10.1055@s 0039 3400987

Review Article
Tone Reduction and Physical Therapy: Strengthening

Partners in Treatment of Children with Spastic
Cerebral Palsy
Inge Franki1,2 Lynn Bar-On3 Guy Molenaers1,4,5 Anja Van Campenhout1,4,5 Karen Craenen2
Kaat Desloovere3,4 Hilde Feys3 Petra Pauwels2 Jos De Cat2 Els Ortibus1,2,6
1 Department of Development and Regeneration, Katholieke Address for correspondence Inge Franki, PT, PhD, Department of
Universiteit Leuven, Leuven, Belgium Development and Regeneration, Centre for Developmental
2 Cerebral Palsy Clinic, University Hospitals Leuven—Campus Disabilities, Katholieke Universiteit Leuven, Kapucijnenvoer 33,
Pellenberg, Leuven, Belgium 3000 Leuven, Belgium (e-mail: [email protected]).
3 Department of Rehabilitation Sciences, Katholieke Universiteit
Leuven, Leuven, Belgium
4 Clinical Motion Analysis Laboratory, University Hospitals Leuven—
Campus Pellenberg, Leuven, Belgium
5 Department of Orthopedics, University Hospital Leuven, Leuven,
Belgium
Downloaded by: Universiteit Leiden / LUMC. Copyrighted material.

6 Centre for Developmental Disabilities, Leuven, Belgium
Neuropediatrics
Abstract The aim of this paper is to provide a clinically applicable overview of different tone
reducing modalities and how these can interact with or augment concurrent physical
therapy (PT). Botulinum toxin (BoNT), oral tone-regulating medication, intrathecal
baclofen (ITB), and selective dorsal rhizotomy are discussed within a physiotherapeutic
context and in view of current scientific evidence. We propose clinical reasoning
strategies to identify treatment goals as well as the appropriate and corresponding
treatment interventions. Instrumented measurement of spasticity, standardized clini-
cal assessment, and 3D clinical motion analysis are scientifically sound tools to help
select the appropriate treatment and, when needed, to selectively target or spare
individual muscles. In addition, particular attention is given to strength training as a
Keywords necessary tool to tackle muscle weakness associated with specific modalities of tone
► cerebral palsy reduction. More research is needed to methodologically assess the long-term effec-
► tone reduction tiveness of such individualized tone treatment, optimize parameters such as medica-
► spasticity tion dosage, and gain more insight into the kind of PT techniques that are essential in
► physical therapy conjunction with tone reduction.
Introduction to 4 per 1,000 newborn children, it is the most common cause

of physical disability in childhood.2,3 Data published by the
Cerebral palsy (CP) describes “a group of permanent disorders of network for Surveillance of Cerebral Palsy in Europe illustrated
the development of movement and posture causing activity that 85% of the children with CP are classified as spastic and
limitations, which are attributed to nonprogressive disturbances thereby, spasticity is considered as the most frequently
in the developing fetal or infant brain.”1 With an incidence of 2 observed symptom in CP.2 Spasticity is defined by Lance as
received © Georg Thieme Verlag KG DOI https://doi.org/

April 30, 2019 Stuttgart · New York 10.1055/s-0039-3400987.
accepted after revision ISSN 0174-304X.
October 16, 2019
Tone Reduction and Physical Therapy Franki et al..
“a velocity-dependent increase in muscle tone.”4 It is, however,

only one contributor to joint hyper-resistance, as structural
muscle and tendon alterations (e.g., muscle contractures) may
also contribute to increased resistance to passive joint move-
ment.5 Combined with decreased muscle strength, spasticity
may be a major cause of muscle contractures and/or bone
deformities and may also be painful.6 A recent large systematic
review including 57 studies, showed that pain prevalence
varied widely from 14 to 76% and was higher in females, older
age groups, and those classified within Gross Motor Function
Classification System (GMFCS) level V.7 Chalkiadis et al
described children with spasticity as the largest group of
patients referred to a pediatric multidisciplinary pain clinic
in Australia.8 Several authors have also investigated the rela-
tionship between spasticity, muscle strength, muscle length,
and functional limitations and concluded a complex entity of
direct and indirect interactions that has not yet been Fig. 1 Management of spasticity. (Adapted and updated from Gra-
unraveled.9–12 ham et al, 2000 28.) BoNT, botulinum toxin; ITB, intrathecal baclofen;
Oral Med, oral medication; SDR, selective dorsal rhizotomy.
Wright et al found poor relationships (r < 0.40) between

