An evaluation of onobotulinumtoxinA as a therapeutic option for pediatric neurogenic detrusor overactivity

References

• Guys JM, Hery G, Haddad M, et al. Neurogenic bladder in children: basic principles, new therapeutic trends. Scand J Surg. 2011;100(4):256–263. doi: 10.1177/145749691110000405
   PubMed Web of Science ®Google Scholar
• Bauer SB. Neurogenic bladder: etiology and assessment. Pediatr Nephrol. 2008 Apr;23(4):541–551. doi: 10.1007/s00467-008-0764-7
   PubMed Web of Science ®Google Scholar
• Copp AJ, Adzick NS, Chitty LS, et al. Spina bifida. Nat Rev Dis Primers. 2015 Apr 30;1(1):15007.
   PubMedGoogle Scholar
• Stein R, Bogaert G, Dogan HS, et al. EAU/ESPU guidelines on the management of neurogenic bladder in children and adolescent part I diagnostics and conservative treatment. Neurourol Urodyn. 2020 Jan;39(1):45–57. doi: 10.1002/nau.24211
   PubMed Web of Science ®Google Scholar
• Malakounides G, Lee F, Murphy F, et al. Single centre experience: long term outcomes in spina bifida patients. J Pediatr Urol. 2013 Oct;9(5):585–589. doi: 10.1016/j.jpurol.2013.02.015
   PubMed Web of Science ®Google Scholar
• Lapides J, Diokno AC, Silber SJ, et al. Clean, intermittent self-catheterization in the treatment of urinary tract disease. J Urol. 1972 Mar;107(3):458–461. doi: 10.1016/S0022-5347(17)61055-3
   PubMed Web of Science ®Google Scholar
• Le HK, Cardona-Grau D, Chiang G. Evaluation and long-term management of neurogenic bladder in spinal dysraphism. NeoReviews. 2019 Dec;20(12):e711–e724. doi: 10.1542/neo.20-12-e711
   PubMedGoogle Scholar
• Joseph DB, Baum MA, Tanaka ST, et al. Urologic guidelines for the care and management of people with spina bifida. J Pediatr Rehabil Med. 2020;13(4):479–489. doi: 10.3233/PRM-200712
   PubMed Web of Science ®Google Scholar
• Routh JC, Cheng EY, Austin JC, et al. Design and methodological considerations of the centers for disease control and prevention urologic and renal protocol for the newborn and young child with spina bifida. J Urol. 2016 Dec;196(6):1728–1734. doi: 10.1016/j.juro.2016.07.081
   PubMed Web of Science ®Google Scholar
• Kilic N, Balkan E, Akgoz S, et al. Comparison of the effectiveness and side-effects of tolterodine and oxybutynin in children with detrusor instability. Int J Urol. 2006 Feb;13(2):105–108. doi: 10.1111/j.1442-2042.2006.01240.x
   PubMed Web of Science ®Google Scholar
• FDA approves New indication for drug to treat neurogenic detrusor overactivity in pediatric patients: Food and drug administration; 2021 [cited 2023 May 17]. Available from: https://www.fda.gov/news-events/press-announcements/fda-approves-new-indication-drug-treat-neurogenic-detrusor-overactivity-pediatric-patients
   Google Scholar
• Sager C, Sanmartino M, Burek C, et al. Efficacy and safety of Mirabegron as adjuvant treatment in children with refractory neurogenic bladder dysfunction. J Pediatr Urol. 2020 Oct;16(5):e655 1–e655 6. doi: 10.1016/j.jpurol.2020.07.020
   Web of Science ®Google Scholar
• Biers SM, Venn SN, Greenwell TJ. The past, present and future of augmentation cystoplasty. BJU Int. 2012 May;109(9):1280–1293. doi: 10.1111/j.1464-410X.2011.10650.x
   PubMed Web of Science ®Google Scholar
• Stein R, Bogaert G, Dogan HS, et al. EAU/ESPU guidelines on the management of neurogenic bladder in children and adolescent part II operative management. Neurourol Urodyn. 2020 Feb;39(2):498–506. doi: 10.1002/nau.24248
   PubMed Web of Science ®Google Scholar
• Schulte-Baukloh H, Michael T, Schobert J, et al. Efficacy of botulinum-a toxin in children with detrusor hyperreflexia due to myelomeningocele: preliminary results. Urology. 2002 Mar;59(3):325–327. discussion 327-8. doi: 10.1016/S0090-4295(01)01641-7
   PubMed Web of Science ®Google Scholar
• Billante CR, Zealear DL, Billante M, et al. Comparison of neuromuscular blockade and recovery with botulinum toxins a and F. Muscle Nerve. 2002 Sep;26(3):395–403. doi: 10.1002/mus.10213
   PubMed Web of Science ®Google Scholar
• Scott AB. Botulinum toxin injection of eye muscles to correct strabismus. Trans Am Ophthalmol Soc. 1981;79:734–770.
