Combining strength training and botulinum neurotoxin intervention in children with cerebral palsy: the impact on muscle morphology and strength

References

• Reid S, Hamer P, Alderson J, Lloyd D. Neuromuscular adaptations to eccentric strength training in children and adolescents with cerebral palsy. Dev Med Child Neurol 2010;52:358–363.
   PubMed Web of Science ®Google Scholar
• Wiley ME, Damiano DL. Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol 1998;40:100–107.
   PubMed Web of Science ®Google Scholar
• Ross SA, Engsberg JR. Relationships between spasticity, strength, gait, and the GMFM-66 in persons with spastic diplegia cerebral palsy. Arch Phys Med Rehabil 2007;88:1114–1120.
   PubMed Web of Science ®Google Scholar
• Mockford M, Caulton JM. Systematic review of progressive strength training in children and adolescents with cerebral palsy who are ambulatory. Pediatr Phys Ther 2008;20:318–333.
   PubMedGoogle Scholar
• Lieber RL, Fridén J. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 2000;23:1647–1666.
   PubMed Web of Science ®Google Scholar
• Barrett RS, Lichtwark GA. Gross muscle morphology and structure in spastic cerebral palsy: a systematic review. Dev Med Child Neurol 2010;52:794–804.
   PubMed Web of Science ®Google Scholar
• Elder GC, Kirk J, Stewart G, Cook K, Weir D, Marshall A, Leahey L. Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol 2003;45:542–550.
   PubMed Web of Science ®Google Scholar
• Stackhouse SK, Binder-Macleod SA, Lee SC. Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 2005;31:594–601.
   PubMed Web of Science ®Google Scholar
• Molenaers G, Van Campenhout A, Fagard K, De Cat J, Desloovere K. The use of botulinum toxin A in children with cerebral palsy, with a focus on the lower limb. J Child Orthop 2010;4:183–195.
   PubMedGoogle Scholar
• Flett PJ. Rehabilitation of spasticity and related problems in childhood cerebral palsy. J Paediatr Child Health 2003;39:6–14.
   PubMed Web of Science ®Google Scholar
• Dodd KJ, Taylor NF, Damiano DL. A systematic review of the effectiveness of strength-training programs for people with cerebral palsy. Arch Phys Med Rehabil 2002;83:1157–1164.
   PubMed Web of Science ®Google Scholar
• Damiano DL, Abel MF. Functional outcomes of strength training in spastic cerebral palsy. Arch Phys Med Rehabil 1998;79:119–125.
   PubMed Web of Science ®Google Scholar
• MacPhail HE, Kramer JF. Effect of isokinetic strength-training on functional ability and walking efficiency in adolescents with cerebral palsy. Dev Med Child Neurol 1995;37:763–775.
   PubMed Web of Science ®Google Scholar
• Taylor NF, Dodd KJ, Damiano DL. Progressive resistance exercise in physical therapy: a summary of systematic reviews. Phys Ther 2005;85:1208–1223.
   PubMed Web of Science ®Google Scholar
• Verschuren O, Ketelaar M, Takken T, Helders PJ, Gorter JW. Exercise programs for children with cerebral palsy: a systematic review of the literature. Am J Phys Med Rehabil 2008;87:404–417.
   PubMed Web of Science ®Google Scholar
• Anttila H, Autti-Rämö I, Suoranta J, Mäkelä M, Malmivaara A. Effectiveness of physical therapy interventions for children with cerebral palsy: a systematic review. BMC Pediatr 2008;8:14.
   PubMed Web of Science ®Google Scholar
• Scianni A, Butler JM, Ada L, Teixeira-Salmela LF. Muscle strengthening is not effective in children and adolescents with cerebral palsy: a systematic review. Aust J Physiother 2009;55:81–87.
   PubMed Web of Science ®Google Scholar
• Verschuren O, Ada L, Maltais DB, Gorter JW, Scianni A, Ketelaar M. Muscle strengthening in children and adolescents with spastic cerebral palsy: considerations for future resistance training protocols. Phys Ther 2011;91:1130–1139.
   PubMed Web of Science ®Google Scholar
• McBurney H, Taylor NF, Dodd KJ, Graham HK. A qualitative analysis of the benefits of strength training for young people with cerebral palsy. Dev Med Child Neurol 2003;45:658–663.