the change scores of spasticity and changes of gross motor
abilities after injections with BoNT type A, which may imply Modalities of Tone Reduction
that tone reduction as a standalone treatment might not be
sufficient to reduce functional limitations.13 Recent research Several treatment modalities are available for tone reduction
by Geertsen et al showed that adults with CP were not able to in CP. Graham et al classifies tone reducing modalities accord-
suppress the soleus H reflex during active dorsiflexion, ing to specificity and reversibility (►Fig. 1).28 Whereas oral
indicating impaired regulation of spinal interneurons, medications and ITB are reversible, SDR is not. However, in
responsible for Ia inhibition and/or presynaptic inhibition contrast to drugs and ITB, SDR is supposed to be selective. As
of Ia afferents. Geertsen et al therefore state that the evident from ►Fig. 1, BoNT type A is both selective and
impaired reciprocal inhibition together with impaired trans- reversible. Depending on their pathophysiological mechanism
mission of the corticospinal pathway might explain why and the clinical situation, any of these approaches may be
children and adults with CP are not able to generate force considered as modalities of tone reduction.
quickly and efficiently.14 Motor learning in this group will
have to involve de-learning of the unwanted patterns of
Botulinum Toxin
co-contractions, preferably at a young age.14–18 Inhibition
is of course only one part of the process, as it will have to be Effectiveness
followed by learning a more efficient pattern of movement, When injected intramuscularly, the neurotoxin BoNT is taken
which is only possible with the appropriate muscle strength up at the cholinergic nerve terminal, where it blocks the
and predictive coding of the sensory consequences of move- release of acetylcholine, causing selective, temporary muscle
ment.14–18 This underlying mechanism illustrates the needs denervation. This treatment is most effective when the motor
for a multimodal, combined treatment approach, combining end plate zones of the selected muscles are targeted.29 The
appropriate tone reduction with different physical therapy injections can be performed under ultrasound guidance.28–30
(PT) approaches and techniques.16–27 Although tone reduc- Besides its effective tone reducing mechanism, BoNT is also
tion and PT are generally considered as strengthening part- known for its direct and indirect pain reducing effects.31
ners, to the best of our knowledge, there are no specific The optimal timing for BoNT treatment is between 2 and
international guidelines to support this combined approach 5 years of age, during the period of dynamic neuromotor
in clinical practice. development, offering the greatest chance to modify its
Therefore, the aim of this paper is to provide a clinical and course.32,33 This will lead to a maximum response and pro-
evidence-based overview of different tone reducing modalities longed effect, reduced contractures, and delayed surgery.33,34 In
and how they interact with different physiotherapeutic inter- older children, responses are more limited, short-lived, increas-
ventions. This review is not systematic, but represents the ingly inhibited by the presence of fixed contractures.33 Kahra-
clinical expertise of the Cerebral Palsy Team of the University man et al, who found that repeated BoNT is a safe and effective
Hospitals Leuven, combined with the current available data- treatment approach, demonstrated that the first two injections
based on the greatest level of evidence from literature. Botu- were especially effective in relieving spasticity and improving
linum toxin (BoNT), oral medication, intrathecal baclofen (ITB), fine and gross motor activities.33 However, other crucial factors
and selective dorsal rhizotomy (SDR) will be discussed within a in the success of BoNT-injections are an adequate selection of
physiotherapeutic context. In addition, we will describe clinical the target muscles, specific and multidisciplinary goal-setting,
reasoning strategies to identify treatment goals as well as the and an integrated approach including PT and orthotic manage-
appropriate and corresponding treatment interventions. ment.19,21,22,32 In addition, adequate definition of outcome
Neuropediatrics
measures is a major factor when defining the effectiveness of treatment cycles (six assessments) were reviewed using the
BoNT, as inappropriate measures to assess spasticity can nega- Edinburgh Visual Gait Analysis Scale. The standard post-BoNT
tively affect clinical decisions.35 therapy involved offering all children a 6-week block of weekly
Indeed, positive effects of BoNT injections in the lower goal-directed physiotherapy sessions which included isolated
limb in children with CP combined with PT are reported, in and functional muscle strengthening, balance skills, muscle
particular when treated muscles are included in a strength stretching, gait re-education, training of activities of daily
training program. Jang and Sung demonstrated that higher living. Improvements in gait quality were statistically signifi-
frequencies of PT post BoNT, varying between 1 and 5 h/wk, cant, but did not reach the EVGS smallest real difference value
were associated with greater gait improvements, as deter- of 4 points.
mined by the physicians rating scale (PRS). The frequency of
PT was associated with both a change in dorsiflexion at the Dosage
ankle joint and a change in PRS at 12 weeks after injection.36 The total BoNT dose is a crucial determinant of outcome. Still,
Unfortunately, Jang and Sung did not specify the exact although general guidelines are available,21,42 the optimal
training programs used. Similarly, Williams et al applied dosage per muscle depends on the muscle volume (possible
BoNT in the lower limb, combined with a predefined pro- to assess using 3D freehand ultrasound), the amount of
gressive strengthening program based on an extensive spasticity, and the degree of the muscle’s involvement in
strength evaluation of the child, stretching and functional the pathological motion pattern.28–32 Other crucial factors in
tasks. Compared with the isolated treatment with BoNT, the the definition of the exact dosage are age, therapeutic
results of the combined approach caused better results on indication, number of previous treatments, and treatment

