophy: new challenges. Lancet Neurol. 19, 283–284 (2020).
pubmed: 32199087
Finkel, R. S. et al. RESTORE: a prospective multinational registry of patients with genetically confirmed spinal muscular atrophy—rationale and study design. Neuromuscul. Dis. 7, 145–152 (2020).
Messina, S. et al. A critical review of patient and parent caregiver oriented tools to assess health-related quality of life, activity of daily living and caregiver burden in spinal muscular atrophy. Neuromuscul. Disord. 29, 940–950 (2019).
pubmed: 31791871
Landfeldt, E. et al. Quality of life of patients with spinal muscular atrophy: a systematic review. Eur. J. Paediatr. Neurol. 23, 347–356 (2019).
pubmed: 30962132
Mercuri, E. E. A. Patient and parent oriented tools to assess health-related quality of life, activity of daily living and caregiver burden in SMA. Neuromuscul. Disord. 29, 940–950 (2020).
Pasternak, A. et al. Rasch analysis of the pediatric evaluation of disability inventory-computer adaptive test (PEDI-CAT) item bank for children and young adults with spinal muscular atrophy. Muscle Nerve 54, 1097–1107 (2016).
pubmed: 27121348
Mongiovi, P. et al. Patient Reported Impact of Symptoms in Spinal Muscular Atrophy (PRISM-SMA). Neurology 91, e1206–e1214 (2018).
pubmed: 30143566
pmcid: 6161547
Chen, T. H. New and developing therapies in spinal muscular atrophy: from genotype to phenotype to treatment and where do we stand? Int. J. Mol. Sci. 21, 3297 (2020).
pmcid: 7246502
Schorling, D. C., Pechmann, A. & Kirschner, J. Advances in treatment of spinal muscular atrophy — new phenotypes, new challenges, new implications for care. J. Neuromuscul. Dis. 7, 1–13 (2020).
pubmed: 31707373
pmcid: 7029319
Tizzano, E. F. & Finkel, R. S. Spinal muscular atrophy: a changing phenotype beyond the clinical trials. Neuromuscul. Disord. 27, 883–889 (2017).
pubmed: 28757001
National Institute for Health and Care Excellence. Nusinersin for treating spinal muscular atrophy. Technology appraisal guidance [TA588]. NICE https://www.nice.org.uk/guidance/ta588 (2019).
Yeo, C. J. J. & Darras, B. T. Overturning the paradigm of spinal muscular atrophy as just a motor neuron disease. Pediatr. Neurol. 109, 12–19 (2020). This paper presents a comprehensive review of the implications of peripheral SMN deficiency for patients with SMA.
pubmed: 32409122
Pechmann, A. et al. Treatment with nusinersen — challenges regarding the indication for children with SMA type 1. Neuromuscul. Dis. 7, 41–46 (2020).
Ziegler, A. et al. Recommendations for gene therapy of spinal muscular atrophy with onasemnogene abeparvovec-AVXS-101: consensus paper of the German representatives of the Society for Pediatric Neurology (GNP) and the German treatment centers with collaboration of the medical scientific advisory board of the German Society for Muscular Diseases (DGM)]. Nervenarzt. 91, 518–529 (2020).
pubmed: 32394004
Salazar, R. et al. Quantitative evaluation of lower extremity joint contractures in spinal muscular atrophy: implications for motor function. Pediatr. Phys. Ther. 30, 209–215 (2018).
pubmed: 29924070
Crawford, T. O. et al. Evaluation of SMN protein, transcript, and copy number in the biomarkers for spinal muscular atrophy (BforSMA) clinical study. PLoS ONE 7, e33572 (2012).
pubmed: 22558076
pmcid: 3338744
Finkel, R. S. et al. Candidate proteins, metabolites and transcripts in the Biomarkers for Spinal Muscular Atrophy (BforSMA) clinical study. PLoS ONE 7, e35462 (2012).
pubmed: 22558154
pmcid: 3338723
Lee, Y., Lee, B. H., Yip, W., Chou, P. & Yip, B. S. Neurofilament proteins as prognostic biomarkers in neurological disorders. Curr. Pharm. Des. 25, 4560–4569 (2020).
pubmed: 31820696
Catapano, F. et al. Altered levels of microRNA-9, -206, and -132 in spinal muscular atrophy and their response to antisense oligonucleotide therapy. Mol. Ther. Nucleic Acids 5, e331 (2016).
pubmed: 27377135
pmcid: 5014531
Also-Rallo, E. et al. Treatment of spinal muscular atrophy cells with drugs that upregulate SMN expression reveals inter- and intra-patient variability. Eur. J. Hum. Genet. 19, 1059–1065 (2011).
pubmed: 21610752
pmcid: 3190259
Wilson, J. M. & Jungner, Y. G. Principles and practice of mass screening for disease. Bol. Oficina Sanit. Panam. 65, 281–393 (1968).
pubmed: 4234760
Health Resources and Services Administration. Newborn screening for spinal muscular atrophy. A summary of the evidence and advisory committee decision https://www.hrsa.gov/sites/default/files/hrsa/advisory-committees/heritable-disorders/rusp/previous-nominations/sma-consumer-summary.pdf (2018).
Glascock, J. et al. Treatment algorithm for infants diagnosed with spinal muscular atrophy through newborn screening. J. Neuromuscul. Dis. 5, 145–158 (2018).
pubmed: 29614695
pmcid: 6004919
Glascock, J. 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. 7, 97–100 (2020).
pubmed: 32007960
pmcid: 7175931
Schorling, D. C. et al. Discrepancy in redetermination of SMN2 copy numbers in children with SMA. Neurology 93, 267–269 (2019).
pubmed: 31235659
US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT02644668 (2020).