Efficacy and Safety of Fenfluramine in Epilepsy: A Systematic Review and Meta-analysis.

Dravet syndrome Epilepsy Fenfluramine Lennox–Gastaut syndrome Seizures

Journal

Neurology and therapy
ISSN: 2193-8253
Titre abrégé: Neurol Ther
Pays: New Zealand
ID NLM: 101637818

Informations de publication

Date de publication:
Apr 2023
Historique:
received: 07 01 2023
accepted: 07 02 2023
medline: 1 3 2023
pubmed: 1 3 2023
entrez: 28 2 2023
Statut: ppublish

Résumé

Fenfluramine (FFA) is an amphetamine derivative that promotes the release and blocks the neuronal reuptake of serotonin. Initially introduced as an appetite suppressant, FFA also showed antiseizure properties. This systematic review aimed to assess the efficacy and safety of FFA for the treatment of seizures in patients with epilepsy. We systematically searched (in week 3 of June 2022) MEDLINE, the Cochrane Central Register of Controlled Trials, and the US National Institutes of Health Clinical Trials Registry. Randomized, double- or single-blinded, placebo-controlled studies of FFA in patients with epilepsy and uncontrolled seizures were identified. Efficacy outcomes included the proportions of patients with ≥ 50% and 100% reductions in baseline seizure frequency during the treatment period. Tolerability outcomes included the proportions of patients who withdrew from treatment for any reason and suffered adverse events (AEs). The risk of bias in the included studies was assessed according to the recommendations of the Cochrane Handbook for Systematic Reviews of Interventions. The risk ratio (RR) along with the 95% confidence interval (CI) were estimated for each outcome. Three trials were identified and a total of 469 Dravet syndrome (DS) and Lennox-Gastaut syndrome (LGS) subjects were randomized. All three trials were judged to be at low risk of biases. In patients with DS, the RRs for ≥ 50% and 100% reductions in convulsive seizure frequency for the FFA group compared to placebo were 5.61 (95% CI 2.73-11.54) and 4.71 (95% CI 0.57-39.30), respectively. In patients with LGS, the corresponding RRs for ≥ 50% and 100% reductions in drop seizure frequency were 2.58 (95% CI 1.33-5.02) and 0.50 (95% CI 0.031-7.81), respectively. The drug was withdrawn for any reason in 10.1% and 5.8% of patients receiving FFA and placebo, respectively (RR 1.79, 95% CI 0.89-3.59). Treatment discontinuation due to AEs occurred in 5.4% and 1.2% of FFA- and placebo-treated patients, respectively (RR 3.63, 95% CI 0.93-14.16). Decreased appetite, diarrhoea, fatigue, and weight loss were AEs associated with FFA treatment. Fenfluramine reduces the frequency of seizures in patients with DS and LGS. Decreased appetite, diarrhoea, fatigue, and weight loss are non-cardiovascular AEs associated with FFA.

Identifiants

pubmed: 36853503
doi: 10.1007/s40120-023-00452-1
pii: 10.1007/s40120-023-00452-1
pmc: PMC10043095
doi:

Types de publication

Journal Article

Langues

eng

Pagination

669-686

Informations de copyright

© 2023. The Author(s).