spasticity reduction and improving strength. In addition, goals in relation to expected outcome.28–32
they were significantly more successful in achieving individ-
ual functional goals, as measured by the goal attainment Side and Adverse Effects
scale.37 A recent systematic review by Fonseca et al, assessed Systemic effects of BoNT occur as the total dose of BoNT
the effect of combined BoNT and physiotherapeutic inter- increases. Commonly reported side and adverse effects are
ventions on gait parameters. The results showed superior fatigue, flu-like symptoms, swallowing difficulties, increased
results of high-intensity interventions after BoNT and seizures and bladder and bowel incontinence.45–52 These are
showed that improvements in gait were maintained after usually transient. No increased risk is reported between one
the end of the PT protocol.38 The content of the therapy and two episodes of BoNT.50 However, the most commonly
provided was, however, very heterogeneous consisting of a reported adverse effect is muscle weakness and/or fatigue.45,46
combination of stretching, strengthening, functional and gait Animal studies have indicated altered microscopic muscle
training. Other recent reviews by Mathevon et al and Picelli properties, including muscle atrophy (30–60%), changes in
et al found evidence for the effectiveness of resistance muscle fiber distribution, decreased quantity of myosin heavy
training and electrical stimulation post BoNT.39,40 chains, increased amount of collagen (40%), and altered
In upper limb treatment, Lidman et al found better out- microribonucleic acid (mRNA) profiles for a select subset of
comes on the Assisting Hand Function Assessment (AHA) in a relevant molecules, 1 to 6 months post-BTX injections.51–53
group of children receiving bimanual training of repetitive Loss of contractile material, associated with fatty infiltration,
functional ADL tasks combined with stretching and BoNT did not fully recover within 6 months.53 Surprisingly, the
versus a group receiving bimanual training and stretching structural alterations seemed to get established after the first
only.41 A similar bimanual training program combined with injection and were not exacerbated by multiple BoNT injec-
BoNT by Speth et al, led to superior effects on hand grip tions.53 This is in contrast to mRNA profiling, showing upre-
function, active supination, and thumb abduction compared gulation of several inflammatory mediators, proteinases, and
with the treatments performed separately.42 adipocytes-related molecules that worsened with increasing
In addition to those described above, literature describing number of BTX sessions.52 These studies were, however, done
the long-term combined effects with PT is scarce. Löwing et al43 with high doses of BoNT and short intervals, when compared
evaluated short and long-term effects of repeated BoNT com- with clinical practice in patients with CP. Human studies on
bined with goal-directed physiotherapy in a group of 40 microscopic properties post BoNT are rare. One pilot study,
children with CP (4–12 years old, GMFCS I and II). The authors involving only two healthy participants,54 documented 24%
found significant but clinically small long-term improvements atrophy in the gastrocnemius up to 12 months post BoNT,
in gait. Plantarflexor spasticity was reduced after three 3 and while a more recent uncontrolled cross-sectional study55
remained stable, while passive ankle dorsiflexion increased confirmed the risk for atrophy and reported altered fiber
after 3 months but decreased again slightly after 12 months. distribution after multiple BTX sessions. Yet, muscle volume
Goal-attainment gradually increased, reached the highest defined by muscle imaging did not differ between children
levels at 12 months, which were maintained at 24 months. with a treatment history of repeated BoNT injection sessions
A longer term study by Read et al44 included 17 children from those receiving no more than one session of BoNT
with bilateral CP and dynamic equinus (age mean [standard injections. However, while muscle volume approximates mus-
deviation, 4.0 [2.2] years, GMFCS I and II) after a retrospective cle mass, it may not be directly representative for the amount
analysis of their gait analysis records. Pre- and posttreatment of contractile material, especially taking into account the
2D video gait analyses for the first three lower limb BoNT suspected increased levels of fatty infiltration and collagen.
Neuropediatrics
Promising results were demonstrated by a recent study by well as at the supraspinal level and the reticular formation. It
Eek and Himmelmann and by Lee et al who found increased thereby reduces mono-and polysynaptic reflexes and is
muscle strength in the injected muscles 6 months after the particularly useful in reducing painful spasms.60 The most
injection.56,57 Thereby, also Williams et al showed muscle commonly used type of benzodiazepines is diazepam.
atrophy up to 5% immediately after injection, which was Although the report of the Quality Standards Subcommittee
almost completely recovered after an intensive training of the American Academy of Neurology and the Practice
program.37 Hence, BoNT treatment is advised to be com- Committee of the Child Neurology Report does not support
bined with an exercise protocol, which proved to be helpful or refute the use of diazepam, several studies report behav-
to avoid muscle atrophy and weakness. ioral improvements and sleep improvements attributed to
its use.59 Still, as some studies do report a potential risk of
Specific Key Points in PT and BoNT respiratory distress symptoms, long-term use as well as
high-dose treatment using diazepam should optimally be
• The use of BoNT reduces spasticity and therefore provides
avoided.60,61
a window of opportunity for muscle function and activity-
Feeding, bathing, and exercise times are reported as less
based training.14,20,39,40
stressful for children, with less crying and irritability.62,63 A
• In the lower limb, specific gait training and active func-
randomized controlled trial by Mathew and Mathew dem-
tional training are essential parts of the training
onstrated significant improvements in passive range of
process.27,31,38,39,43,44
motion, reduced spasticity, and decreased voluntary move-
• In the upper limb, bimanual training of repetitive func-
ments after administering bedtime diazepam.62 To the best
tional activities are recommended.19,42,58