   PubMedGoogle Scholar
• Dykstra DD, Sidi AA, Scott AB, et al. Effects of botulinum a toxin on detrusor-sphincter dyssynergia in spinal cord injury patients. J Urol. 1988 May;139(5):919–922. doi: 10.1016/S0022-5347(17)42717-0
   PubMed Web of Science ®Google Scholar
• Neel KF, Soliman S, Salem M, et al. Botulinum-A toxin: solo treatment for neuropathic noncompliant bladder. J Urol. 2007 Dec;178(6):2593–2597. discussion 2597-8. doi: 10.1016/j.juro.2007.08.032
   PubMed Web of Science ®Google Scholar
• Linsenmeyer TA. Use of botulinum toxin in individuals with neurogenic detrusor overactivity: state of the art review. J Spinal Cord Med. 2013 Sep;36(5):402–419. doi: 10.1179/2045772313Y.0000000116
   PubMed Web of Science ®Google Scholar
• Ginsberg DA, Boone TB, Cameron AP, et al. The AUA/SUFU Guideline on adult neurogenic lower urinary tract dysfunction: treatment and follow-up. J Urol. 2021 Nov;206(5):1106–1113. doi: 10.1097/JU.0000000000002239
   PubMed Web of Science ®Google Scholar
• Austin PF, Franco I, Dobremez E, et al. OnabotulinumtoxinA for the treatment of neurogenic detrusor overactivity in children. Neurourol Urodyn. 2021 Jan;40(1):493–501. doi: 10.1002/nau.24588
   PubMed Web of Science ®Google Scholar
• Bowen DK, Meyer T, Rosoklija I, et al. Botulinum toxin in patients at-risk for bladder augmentation: Durable impact or kicking the can? Neurourol Urodyn. 2022 Aug;41(6):1406–1413. doi: 10.1002/nau.24962
   PubMed Web of Science ®Google Scholar
• Chancellor MB, Fowler CJ, Apostolidis A, et al. Drug Insight: biological effects of botulinum toxin a in the lower urinary tract. Nat Clin Pract Urol. 2008 Jun;5(6):319–328. doi: 10.1038/ncpuro1124
   PubMedGoogle Scholar
• Hirst GR, Watkins AJ, Guerrero K, et al. Botulinum toxin B is not an effective treatment of refractory overactive bladder. Urology. 2007 Jan;69(1):69–73. doi: 10.1016/j.urology.2006.09.005
   PubMed Web of Science ®Google Scholar
• Frevert J. Pharmaceutical, biological, and clinical properties of botulinum neurotoxin type a products. Drugs R D. 2015 Mar;15(1):1–9. doi: 10.1007/s40268-014-0077-1
   PubMed Web of Science ®Google Scholar
• Field M, Splevins A, Picaut P, et al. AbobotulinumtoxinA (Dysport®), OnabotulinumtoxinA (botox®), and IncobotulinumtoxinA (Xeomin®) neurotoxin content and potential Implications for Duration of response in patients. Toxins (Basel). 2018 Dec 13;10(12):535.