   PubMed Web of Science ®Google Scholar
• McNee AE, Gough M, Morrissey MC, Shortland AP. Increase in muscle volume after plantarflexor strength training in children with spastic cerebral palsy. Dev Med Child Neurol 2009;51:1–7.
   Web of Science ®Google Scholar
• Love SC, Novak I, Kentish M, Desloovere K, Heinen F, Molenaers G, O’Flaherty S, Graham HK; Cerebral Palsy Institute. Botulinum toxin assessment, intervention and after-care for lower limb spasticity in children with cerebral palsy: international consensus statement. Eur J Neurol 2010;17 Suppl 2:9–37.
   PubMed Web of Science ®Google Scholar
• Koman LA, Mooney JF 3rd, Smith BP, Walker F, Leon JM. Botulinum toxin type A neuromuscular blockade in the treatment of lower extremity spasticity in cerebral palsy: a randomized, double-blind, placebo-controlled trial. BOTOX Study Group. J Pediatr Orthop 2000;20:108–115.
   PubMed Web of Science ®Google Scholar
• Steenbeek D, Meester-Delver A, Becher JG, Lankhorst GJ. The effect of botulinum toxin type A treatment of the lower extremity on the level of functional abilities in children with cerebral palsy: evaluation with goal attainment scaling. Clin Rehabil 2005;19:274–282.
   PubMed Web of Science ®Google Scholar
• Fortuna R, Vaz MA, Youssef AR, Longino D, Herzog W. Changes in contractile properties of muscles receiving repeat injections of botulinum toxin (Botox). J Biomech 2011;44:39–44.
   PubMed Web of Science ®Google Scholar
• Yaraskavitch M, Leonard T, Herzog W. Botox produces functional weakness in non-injected muscles adjacent to the target muscle. J Biomech 2008;41:897–902.
   PubMed Web of Science ®Google Scholar
• Gough M, Fairhurst C, Shortland AP. Botulinum toxin and cerebral palsy: time for reflection? Dev Med Child Neurol 2005;47:709–712.
   PubMed Web of Science ®Google Scholar
• Schroeder AS, Ertl-Wagner B, Britsch S, Schröder JM, Nikolin S, Weis J, Müller-Felber W, et al. Muscle biopsy substantiates long-term MRI alterations one year after a single dose of botulinum toxin injected into the lateral gastrocnemius muscle of healthy volunteers. Mov Disord 2009;24:1494–1503.
   PubMed Web of Science ®Google Scholar
• Palisano RJ. Validity of goal attainment scaling in infants with motor delays. Phys Ther 1993;73:651–8; discussion 658.
   PubMed Web of Science ®Google Scholar
• Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987;67:206–207.
   PubMed Web of Science ®Google Scholar
• Fowler EG, Staudt LA, Greenberg MB, Oppenheim WL. Selective Control Assessment of the Lower Extremity (SCALE): development, validation, and interrater reliability of a clinical tool for patients with cerebral palsy. Dev Med Child Neurol 2009;51:607–614.
   PubMed Web of Science ®Google Scholar
• Pitcher C, Elliott C, Williams S, et al. Childhood muscle morphology and strength: alterations over six months of growth. Muscle Nerve 2012; In press.
   PubMed Web of Science ®Google Scholar
• ACSM. Guidelines for exercise testing and prescription. 7th Edition ed. Philadelphia: Lippincot, Williams & Wilkins; 2006.
   Google Scholar
• Dodd KJ, Taylor NF, Graham HK. A randomized clinical trial of strength training in young people with cerebral palsy. Dev Med Child Neurol 2003;45:652–657.
   PubMed Web of Science ®Google Scholar
• Williams SA, Reid SL, Elliott CM, Shipman P, Valentine J. Morphological alterations in spastic muscles immediately following Botulinum Toxin Type-A treatment in children with Cerebral Palsy. Unpublished observations 2012.
   Google Scholar
• Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G. Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy. Dev Med Child Neurol 2011;53:543–548.
   PubMed Web of Science ®Google Scholar
• Shepherd R. Cerebral palsy. In: Physiotherapy in paediatrics. Oxford: Butterworth-Heinemann; 1995.
   Google Scholar
• Lampe R, Grassl S, Mitternacht J, Gerdesmeyer L, Gradinger R. MRT-measurements of muscle volumes of the lower extremities of youths with spastic hemiplegia caused by cerebral palsy. Brain Dev 2006;28:500–506.
   PubMed Web of Science ®Google Scholar