of our knowledge, none of these studies assessed improved
• Strength training enhances the recruitment of antagonist
motor function. Diazepam is recommended for short-term
muscles in the advantageous timing of tone reduction. It
use, as experts caution that the prolonged use of this
reduces the potential decrease in muscle volume associ-
medication can produce physical dependence.60,64
ated with the use of BoNT and should optimally include
the injected muscles, build up progressively.14,37,40,56,57
Conclusion
Conclusion Diazepam can be considered as a cheap and effective way of
There is high-level evidence that BoNT has positive effects on relieving spasm and hypertonia and is an appropriate mea-
muscle tone. There is a need for an integrated approach sure to decrease hypertonia during sleep.62,63 Direct effects
including activity-based therapy and intensive strength train- in optimizing PT and facilitating movement in children with
ing to improve muscle recruitment and prevent the negative spasticity are rarely investigated. It should be considered as a
effects of muscle atrophy. Evidence of its effectiveness on gross short-term antispasticity treatment in children with CP and
and fine motor function is available. More research is needed should optimally be administered before bedtime.63
on the possible long-term effect of its use if not carefully
prescribed with an intense strength training regime. Oral Baclofen
Baclofen acts at the level of the spinal cord binding to
Oral Medication GABA-B receptor sites, suppressing the release of excitatory
The oral medications for tone reduction work at various points neurotransmitters. Augmenting GABAergic activity conse-
along the tonic stretch-spinal reflex arc, or at the level of the quently reduces spasticity. Monosynaptic responses are
muscle itself. The majority of these medications work either to more affected than polysynaptic responses.65 Delgado
increase the GABAergic inhibition, or to inhibit excitatory et al59 report conflicting level II evidence regarding the
neurotransmitters.59 Others, however, such as dantrolene effectiveness of oral baclofen in reducing spasticity and
work by inhibiting the release of calcium ions from the improving function in children with CP, a finding that
sarcoplasmic reticulum, thereby diminishing the force of was confirmed in a very recent high-quality review by
the contraction of the muscles. Unfortunately, the majority Navarette-Opazo et al.65 Nevertheless, van Doornik et al
of oral medications are not likely to manage high tone and evaluated voluntary ability to activate ankle plantar flexor
rarely eliminate spasticity entirely.59 Nevertheless, these com- muscles and found that mean maximal voluntary neuro-
monly used tone reducing modalities can be used in conjunc- muscular activation significantly increased after treatment
tion with each other, to potentially produce adjunctive effects with oral baclofen. Maximal plantar flexion torque did not
on the patient’s hypertonicity.59 change.66 These results indicate that tone reducing medi-
►Table 1 provides an overview of the mode of action, side- cation can facilitate strength training by increasing the
effects, and recommended doses for the most commonly ability to voluntarily activate muscles.66
used tone reducing medication.
Conclusion
Benzodiazepines Conclusions regarding the administration of oral baclofen
The mechanism of action of benzodiazepines is the increased demonstrate its safe long-term use, however, conflicting
presynaptic inhibition at the spinal cord level. It directly evidence results on its effectiveness. There is limited but
augments gamma-aminobutyric acid (GABA) postsynaptic promising knowledge that baclofen both directly and indi-
action, creates an inhibitory effect at the spinal reflex arc, as rectly facilitates PT and more specifically, strength training.
Neuropediatrics
Table 1 Mode of action, effectiveness, recommended dosage, and side/adverse effect of the most commonly used tone-reducing
oral medications
Mode of action Effectiveness Side and Dosage Peak level