   PubMed Web of Science ®Google Scholar
• Highlights of prescribing information, BOTOX (onabotulinumtoxinA for injection, for intramuscular, intradetrusor, or intradermal use. 2021 https://www.accessdata.fda.gov/drugsatfda_docs/label/2021/103000s5320lbl.pdf
   Google Scholar
• Safari S, Jamali S, Habibollahi P, et al. Intravesical injections of botulinum toxin type a for management of neuropathic bladder: a comparison of two methods. Urology. 2010 Jul;76(1):225–230. doi: 10.1016/j.urology.2009.09.087
   PubMed Web of Science ®Google Scholar
• Naqvi S, Clothier J, Wright A, et al. Urodynamic outcomes in children after single and multiple injections for overactive and low Compliance neurogenic bladder treated with Abobotulinum toxin a. J Urol. 2020 Feb;203(2):413–419. doi: 10.1097/JU.0000000000000540
   PubMed Web of Science ®Google Scholar
• Franco I, Hoebeke PB, Dobremez E, et al. Long-term safety and tolerability of repeated Treatments with OnabotulinumtoxinA in children with neurogenic detrusor overactivity. J Urol. 2023 April 209;(4): 774–784.
   PubMed Web of Science ®Google Scholar
• Rovner E, Chai TC, Jacobs S, et al. Evaluating the safety and potential activity of URO-902 (hMaxi-K) gene transfer by intravesical instillation or direct injection into the bladder wall in female participants with idiopathic (non-neurogenic) overactive bladder syndrome and detrusor overactivity from two double-blind, imbalanced, placebo-controlled randomized phase 1 trials. Neurourol Urodyn. 2020 Feb;39(2):744–753. doi: 10.1002/nau.24272
   PubMed Web of Science ®Google Scholar
• Kajbafzadeh AM, Ahmadi H, Montaser-Kouhsari L, et al. Intravesical electromotive botulinum toxin type a administration–part II: clinical application. Urology. 2011 Feb;77(2):439–445. doi: 10.1016/j.urology.2010.06.003
   PubMed Web of Science ®Google Scholar
• Eisele KH, Fink K, Vey M, et al. Studies on the dissociation of botulinum neurotoxin type a complexes. Toxicon. 2011 Mar 15;57(4):555–565. doi: 10.1016/j.toxicon.2010.12.019
   PubMed Web of Science ®Google Scholar
• Lin YH, Chiang BJ, Liao CH. Mechanism of action of botulinum toxin a in treatment of functional urological disorders. Toxins (Basel). 2020 Feb 18;12(2):129.
   PubMed Web of Science ®Google Scholar
• Coelho A, Dinis P, Pinto R, et al. Distribution of the high-affinity binding site and intracellular target of botulinum toxin type a in the human bladder. Eur Urol. 2010 May;57(5):884–890. doi: 10.1016/j.eururo.2009.12.022
   PubMed Web of Science ®Google Scholar
• Byun J, Kwak S, Kwon JH, et al. Comparative Pharmacodynamics of three different botulinum toxin type a preparations following repeated Intramuscular administration in Mice. Toxins (Basel). 2022 May 25;14(6):365.
   PubMed Web of Science ®Google Scholar
• Jiang YH, Liao CH, Kuo HC. Current and potential urological applications of botulinum toxin a. Nat Rev Urol. 2015 Sep;12(9):519–533. doi: 10.1038/nrurol.2015.193
   PubMed Web of Science ®Google Scholar
• Jiang YH, Jhang JF, Kuo HC. The clinical application of intravesical botulinum toxin a injection in patients with overactive bladder and interstitial cystitis. Tzu Chi Med J. 2023 Jan;35(1):31–37. doi: 10.4103/tcmj.tcmj_313_21
   PubMed Web of Science ®Google Scholar
• Schulte-Baukloh H, Priefert J, Knispel HH, et al. Botulinum toxin a detrusor injections reduce postsynaptic muscular M2, M3, P2X2, and P2X3 receptors in children and adolescents who have neurogenic detrusor overactivity: a single-blind study. Urology. 2013 May;81(5):1052–1057. doi: 10.1016/j.urology.2012.12.021
   PubMed Web of Science ®Google Scholar
• Apostolidis A, Rahnama’i MS, Fry C, et al. Do we understand how botulinum toxin works and have we optimized the way it is administered to the bladder? ICI-RS 2014. Neurourol Urodyn. 2016 Feb;35(2):293–298. doi: 10.1002/nau.22797
   PubMed Web of Science ®Google Scholar
• Papagiannopoulou D, Vardouli L, Dimitriadis F, et al. Retrograde transport of radiolabelled botulinum neurotoxin type a to the CNS after intradetrusor injection in rats. BJU Int. 2016 Apr;117(4):697–704. doi: 10.1111/bju.13163
   PubMed Web of Science ®Google Scholar
• Conte A, Giannantoni A, Proietti S, et al. Botulinum toxin a modulates afferent fibers in neurogenic detrusor overactivity. Eur J Neurol. 2012 May;19(5):725–732. doi: 10.1111/j.1468-1331.2011.03618.x
   PubMed Web of Science ®Google Scholar
• Coelho A, Cruz F, Cruz CD, et al. Spread of onabotulinumtoxinA after bladder injection. Experimental study using the distribution of cleaved SNAP-25 as the marker of the toxin action. Eur Urol. 2012 Jun;61(6):1178–1184. doi: 10.1016/j.eururo.2012.01.046
   PubMed Web of Science ®Google Scholar
• Schulte-Baukloh H, Weiss C, Weinberger S, et al. Real-time documentation of the effect of Onabotulinumtoxin a detrusor injection in OAB patients—preliminary results. Toxins (Basel). 2022 Dec 30;15(1):30.