Références

Cockerell OC, Johnson AL, Sander JW, Hart YM, Shorvon SD. Remission of epilepsy: results from the national general practice study of epilepsy. Lancet. 1995;346:140–4.
pubmed: 7603228 doi: 10.1016/S0140-6736(95)91208-8
Lattanzi S, Trinka E, Zaccara G, Striano P, Russo E, Del Giovane C, Silvestrini M, Brigo F. Third-generation antiseizure medications for adjunctive treatment of focal-onset seizures in adults: a systematic review and network meta-analysis. Drugs. 2022;82:199–218.
pubmed: 35061214 pmcid: 8843918 doi: 10.1007/s40265-021-01661-4
Josephson CB, Patten SB, Bulloch A, Williams JVA, Lavorato D, Fiest KM, Secco M, Jette N. The impact of seizures on epilepsy outcomes: a national, community-based survey. Epilepsia. 2017;58:764–71.
pubmed: 28345152 doi: 10.1111/epi.13723
Pinder RM, Brogden RN, Sawyer PR, Speight TM, Avery GS. Fenfluramine: a review of its pharmacological properties and therapeutic efficacy in obesity. Drugs. 1975;10:241–323.
pubmed: 765100 doi: 10.2165/00003495-197510040-00001
Rothman RB, Baumann MH. Therapeutic and adverse actions of serotonin transporter substrates. Pharmacol Ther. 2002;95:73–88.
pubmed: 12163129 doi: 10.1016/S0163-7258(02)00234-6
Abenhaim L, Moride Y, Brenot F, et al. Appetite-suppressant drugs and the risk of primary pulmonary hypertension. International Primary Pulmonary Hypertension Study Group. N Engl J Med. 1996;335:609–16.
pubmed: 8692238 doi: 10.1056/NEJM199608293350901
Connolly HM, Crary JL, McGoon MD, Hensrud DD, Edwards BS, Edwards WD, Schaff HV. Valvular heart disease associated with fenfluramine-phentermine. N Engl J Med. 1997;337:581–8.
pubmed: 9271479 doi: 10.1056/NEJM199708283370901
Aicardi J, Gastaut H. Treatment of self-induced photosensitive epilepsy with fenfluramine. N Engl J Med. 1985;313:1419.
pubmed: 3932858 doi: 10.1056/NEJM198511283132219
Schoonjans A-N, Lagae L, Ceulemans B. Low-dose fenfluramine in the treatment of neurologic disorders: experience in Dravet syndrome. Ther Adv Neurol Disord. 2015;8:328–38.
pubmed: 26600876 pmcid: 4643872 doi: 10.1177/1756285615607726
Ceulemans B, Boel M, Leyssens K, et al. Successful use of fenfluramine as an add-on treatment for Dravet syndrome. Epilepsia. 2012;53:1131–9.
pubmed: 22554283 doi: 10.1111/j.1528-1167.2012.03495.x
Ceulemans B, Schoonjans A-S, Marchau F, Paelinck B, Lagae L. Five-year extended follow-up of 10 Dravet patients treated with fenfluramine. Epilepsia. 2016;57:e129–34.
pubmed: 27197941 doi: 10.1111/epi.13407
Schoonjans A, Paelinck BP, Marchau F, et al. Low-dose fenfluramine significantly reduces seizure frequency in Dravet syndrome: a prospective study of a new cohort of patients. Eur J Neurol. 2017;24(2):309–314.
Schoonjans AS, Marchau F, Paelinck BP, et al. Cardiovascular safety of low-dose fenfluramine in Dravet syndrome: a review of its benefit-risk profile in a new patient population. Curr Med Res Opin. 2017;33:1773–81.
pubmed: 28704161 doi: 10.1080/03007995.2017.1355781
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021;10:89.
pubmed: 33781348 pmcid: 8008539 doi: 10.1186/s13643-021-01626-4
Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions, version 5.1.0 (updated March 2011). London: The Cochrane Collaboration; 2011. http://handbook-5-1.cochrane.org/ . Accessed Dec 2021.
Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.
pubmed: 12958120 pmcid: 192859 doi: 10.1136/bmj.327.7414.557
Higgins JP, Thompson SG. Quantifying heterogeneity in a metaanalysis. Stat Med. 2002;21:1539–58.
pubmed: 12111919 doi: 10.1002/sim.1186
Lattanzi S, Trinka E, Zaccara G, et al. Adjunctive cenobamate for focal-onset seizures in adults: a systematic review and meta-analysis. CNS Drugs. 2020;34:1105–20.
pubmed: 32851590 pmcid: 7658084 doi: 10.1007/s40263-020-00759-9
Lattanzi S, Brigo F, Grillo E, Cagnetti C, Verrotti A, Zaccara G, et al. Adjunctive eslicarbazepine acetate in pediatric patients with focal epilepsy: a systematic review and meta-analysis. CNS Drugs. 2018;32:189–96.
pubmed: 29508243 doi: 10.1007/s40263-018-0504-x