adverse after intake
effects
Benzo-diazepines59–64 Increases presynaptic Behavioral improvement Weakness 0.12–0.8 mg/kg/d 1–2 h
inhibition at the spinal
cord level.
Directly augments Sleep improvement Ataxia
GABA postsynaptic
action.
Inhibitory effect at the Improved care/reduced Drowsiness
spinal reflex arc, stress (bathing, feeding,
supraspinal level, and and exercising)
the reticular
formation.
Monosynaptic > Improvements in pROM, Hypersalivation
polysynaptic spasticity and voluntary
movements
Oral baclofen59,65,66 Acts at the level of the Conflicting regarding the Somnolence 5–15 to 2–3 h

spinal cord binding to effectiveness in reducing 40–60 mg/d
GABA-B receptor sites. spasticity and improving
function
Agonizing the site and Increased mean maximal Hypotonia
suppressing the voluntary neuromuscular
release of excitatory activation
neurotransmitters.
Withdrawal symptoms in Weakness
abrupt discontinuation
Nausea
Vomiting
Dizziness
Dantrolene59,67–71 Inhibits the release of Nonsignificantly reduced Decrease in 0.5–1.0 mg/kg 30 min
calcium ions from the spasticity grip strength
sarcoplasmic
reticulum.
Diminishes the force Nonsignificantly reduced Sedation Max. 12 mg/kg/d
of the muscle’s reflexes
contraction.
Nonsignificantly reduced Nausea
scissoring
Functional improvement Vomiting
Diarrhea
Paresthesia
Hepatoxicity
Alpha-2-cholinergic Presynaptically hyper- Significantly reduced Sedation 1–2 mg 2h
agonists59,72–75 polarizes the spasticity and
motoneurons and hyperreflexia
decreases the release
of excitatory
neurotransmitters.
Brain and spinal level Reduced diazepam use Bradycardia
Antinociceptive Hypotension
effects by release of
substance P in the
spinal cord.
Abbreviations: GABA, gamma-aminobutyric acid; pROM, patient-reported outcome measures.
Neuropediatrics
Dantrolene Specific Key Points in PT

Dantrolene acts by inhibiting the release of calcium ions
• Taking into account the optimal time of action, diazepam
from the sarcoplasmic reticulum and this diminishes the
and dantrolene are optimally administered before night
force of the muscle’s contraction. It has the largest impact on
time,59,60 tizanidine and clonidine 1 to 2 hours before
the fast contracting muscles. It is, however, not selective for
therapy,8,72 and oral baclofen 2 to 3 hours before
only spastic muscles and may therefore not be an optimal
therapy.59,65,66
choice for ambulant children with CP and is contraindicated
• The therapist should optimally be in close interaction
for children with myocardial diseases.67–71
with the medical doctor regarding general weakness.59
Only a limited number of studies have reported positive
• Oral baclofen can increase the ability to voluntarily acti-
effects of dantrolene on spasticity, reflexes, and scissoring in
vate muscles, indicating a potential facilitation of strength
which the majority were not significant.64,65 A double-blind
training.66
study performed by Joynt and Leonard on 20 children with
spastic CP, found irregular and nonsignificantly reduced
Intrathecal Baclofen
force of muscle contraction, yet with objective functional
improvement, as measured by multiple performance tests.69 Effectiveness
The main side effect of this drug is a dose-dependent Baclofen can also be delivered intrathecally via a drug deliv-
decrease in stretch reflexes and grip strength with diffuse ery system, consisting of a subcutaneously-placed pump
weakness.70,71 containing a drug reservoir, connected to a catheter running
posteriorly into the subarachnoid space. This produces

