Matching-adjusted indirect treatment comparison of onasemnogene abeparvovec and nusinersen for the treatment of symptomatic patients with spinal muscular atrophy type 1

References

• Kolb SJ, Kissel JT. Spinal muscular atrophy. Neurol Clin. 2015;33(4):831–846.
   PubMed Web of Science ®Google Scholar
• Sheng-Yuan Z, Xiong F, Chen YJ, et al. Molecular characterization of SMN copy number derived from carrier screening and from core families with SMA in a Chinese population. Eur J Hum Genet. 2010;18(9):978–984.
   PubMed Web of Science ®Google Scholar
• Messina S, Sframeli M. New Treatments in spinal muscular atrophy: positive results and new challenges. JCM. 2020;9(7):2222.
   Web of Science ®Google Scholar
• Lefebvre S, Burglen L, Reboullet S, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80(1):155–165.
   PubMed Web of Science ®Google Scholar
• Sugarman EA, Nagan N, Zhu H, et al. Pan-ethnic carrier screening and prenatal diagnosis for spinal muscular atrophy: clinical laboratory analysis of >72,400 specimens. Eur J Hum Genet. 2012;20(1):27–32.
   PubMed Web of Science ®Google Scholar
• Finkel RS, Mercuri E, Meyer OH, 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. 2018;28(3):197–207.
   PubMed Web of Science ®Google Scholar
• Mercuri E, Finkel RS, Muntoni F, et al. Diagnosis and management of spinal muscular atrophy: part 1 recommendations for diagnosis, rehabilitation, orthopedic and nutritional care. Neuromuscul Disord. 2018;28(2):103–115.
   PubMed Web of Science ®Google Scholar
• Awano T, Kim JK, Monani UR. Spinal muscular atrophy: journeying from bench to bedside. Neurotherapeutics. 2014;11(4):786–795.
   PubMed Web of Science ®Google Scholar
• Arnold WD, Kassar D, Kissel JT. Spinal muscular atrophy: diagnosis and management in a new therapeutic era. Muscle Nerve. 2015;51(2):157–167.
   PubMed Web of Science ®Google Scholar
• Ogino S, Wilson RB, Gold B. New insights on the evolution of the SMN1 and SMN2 region: simulation and meta-analysis for allele and haplotype frequency calculations. Eur J Hum Genet. 2004;12(12):1015–1023.
   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.
   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.
   PubMed Web of Science ®Google Scholar
• Mercuri E, Lucibello S, Perulli M, et al. Longitudinal natural history of type I spinal muscular atrophy: a critical review. Orphanet J Rare Dis. 2020;15(1):84.
   PubMed Web of Science ®Google Scholar
• Wirth B, Karakaya M, Jeong Kye M, et al. Twenty-five years of spinal muscular atrophy research: from phenotype to genotype to therapy, and what comes next. Annu Rev Genom Hum Genet. 2020;21(1):231–261.
   PubMed Web of Science ®Google Scholar
• Lorson CL, Hahnen E, Androphy EJ, et al. A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci U S A. 1999;96(11):6307–6311.
   PubMed Web of Science ®Google Scholar
• Calucho M, Bernal S, Alias 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. Neuromuscul Disord. 2018;28(3):208–215.
   PubMed Web of Science ®Google Scholar
• Monnette A, Chen E, Hong D, et al. Treatment preference among patients with spinal muscular atrophy (SMA): a discrete choice experiment. Orphanet J Rare Dis. 2021;16(1):36.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Al-Zaidy S, Shell R, et al. Single-dose gene-replacement therapy for spinal muscular atrophy. N Engl J Med. (18)2017;377:1713–1722.
   PubMed Web of Science ®Google Scholar
• US Food & Drug Administration. FDA approves innovative gene therapy to treat pediatric patients with spinal muscular atrophy, a rare disease and leading genetic cause of infant mortality. Available from: https://www.fda.gov/news-events/press-announcements/fda-approves-innovative-gene-therapy-treat-pediatric-patients-spinal-muscular-atrophy-rare-disease#:∼:text=The%20U.S.%20Food%20and%20Drug,genetic%20cause%20of%20infant%20mortality
   Google Scholar
• European Medicines Agency. Zolgensma. Available from: https://www.ema.europa.eu/en/medicines/human/EPAR/zolgensma#authorisation-details-section
   Google Scholar
• US Food & Drug Administration. FDA approves first drug for spinal muscular atrophy. Available from: https://www.fda.gov/news-events/press-announcements/fda-approves-first-drug-spinal-muscular-atrophy#:∼:text=The%20U.S.%20Food%20and%20Drug,affecting%20muscle%20strength%20and%20movement
   Google Scholar
• European Medicines Agency. Spinraza. Available from: https://www.ema.europa.eu/en/medicines/human/EPAR/spinraza
   Google Scholar
• US Food & Drug Administration. FDA approves first oral drug treatment for spinal muscular atrophy. Available from: https://www.news-medical.net/news/20200807/FDA-approves-first-oral-drug-for-treatment-of-spinal-muscular-atrophy.aspx
   Google Scholar
• Stavarachi M, Apostol P, Toma M, et al. Spinal muscular atrophy disease: a literature review for therapeutic strategies. J Med Life. 2010;3(1):3–9.