   PubMed Web of Science ®Google Scholar
• Rogozhin AA, Pang KK, Bukharaeva E, et al. Recovery of mouse neuromuscular junctions from single and repeated injections of botulinum neurotoxin a. J Physiol. 2008 Jul 1;586(13):3163–3182.
   PubMed Web of Science ®Google Scholar
• Greer T, Abbott J, Breytenbach W, et al. Ten Years of experience with intravesical and intrasphincteric onabotulinumtoxinA in children. J Pediatr Urol. 2016 Apr;12(2):94 e1–6. doi: 10.1016/j.jpurol.2015.06.019
   PubMed Web of Science ®Google Scholar
• Kroll P, Jankowski A, Soltysiak J, et al. Botulinum toxin-A injections in children with neurogenic bladder. Nephro-Urol Mon. 2011;3(2):125–128.
   Google Scholar
• Ringoir A, Dhondt B, De Bleser E, et al. Intradetrusor onabotulinum-a toxin injections in children with therapy-resistant idiopathic detrusor overactivity. A retrospective study. J Pediatr Urol. 2020 Apr;16(2):e181 1–e181 8. doi: 10.1016/j.jpurol.2019.12.013
   Web of Science ®Google Scholar
• Overland MR, Leva NV, DiSandro M, et al. Feasibility of awake intravesical botulinum toxin injection in pediatric neurogenic bladder. J Urol. 2022 Sep;208(3):702–710. doi: 10.1097/JU.0000000000002709
   PubMed Web of Science ®Google Scholar
• Mensah EE, Toia B, Nguyen L, et al. Intravesical onabotulinumtoxinA injections in patients on antiplatelet and anticoagulation therapy. Neurourol Urodyn. 2021 Sep;40(7):1829–1833. doi: 10.1002/nau.24758
   PubMed Web of Science ®Google Scholar
• Rajaganapathy BR, Chancellor MB, Nirmal J, et al. Bladder uptake of liposomes after intravesical administration occurs by endocytosis. Plos One. 2015;10(3):e0122766. doi: 10.1371/journal.pone.0122766
   PubMed Web of Science ®Google Scholar
• Chuang YC, Kaufmann JH, Chancellor DD, et al. Bladder instillation of liposome encapsulated onabotulinumtoxina improves overactive bladder symptoms: a prospective, multicenter, double-blind, randomized trial. J Urol. 2014 Dec;192(6):1743–1749. doi: 10.1016/j.juro.2014.07.008
   PubMed Web of Science ®Google Scholar
• Wu SY, Chang SJ, Yang SS, et al. Botulinum toxin injection for medically refractory neurogenic bladder in children: a systematic review. Toxins (Basel). 2021 Jun 28;13(7):447.
   PubMed Web of Science ®Google Scholar
• Hascoet J, Manunta A, Brochard C, et al. Outcomes of intra-detrusor injections of botulinum toxin in patients with spina bifida: a systematic review. Neurourol Urodyn. 2017 Mar;36(3):557–564. doi: 10.1002/nau.23025
   PubMed Web of Science ®Google Scholar
• Marte A. Onabotulinumtoxin a for treating overactive/poor compliant bladders in children and adolescents with neurogenic bladder secondary to myelomeningocele. Toxins (Basel). 2012 Dec 28;5(1):16–24.
