BOTULINUM TOXIN: RESEARCH ISSUES ARISING FROM PRACTICE

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1 % of baseline CMAP Botulinum toxin: mechanism of action BOTULINUM TOXIN: RESEARCH ISSUES ARISING FROM PRACTICE Clinical benefits of botulinum toxin (BT) injections depend primarily on the toxin's peripheral action General assumption is that effects of BT remain localized to the injection site Degree of muscle paralysis depends on BT dosage Maja Kojović The time course of the effects of intramuscular BT-serial EMG CMAP amplitude The amplitude CMAP in the injected EDB starts to decline 48 hours after the injection This decline peaks between days 7 and 21. Recovery in 90 or more days Greater the dosage of BT greater the paralysis of the muscle However observations from clinical practice BT peripheral action depends also on the state of the injected muscle-bt is preferentially uptaken by the most active muscle fibers( autofocusing ) Remote effects in the non-injected muscles Clinical benefit may be out of proportion of BT induced weakness No or loss of clinical benefit despite Long-term effect of BT CENTRAL ACTION OF BT? Hamjian and Walker, 1994 Possible mechanisms for central action of BT 1. Reduction of Ia afferent input Changes in reciprocal inhibition Changes in excitability and sensorimotor integration at cortical level 2. Retrograde transport to the spinal cord and transcytosis to other neurons 3.Changes in gene expression in α motoneuron 4. Hematogeneous spread (unlikely) From Caleo M. et al state of the injected muscle Animal experiments suggest that the toxin is preferentially taken up by the most active muscle fibers- autofocusing (Hughes and Whaler, 1962) In hemifacial spasm, injections of BT to OO muscle: moderate muscle paralysis, but complete loss of ephatic response ( Glocker, 1995 ) preferential uptake of BT by hyperactive synapses involved in ephaptic transmission Injection of BT in both EDB : the effect of the induced neuromuscular blockade was greater on the side that received peripheral nerve stimulation (Eleopra, 1997) 1

2 active inactive state of the injected muscle-dystonia state of the injected muscle-spasticity Nerve stimulation improve BT effect in spastic paraparesis ( Frasson, 2005) However Electrical activation of OO does not improve effectiveness of BT in blepharospasm ( Conte, 2010)- celling effect? Increased efficacy of BT after active and passive muscle activity in animal experiments (Minamoto, 2007) Remote effects in the non-injected muscles When BT was injected to one side in patients with blepharospasm ( Girlada, 1996) Clinical benefit was bilateral CMAP and SFEMG changes were present on both sides Clinical benefit out of proportion of weakness- central effect of BT Tonic vibration reflex All patients Patients with prolonged clinical benefit In adductor spasmodic dysphonia with unilateral thyroarytenoid muscle injections of BT-A ( Bielamowicz and Ludlow,2000) EMG bursts were reduced bilaterally (thus also in the non-injected muscles) Improvement in speech symptoms as a result of changes in a central pathophysiological mechanism? Trompetto,2006 Central effect of BT- effect on inhibition Loss of inhibition at different CNS levels: SPINAL CORD: Loss of Reciprocal inhibition (Nakashima, 1989) BRAINSTEM: Enhanced blink reflex recovery cycle (Berardelli, 1985) MOTOR CORTEX: Reduced intracortical inhibition (Ridding, 1995) Loss of inhibition at different CNS levels: SPINAL CORD: Loss of Reciprocal inhibition (Nakashima, 1989)- reversed by s ( Priori, 1995) BRAINSTEM: Enhanced blink reflex recovery cycle (Berardelli, 1985)- not affected by BT inj MOTOR CORTEX: Reduced intracortical inhibition (Ridding, 1995)- reversed by ( Gilio, 2000) Possible clinical manifestation of deficient inhibition: Co-contraction of antagonist muscles Non-selective activation of muscles Overflow of dystonia Mirror dystonia 2