Lattanzi S, Grillo E, Brigo F, Silvestrini M. Efficacy and safety of perampanel in Parkinson’s disease. A systematic review with meta-analysis. J Neurol. 2018;265:733–40.
pubmed: 29159466 doi: 10.1007/s00415-017-8681-y
Lattanzi S, Cagnetti C, Danni M, Provinciali L, Silvestrini M. Oral and intravenous steroids for multiple sclerosis relapse: a systematic review and meta-analysis. J Neurol. 2017;264:1697–704.
pubmed: 28492970 doi: 10.1007/s00415-017-8505-0
Lattanzi S, Brigo F, Cagnetti C, Di Napoli M, Silvestrini M. Patent foramen ovale and cryptogenic stroke or transient ischemic attack: to close or not to close? A systematic review and meta-analysis. Cerebrovasc Dis. 2018;45:193–203.
Lagae L, Sullivan J, Knupp K, Laux L, Polster T, Nikanorova M, Devinsky O, Cross JH, Guerrini R, Talwar D, Miller I, Farfel G, Galer BS, Gammaitoni A, Mistry A, Morrison G, Lock M, Agarwal A, Lai WW, Ceulemans B, FAiRE DS Study Group. Fenfluramine hydrochloride for the treatment of seizures in Dravet syndrome: a randomised, double-blind, placebo-controlled trial. Lancet. 2019;394:2243–54.
pubmed: 31862249 doi: 10.1016/S0140-6736(19)32500-0
Nabbout R, Mistry A, Zuberi S, Villeneuve N, Gil-Nagel A, Sanchez-Carpintero R, Stephani U, Laux L, Wirrell E, Knupp K, Chiron C, Farfel G, Galer BS, Morrison G, Lock M, Agarwal A, Auvin S, FAiRE, DS Study Group. Fenfluramine for treatment-resistant seizures in patients with Dravet syndrome receiving stiripentol-inclusive regimens: a randomized clinical trial. JAMA Neurol. 2020;77:300–8.
pubmed: 31790543 doi: 10.1001/jamaneurol.2019.4113
Knupp KG, Scheffer IE, Ceulemans B, Sullivan JE, Nickels KC, Lagae L, Guerrini R, Zuberi SM, Nabbout R, Riney K, Shore S, Agarwal A, Lock M, Farfel GM, Galer BS, Gammaitoni AR, Davis R, Gil-Nagel A. Efficacy and safety of fenfluramine for the treatment of seizures associated with Lennox–Gastaut syndrome: a randomized clinical trial. JAMA Neurol. 2022;79:554–64.
Martin P, de Witte PAM, Maurice T, Gammaitoni A, Farfel G, Galer B. Fenfluramine acts as a positive modulator of sigma-1 receptors. Epilepsy Behav. 2020;105: 106989.
pubmed: 32169824 doi: 10.1016/j.yebeh.2020.106989
Sourbron J, Smolders I, de Witte P, Lagae L. Pharmacological analysis of the anti-epileptic mechanisms of fenfluramine in scn1a mutant zebrafish. Front Pharmacol. 2017;8:191.
pubmed: 28428755 pmcid: 5382218 doi: 10.3389/fphar.2017.00191
Martin P, Reeder T, Sourbron J, de Witte PAM, Gammaitoni AR, Galer BS. An emerging role for sigma-1 receptors in the treatment of developmental and epileptic encephalopathies. Int J Mol Sci. 2021;22:8416.
pubmed: 34445144 pmcid: 8395113 doi: 10.3390/ijms22168416
Bishop KI, Isquith PK, Gioia GA, et al. Improved everyday executive functioning following profound reduction in seizure frequency with fenfluramine: analysis from a phase 3 long-term extension study in children/young adults with Dravet syndrome. Epilepsy Behav. 2021;121(pt A): 108024.
pubmed: 34023810 doi: 10.1016/j.yebeh.2021.108024
Bishop KI, Isquith PK, Gioia GA, et al. FINTEPLA (fenfluramine) treatment improves everyday executive functioning in patients with Lennox–Gastaut syndrome: analysis from a phase 3 clinical trial. Presented at American Academy of Neurology Annual Meeting; 2021 Apr 17–22; virtual meeting.
Bishop KI, Isquith PK, Gioia GA, Knupp KG, Scheffer IE, Nabbout R, Specchio N, Sullivan J, Auvin S, Helen Cross J, Guerrini R, Farfel G, Galer BS, Gammaitoni AR. Fenfluramine treatment is associated with improvement in everyday executive function in preschool-aged children (<5 years) with Dravet syndrome. Epilepsy Behav. 2022;1(138): 108994.
Ng YT, Conry JA, Drummond R, Stolle J, Weinberg MA, OV-1012 Study Investigators. Randomized, phase III study results of clobazam in Lennox-Gastaut syndrome. Neurology. 2011;77:1473–81.
pubmed: 21956725 doi: 10.1212/WNL.0b013e318232de76
Glauser T, Kluger G, Sachdeo R, Krauss G, Perdomo C, Arroyo S. Rufinamide for generalized seizures associated with Lennox-Gastaut syndrome. Neurology. 2008;70:1950–8.
pubmed: 18401024 doi: 10.1212/01.wnl.0000303813.95800.0d