   PubMedGoogle Scholar
• Schorling DC, Pechmann A, Kirschner J. Advances in treatment of spinal muscular atrophy: new phenotypes, new challenges, new implications for care. J Neuromuscul Dis. 2020;7(1):1–13.
   PubMedGoogle Scholar
• Hua Y, Sahashi K, Hung G, et al. Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev. 2010;24(15):1634–1644.
   PubMed Web of Science ®Google Scholar
• Poirier A, Weetall M, Heinig K, et al. Risdiplam distributes and increases SMN protein in both the central nervous system and peripheral organs. Pharmacol Res Perspect. 2018;6(6):e00447.
   PubMed Web of Science ®Google Scholar
• Sivaramakrishnan M, McCarthy KD, Campagne S, et al. Binding to SMN2 pre-mRNA-protein complex elicits specificity for small molecule splicing modifiers. Nat Commun. 2017;8(1):1476.
   PubMed Web of Science ®Google Scholar
• Wurster CD, Ludolph AC. Nusinersen for spinal muscular atrophy. Ther Adv Neurol Disord. 2018;11:1756285618754459.
   Web of Science ®Google Scholar
• Evrysdi. Evrysdi prescribing information. 2021. Available from: https://www.gene.com/download/pdf/evrysdi_prescribing.pdf
   Google Scholar
• European Medicines Agency. Evrysdi. Available from: https://www.ema.europa.eu/en/medicines/human/EPAR/evrysdi
   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.
   PubMed Web of Science ®Google Scholar
• Day JD, 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.
   PubMed Web of Science ®Google Scholar
• Lowes L, Alfano LN, Arnold WD, et al. Impact of age and motor function in a phase 1/2A study of infants with SMA type 1 receiving single-dose gene replacement therapy. Pediatr Neurol. 2019;19:30280–30282.
   Google Scholar
• Al-Zaidy SA, Kolb SJ, Lowes L, et al. AVXS-101 (onasemnogene abeparvovec) for SMA1: comparative study with a prospective natural history cohort. J Neuromuscul Dis. 2019;6(3):307–317.
   PubMedGoogle Scholar
• Chiriboga CA, Swoboda KJ, Darras BT, et al. Results from a phase 1 study of nusinersen (ISIS-SMN(Rx)) in children with spinal muscular atrophy. Neurology. 2016;86(10):890–897.
   PubMed Web of Science ®Google Scholar
• Castro D, Farrar M, Finkel R, et al. Interim report on the safety and efficacy of longer-term treatment with nusinersen in infantile-onset spinal muscular atrophy: results from the SHINE study. Neuromuscul Disord. 2018;28(2):S79–S80.
   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.
   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.
   PubMed Web of Science ®Google Scholar
• Kirschner J, Darras B, Farrar M, et al. Interim report on the safety and efficacy of longer-term treatment with nusinersen in later-onset spinal muscular atrophy (SMA): results from the SHINE study. Neuromuscul Disord. 2019;29:S184.
   Web of Science ®Google Scholar
• De Vivo DC, Bertini E, Swoboda KJ, 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. 2019;29(11):842–856.
   PubMed Web of Science ®Google Scholar
• Singh RN, Ottesen EW, Singh NN. The first orally deliverable small molecule for the treatment of spinal muscular atrophy. Neurosci Insights. 2020;15:2633105520973985.
   Google Scholar
• Ojala KS, Reedich EJ, DiDonato CJ, et al. In search of a cure: the development of therapeutics to alter the progression of spinal muscular atrophy. Brain Sci. 2021;11(2):194.
   PubMed Web of Science ®Google Scholar
• Phillippo DM, Ades AE, Dias S, et al. Methods for population-adjusted indirect comparisons in health technology appraisal. Med Decis Making. 2018;38(2):200–211.
   PubMed Web of Science ®Google Scholar
• Signorovitch JE, Sikirica V, Erder MH, et al. Matching-adjusted indirect comparisons: a new tool for timely comparative effectiveness research. Value Health. 2012;15(6):940–947.