3 APB MEP amplitude (mv) Central effect of BT- effect on intracortical inhibition ABNORMAL ( ENHANCED) CORTICAL PLASTICITY Healthy controls Dystonia before BT Dystonia 1 month after BT Dystonia 3 months after BT Patients with primary dystonia have enhanced response to different experimental plasticity protocols (Quartarone, 2003; Quartarone, 2008). Focal limb dystonia is typically triggered by a period of intensive training of a particular movement- a clinical feature that may link the role of maladaptive plasticity to development of dystonic symptoms In monkey, overtraining in specific hand movements trigger the symptoms that resemble human dystonia (Byl, 1996). The idea is that overtraining itself triggers functional changes in sensory and motor cortices, leading to abnormal sensorimotor integration that somehow results in dystonic symptoms. Adapted from Gilio, 2000 Central effect of BT- effect on cortical plasticity as assesed by motor mapping studies with TMS The corticomotor representation of upper limb muscles in writer s cramp are distorted and displaced, but this can be temporarly reveresed following botulinum toxin injection (Byrnes, 1998) Reversible reorganisation of corticomotor representation of the hand in cervical dystonia (Thickbroom, 2003) Sensorimotor cortical plasticity as assesed by PAS protocol single pulse TMS Paired Associative Stimulation PAS TMS on the M1 APB ADM APB single pulse TMS ADM 1mV MEP sensory-nerve electrical stimulation on contralateral median nerve > 1mV MEP (Stefan, 2000) Sensorimotor cortical plasticity in dystonia, as assessed by PAS protocol Central effect of BT- effect on sensorimotor cortical plasticity in dystonia s reduce response to PAS in parallel with clinical improvementcontribution to clinical benefit? before 1 month after 3 months after In susceptible individuals an excessive tendency to form association between sensory input and motor output may lead to dystonia ( musician s dystonia, writer s cramp) before PAS 0 min 30 min 60 min before PAS 0 min 30 min 60 min before PAS 0 min 30 min 60 min ( Quartarone, 2003; Weise, 2006; Edwards 2006) Kojović,

4 weeks Central effect of BT- effect on sensorimotor cortical plasticity in dystonia Central effect of BT- effect on SSEPs in dystonia and spasticity The longer was the time elapsed since the last injections the more pronounced was the rpas response R 2 =0 p<0.01 Metodological implications when enrolling dystonia patients in future studies Cervical dystonia: reduction in the amplitude of P22/N30 precentral component after treatment with BT- in parallel with clinical improvement ( Kanowsky, 1998) changes in cortical excitability secondary to BT induced modulation of spindle afferent input But in writer s cramp : no changes in cortical SSEPs before and after BT treatment (Contarino, 2007) Spasticity: An improvement of cortical SEPs associated with reduction of spasticity in cerebral palsy (Park, 2002; Frascarelli, 2011) normalized rpas 200 response at 30 min 400 Kojović, 2011 Some patient with CD report return of symptoms at the time when injected muscles are still paralysed (Gelb, 1989) In some patients there is no clinical improvement despite EMG detected changes in muscle activity pattern after BT injections ( Gelb, 1991) Loss of clinical benefit in patients who were initially good responders Dystonia is an abnormality of central motor programs When the most active muscles are denervated by BT, mechanisms of abnormal central programming may engage previously inactive muscle into dystonic vicious cycle - motor (mal)adaptation This may explain the failure of surgery for torticollis ( rhizotomy, peripheral nerve section, muscle section) - abnormal head position eventually recurs ABNORMAL NECK POSTURE PRODUCED BY ACTIVITY OF DIFFERENT MUSCLES?? ADVANTAGE OF BT TREATMENT could be in preventing central motor adaptation due to its temporary paralysing effect Relevance of changing pattern of injection on repeated treatment sessions? Combination of s with repeated session of rtms? Long-term effect of BT in dystonia Long-term remission of idiopathic cervical dystonia after BT treatment in 6/30 patients (Giladi, 2000) The possibility that BT might have induced early remission in those patients who would otherwise develop spontaneous remission ( 10-20%). Gamma motor neuron paralysis induced by BT may change afferent input from injected muscles and act as continuous sensory trick reorganization in the BG and/ or sensorimotor cortex correction of the basic pathophysiological process which causes cervical dystonia The role of combining s with repeated session of rtms? 4

5 Long-term effect of BT in spasticity CONCLUSIONS Early treatment of spasticity may (theoretically) brake a cycle of spasticity muscle shortening fibrosis contractures Cosgrove et al. (1994) : s in gastrocnemius muscle of hereditary spastic infant rats before they developed spasticity prevented shortening of muscle in adult rats Window of opportunity in children, but studies are lacking Effect on BT on recurrent ( Renshaw) inhibition (Marchand-Pauvert, 2014) possibility of long term effect by modulating maladaptive spinal cord plasticity in stroke patients? Clinical benefits of s depend mainly on the toxin's peripheral action However, this seems not to be the whole story Central action of BT may account for remote effects of BT may contribute to clinical improvement after injections May underlie long-term effects of treatment Research issues arising from practice and possible clinical relevance of feedback information BT research issues: relevance for understanding the pathophysiology of dystonia How to improve the response to BT? How to obtain clinical effect with a lower BT dose? Insight into pathophysiology of disease Dystonia is an abnormality of sensory-motor network Change of afferent input caused by s result in upstream changes that may affect different nodes of network Abnormalities in inhibition and plasticity in dystonia are not predetermined fixed aberrations, but reflect dynamic functional reorganisation influenced by inputs from another nodes in the network THANK YOU FOR YOUR ATTENTION 5

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