Chiron C, Tonnelier S, Rey E, et al. Stiripentol in childhood partial epilepsy: randomized placebo-controlled trial with enrichment and withdrawal design. J Child Neurol. 2006;21:496–502.
pubmed: 16948934 doi: 10.1177/08830738060210062101
Lattanzi S, Brigo F, Trinka E, et al. Adjunctive cannabidiol in patients with Dravet syndrome: a systematic review and meta-analysis of efficacy and safety. CNS Drugs. 2020;34:229–41.
pubmed: 32040850 doi: 10.1007/s40263-020-00708-6
Lattanzi S, Brigo F, Cagnetti C, Trinka E, Silvestrini M. Efficacy and safety of adjunctive cannabidiol in patients with Lennox-Gastaut syndrome: a systematic review and meta-analysis. CNS Drugs. 2018;32:905–16.
pubmed: 30132269 doi: 10.1007/s40263-018-0558-9
Lattanzi S, Trinka E, Striano P, Zaccara G, Del Giovane C, Nardone R, Silvestrini M, Brigo F. Cannabidiol efficacy and clobazam status: A systematic review and meta-analysis. Epilepsia. 2020;61:1090–8.
pubmed: 32452532 doi: 10.1111/epi.16546
Gil-Nagel A, Sullivan J, Ceulemans B, et al. Treatment with fenfluramine in patients with Dravet syndrome has no long-term effects on weight and growth. Epilepsy Behav. 2021;122: 108212.
pubmed: 34352670 doi: 10.1016/j.yebeh.2021.108212
Sharawat IK, Panda PK, Kasinathan A, Panda P, Dawman L, Joshi K. Efficacy and tolerability of fenfluramine in patients with Dravet syndrome: a systematic review and meta-analysis. Seizure. 2021;85:119–26.
pubmed: 33461030 doi: 10.1016/j.seizure.2020.12.016
Zhang L, Li W, Wang C. Efficacy and safety of fenfluramine in patients with Dravet syndrome: a meta-analysis. Acta Neurol Scand. 2021;143:339–48.
pubmed: 33336426 doi: 10.1111/ane.13387
Sullivan J, Scheffer IE, Lagae L, et al. Fenfluramine HCl (Fintepla.) provides long-term clinically meaningful reduction in seizure frequency: analysis of an ongoing open-label extension study. Epilepsia. 2020;61:2396–404.
pubmed: 33078386 pmcid: 7756901 doi: 10.1111/epi.16722
Knupp KG, Scheffer IE, Ceulemans B, et al. Fenfluramine provides clinically meaningful reduction in frequency of drop seizures in patients with Lennox-Gastaut syndrome: interim analysis of an open-label extension study. Epilepsia. 2023;64:139–151.
Lai WW, Galer BS, Wong PC, et al. Cardiovascular safety of fenfluramine in the treatment of Dravet syndrome: analysis of an ongoing long-term open-label safety extension study. Epilepsia. 2020;61:2386–95.
pubmed: 32809271 pmcid: 7754414 doi: 10.1111/epi.16638
Agarwal A, Farfel GM, Gammaitoni AR, Wong PC, Pinto FJ, Galer BS. Long-term cardiovascular safety of fenfluramine in patients with Dravet syndrome treated for up to 3 years: findings from serial echocardiographic assessments. Eur J Paediatr Neurol. 2022;39:35–9.
Devinsky O, King L, Schwartz D, Conway E, Price D. Effect of fenfluramine on convulsive seizures in CDKL5 deficiency disorder. Epilepsia. 2021;7:e98–102.
Millett D, Pach S. Fenfluramine in the successful treatment of super-refractory status epilepticus in a patient with Dravet syndrome. Epilepsy Behav Rep. 2021;16: 100461.
pubmed: 34179745 pmcid: 8214086 doi: 10.1016/j.ebr.2021.100461
Aeby A, Sculier C, Bouza AA, Askar B, Lederer D, Schoonjans AS, Vander Ghinst M, Ceulemans B, Offord J, Lopez-Santiago LF, Isom LL. SCN1B-linked early infantile developmental and epileptic encephalopathy. Ann Clin Transl Neurol. 2019;6:2354–67.
pubmed: 31709768 pmcid: 6917350 doi: 10.1002/acn3.50921
Geenen KR, Doshi SP, Patel S, Sourbron J, Falk A, Morgan A, Vu U, Bruno PL, Thiele EA. Fenfluramine for seizures associated with Sunflower syndrome. Dev Med Child Neurol. 2021;63:1427–32.
pubmed: 34216017 doi: 10.1111/dmcn.14965
Tupal S, Faingold CL. Serotonin 5-HT4 receptors play a critical role in the action of fenfluramine to block seizure-induced sudden death in a mouse model of SUDEP. Epilepsy Res. 2021;177: 106777.
pubmed: 34601387 doi: 10.1016/j.eplepsyres.2021.106777
Cross JH, Galer BS, Gil-Nagel A, Devinsky O, Ceulemans B, Lagae L, Schoonjans AS, Donner E, Wirrell E, Kothare S, Agarwal A, Lock M, Gammaitoni AR. Impact of fenfluramine on the expected SUDEP mortality rates in patients with Dravet syndrome. Seizure. 2021;93:154–9.
pubmed: 34768178 doi: 10.1016/j.seizure.2021.10.024