   PubMed Web of Science ®Google Scholar
• Softness KA, Thaker H, Theva D, et al. Onabotulinumtoxin a (botox): a reasonable alternative for refractory neurogenic bladder dysfunction in children and young adults. Neurourol Urodyn. 2021 Nov;40(8):1981–1988. doi: 10.1002/nau.24778
   PubMed Web of Science ®Google Scholar
• Tiryaki S, Yagmur I, Parlar Y, et al. Botulinum injection is useless on fibrotic neuropathic bladders. J Pediatr Urol. 2015 Feb;11(1):27 e1–4. doi: 10.1016/j.jpurol.2014.08.009
   PubMed Web of Science ®Google Scholar
• Kim SW, Choi JH, Lee YS, et al. Preoperative urodynamic factors predicting outcome of botulinum toxin-A intradetrusor injection in children with neurogenic detrusor overactivity. Urology. 2014 Dec;84(6):1480–1484. doi: 10.1016/j.urology.2014.09.001
   PubMed Web of Science ®Google Scholar
• Danacioglu YO, Keser F, Ersoz C, et al. Factors predicting the success of intradetrusor onabotulinum toxin-A treatment in children with neurogenic bladders due to myelomeningocele: the outcomes of a large cohort. J Pediatr Urol. 2021 Aug;17(4):e520 1–e520 7. doi: 10.1016/j.jpurol.2021.02.020
   Web of Science ®Google Scholar
• Khan MK, VanderBrink BA, DeFoor WR, et al. Botulinum toxin injection in the pediatric population with medically refractory neuropathic bladder. J Pediatr Urol. 2016 Apr;12(2):104 e1–6. doi: 10.1016/j.jpurol.2015.08.018
   PubMed Web of Science ®Google Scholar
• Sekerci CA, Tanidir Y, Garayev A, et al. Clinical and urodynamic results of repeated intradetrusor onabotulinum toxin a injections in refractory neurogenic detrusor overactivity: up to 5 injections in a cohort of children with myelodysplasia. Urology. 2018 Jan;111:168–175.
   PubMed Web of Science ®Google Scholar
• Hascoet J, Peyronnet B, Forin V, et al. Intradetrusor injections of botulinum toxin type a in children with spina bifida: a multicenter study. Urology. 2018 Jun;116:161–167.
   PubMed Web of Science ®Google Scholar
• Riccabona M, Koen M, Schindler M, et al. Botulinum-A toxin injection into the detrusor: a safe alternative in the treatment of children with myelomeningocele with detrusor hyperreflexia. J Urol. 2004 Feb;171(2 Pt 1):845–848. discussion 848. doi: 10.1097/01.ju.0000108892.35041.2d
   PubMed Web of Science ®Google Scholar
• Altaweel W, Jednack R, Bilodeau C, et al. Repeated intradetrusor botulinum toxin type a in children with neurogenic bladder due to myelomeningocele. J Urol. 2006 Mar;175(3 Pt 1):1102–1105. doi: 10.1016/S0022-5347(05)00400-3
   PubMed Web of Science ®Google Scholar
• Kajbafzadeh AM, Moosavi S, Tajik P, et al. Intravesical injection of botulinum toxin type A: management of neuropathic bladder and bowel dysfunction in children with myelomeningocele. Urology. 2006 Nov;68(5):1091–1096. discussion 1096-7. doi: 10.1016/j.urology.2006.05.056
   PubMed Web of Science ®Google Scholar
• Neel KF, Salem M, Soliman S. Total endoscopic management (TEM approach) of children with non-compliant neuropathic bladder: a preliminary report. J Pediatr Urol. 2008 Apr;4(2):124–126. doi: 10.1016/j.jpurol.2007.10.008
   PubMedGoogle Scholar
• Deshpande AV, Sampang R, Smith GH. Study of botulinum toxin a in neurogenic bladder due to spina bifida in children. ANZ J Surg. 2010 Apr;80(4):250–253. doi: 10.1111/j.1445-2197.2009.05129.x
   PubMed Web of Science ®Google Scholar