   PubMed Web of Science ®Google Scholar
• Phillippo DM, Ades A, Dias S, et al. NICE DSU technical support document 18: methods for population-adjusted indirect comparisons in submission to NICE [Internet]. 2016 [cited 2019 Dec 11]. Available from: http://nicedsu.org.uk/wp-content/uploads/2018/08/Population-adjustment-TSD-FINAL-ref-rerun.pdf
   Google Scholar
• Dias S, Sutton AJ, Ades AE, et al. Evidence synthesis for decision making 2: a generalized linear modeling framework for pairwise and network meta-analysis of randomized controlled trials. Med Decis Making. 2013;33(5):607–617.
   PubMed Web of Science ®Google Scholar
• Bucher HC, Guyatt GH, Griffith LE, et al. The results of direct and indirect treatment comparisons in meta-analysis of randomized controlled trials. J Clin Epidemiol. 1997;50(6):683–691.
   PubMed Web of Science ®Google Scholar
• Ishak KJ, Proskorovsky I, Benedict A. Simulation and matching based approaches for indirect comparisons of treatments. Pharmacoeconomics. 2015;33(6):537–549.
   PubMed Web of Science ®Google Scholar
• Thom H, Jugl SM, Palaka E, et al. Matching adjusted indirect comparisons to assess comparative effectiveness of therapies: usage in scientific literature and health technology appraisals. Value Health. 2016;19(3):A100–A101.
   Web of Science ®Google Scholar
• Phillippo DM, Dias S, Elsada A, et al. Population adjustment methods for indirect comparisons: a review of National Institute for Health and Care Excellence Technology Appraisals. Int J Technol Assess Health Care. 2019;35(3):221–228.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
   PubMed Web of Science ®Google Scholar
• Finkel R, Castro D, Farrar M, et al. Interim report on the safety and efficacy of longer-term treatment with nusinersen in infantile-onset spinal muscular atrophy (SMA): updated results from the SHINE study. Neurology. 2019;92(15 Suppl):S25.004.
   Web of Science ®Google Scholar
• Glanzman AM, McDermott MP, Montes J, et al. Validation of the Children’s Hospital of Philadelphia Infant Test of Neuromuscular Disorders (CHOP INTEND). Pediatr Phys Ther. 2011;23(4):322–326.
   PubMed Web of Science ®Google Scholar
• Li YJ, Chen TH, Wu YZ, et al. Metabolic and nutritional issues associated with spinal muscular atrophy. Nutrients. 2020;12(12):3842.
   PubMed Web of Science ®Google Scholar
• van der Heul AMB, Cuppen I, Wadman RI, et al. Feeding and swallowing problems in infants with spinal muscular atrophy type 1: an observational study. J Neuromuscul Dis. 2020;7(3):323–330.
   PubMedGoogle Scholar
• Pane M, Palermo C, Messina S, et al. An observational study of functional abilities in infants, children, and adults with type 1 SMA. Neurology. 2018;91(8):e696–e703.
   PubMed Web of Science ®Google Scholar
• Acsadi G, Crawford TO, Müller-Felber W, et al. Safety and efficacy of nusinersen in spinal muscular atrophy: the EMBRACE study. Muscle Nerve. 2021;63(5):668–677.
   PubMed Web of Science ®Google Scholar
• Darras BT, Chiriboga CA, Iannaccone ST, et al. Nusinersen in later-onset spinal muscular atrophy: long-term results from the phase 1/2 studies. Neurology. 2019;92(21):e2492–e2506.
   PubMed Web of Science ®Google Scholar
• Dabbous O, Benit M, Jansen JP, et al. Survival, motor function, and motor milestones: comparison of AVXS-101 relative to nusinersen for the treatment of infants with spinal muscular atrophy. Adv Ther. 2019;36(5):1164–1176.
   PubMed Web of Science ®Google Scholar
• Welton NJ, Phillippo DM, Owen R, et al. CHTE2020 sources and synthesis of evidence: update to evidence synthesis methods. March 2020. Available from: CHTE-2020_final_20April2020_final.pdf(nicedsu.org.uk)
   Google Scholar
• Daigl M, Kotzeva A, Gorni K, et al. How does risdiplam compare in infantile-onset spinal muscular atrophy (SMA)? Preliminary indirect treatment comparisons based on FIREFISH part 1 data. Poster presented at ISPOR Europe; 2019 Nov 2–6; Copenhagen, Denmark.
   Google Scholar
• Liao S, Bohn J, de Moor C, et al. PRO109 a cautionary TALE for indirect treatment comparisons: an example from infantile-onset spinal muscular atrophy. Value Health. 2020;23(Suppl 2):S709.
   Google Scholar
• Guyot P, Ades AE, Ouwens MJ, et al. Enhanced secondary analysis of survival data: reconstructing the data from published Kaplan–Meier survival curves. BMC Med Res Methodol. 2012;12:9.
   PubMed Web of Science ®Google Scholar