Auteurs

Payam Tabaee Damavandi (P)

Department of Neurology, Fondazione IRCCS San Gerardo dei Tintori, School of Medicine and Surgery, Milan Center for Neuroscience, University of Milano, Bicocca, Monza, Italy.

Natalia Fabin (N)

Laboratory of Epidemiological and Clinical Cardiology, Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.

Riccardo Giossi (R)

Chemical-Clinical Analyses Unit, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy.

Sara Matricardi (S)

Department of Pediatrics, University of Chieti, Chieti, Italy.

Cinzia Del Giovane (C)

Department of Medical and Surgical Sciences for Children and Adults, University-Hospital of Modena and Reggio Emilia, Modena, Italy.
Institute of Primary Health Care (BIHAM), University of Bern, Bern, Switzerland.

Pasquale Striano (P)

Pediatric Neurology and Muscular Diseases Unit, Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, "G. Gaslini" Institute, University of Genoa, Genoa, Italy.

Stefano Meletti (S)

Neurology Unit, OCB Hospital, AOU Modena, Modena, Italy.
Department of Biomedical, Metabolic and Neural Science, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy.

Francesco Brigo (F)

Division of Neurology, "Franz Tappeiner" Hospital, Merano, BZ, Italy.

Eugen Trinka (E)

Department of Neurology, Christian Doppler Klinik, Paracelsus Medical University, Salzburg, Austria.
Center for Cognitive Neuroscience, Salzburg, Austria.
Public Health, Health Services Research and HTA, University for Health Sciences, Medical Informatics and Technology, Hall in Tirol, Austria.

Simona Lattanzi (S)

Department of Experimental and Clinical Medicine, Neurological Clinic, Marche Polytechnic University, Via Conca 71, 60020, Ancona, Italy. alfierelattanzisimona@gmail.com.

Classifications MeSH