• Figueroa V, Romao R, Pippi Salle JL, et al. Single-center experience with botulinum toxin endoscopic detrusor injection for the treatment of congenital neuropathic bladder in children: effect of dose adjustment, multiple injections, and avoidance of reconstructive procedures. J Pediatr Urol. 2014 Apr;10(2):368–373. doi: 10.1016/j.jpurol.2013.10.011
   PubMed Web of Science ®Google Scholar
• Mohajerzadeh L, Tabari AK, Atqiaee K, et al. The effects of botulinum toxin injection on urodynamic changes in pediatric population with neurospastic bladder: first trial in Iran. J Pediatr Surg. 2020 Nov;55(11):2517–2520. doi: 10.1016/j.jpedsurg.2019.12.013
   PubMed Web of Science ®Google Scholar
• Dudley AG, Adams MC, Brock JW 3rd, et al. Interrater reliability in interpretation of neuropathic pediatric urodynamic tracings: an expanded multicenter study. J Urol. 2018 May;199(5):1337–1343. doi: 10.1016/j.juro.2017.12.051
   PubMed Web of Science ®Google Scholar
• Kennelly M, Cruz F, Herschorn S, et al. Efficacy and safety of AbobotulinumtoxinA in patients with neurogenic detrusor overactivity incontinence performing regular clean intermittent catheterization: pooled results from two phase 3 randomized studies (CONTENT1 and CONTENT2). Eur Urol. 2022 Aug;82(2):223–232. doi: 10.1016/j.eururo.2022.03.010
   PubMed Web of Science ®Google Scholar
• Ginsberg D, Gousse A, Keppenne V, et al. Phase 3 efficacy and tolerability study of onabotulinumtoxinA for urinary incontinence from neurogenic detrusor overactivity. J Urol. 2012 Jun;187(6):2131–2139. doi: 10.1016/j.juro.2012.01.125
   PubMed Web of Science ®Google Scholar
• Cruz F, Herschorn S, Aliotta P, et al. Efficacy and safety of onabotulinumtoxinA in patients with urinary incontinence due to neurogenic detrusor overactivity: a randomised, double-blind, placebo-controlled trial. Eur Urol. 2011 Oct;60(4):742–750. doi: 10.1016/j.eururo.2011.07.002
   PubMed Web of Science ®Google Scholar
• Herschorn S, Gajewski J, Ethans K, et al. Efficacy of botulinum toxin a injection for neurogenic detrusor overactivity and urinary incontinence: a randomized, double-blind trial. J Urol. 2011 Jun;185(6):2229–2235. doi: 10.1016/j.juro.2011.02.004
   PubMed Web of Science ®Google Scholar
• Lambregts AP, Nieuwhof-Leppink AJ, Klijn AJ, et al. Intravesical botulinum-A toxin in children with refractory non-neurogenic overactive bladder. J Pediatr Urol. 2022 Jun;18(3):e351 1–e351 8. doi: 10.1016/j.jpurol.2022.02.007
   Web of Science ®Google Scholar
• Rahman E, Banerjee PS, Asghar A, et al. Botulinum toxin type a immunogenicity across multiple indications: an overview systematic review. Plast Reconstr Surg. 2022 Apr 1;149(4):837–848.
   PubMed Web of Science ®Google Scholar
• Committee for proprietary medicinal products (CPMP) summary information on referral opinion following arbitration pursuant to article 29 of council directive 2001/83/EC for: the European agency for the evaluation of medicinal products; 2003. https://www.ema.europa.eu/en/documents/referral/summary-information-referral-opinion-following-arbitration-pursuant-article-29-council-directive/83/ec-botox-active-substance-clostridium-botulinum-type-neurotoxin-complex-background-information_en.pdf
   Google Scholar
• Goessaert AS, Everaert KC. Onabotulinum toxin a for the treatment of neurogenic detrusor overactivity due to spinal cord injury or multiple sclerosis. Expert Rev Neurother. 2012 Jul;12(7):763–775. doi: 10.1586/ern.12.61
   PubMed Web of Science ®Google Scholar