Conclusion higher local concentration in cerebrospinal fluid at a fraction
There is insufficient evidence to support or refute the use of of the equivalent oral dose thereby avoiding excessive seda-
dantrolene for the treatment of spasticity in CP and the tion. ITB is indicated in those patients, in whom predomi-
general concern regarding its potential adverse effects nantly lower extremity spasticity is severe, problematic, and
should be taken into consideration. Therefore, currently it intractable to oral doses of medications and/or focal
is not generally recommended to prescribe dantrolene. treatment.76–80
A Cochrane systematic review by Hasnat and Rice com-
Alpha-Cholinergic Agonists pared the effects of ITB on spasticity, gross motor function,
Alpha-2-adrenergic agonists act at the level of the brain and or other areas of function and controls in a pediatric
the spinal cord, like presynaptically hyperpolarizing the population with CP.77 The short-term studies demonstrated
motoneurons and decreasing the release of excitatory neuro- positive effects on spasticity, comfort, and care.78 One
transmitters, thus decreasing the spastic response.59 In longer-term study included in the review, demonstrated
addition, α-2-adrenergic agonists show antinociceptive limited effects on spasticity but small improvements on
effects by the release of substance P in the spinal cord. gross motor function and quality of life.79 However, all
The most commonly used type of α-2-cholinergic agonists studies were identified with a high risk of bias in the
is tizanidine. Tolerance has been reported to be excellent.72,73 applied methodology.77 The conclusions of the Cochrane
A double-blind randomized controlled trial by Vásquez- review are very similar to the conclusions of Delgado et al
Briceño et al demonstrated that spasticity and the reflex and of Pin et al.59,80 More recently, Bonouvrié et al, ques-
activity decreased significantly more in the group of tizani- tioned 52 patients (39 Spastic CP, 13 Dystonic CP) and found
dine in comparison with a placebo group.72 relatively high satisfaction scores and positive effects on
Clonidine is another type of α-1 adrenergic agonist used personal care and communication.81 Also, McCormick et al
for the treatment of spasticity. Although studies on this found that long-term treatment with intrathecal compared
drug are rare, cases with new onset seizures after starting with oral baclofen was associated with reduced spasm
clonidine have been described, as well as cases of brady- frequency and severity as well as greater dose stability.82
cardia and hypotension requiring cardiac resuscitation Clinical experience in our CP team regarding the use of ITB
and reduced anxiety.59,74,75 Chalkiadis et al compared in younger children indicates a significant impact on gait
diazepam use, muscle spasm, analgesia, and side effects function, improved positioning, and comfort. For example,
when clonidine or fentanyl was added to epidural bupi- as ITB often significantly reduces tone, new adapted seating
vacaine in children with CP after multilevel orthopedic is often necessary.83–85 A recent review by Buizer et al
surgery.8 Clonidine and fentanyl provided adequate anal- described high level evidence for the effectiveness of ITB on
gesia with low rates of muscle spasm, resulting in low different measures of body function and structure, but
diazepam use.8 limited effects on activity and participation.86 None of the
included studies in this review, however, reported a com-
Conclusion bined approach with PT, which might be a possible expla-
Although with limited evidence, tizanidine seems to be nation for the lack of translation of the results to, for
effective on spasticity, without major side or adverse effects. example, gross motor function activities.83 The most com-
No long-term effects have been reported. Optimal effects are monly reported goals for ITB placement are, however,
visible up to 2 hours after intake. There is limited evidence to improve ease of care, positioning, transfers, and goals
support or refute the use of clonidine. related to ambulation.83
Neuropediatrics
Dose • As the PT is usually very familiar to the patient and the

Albright and Ferson reported that a continuous infusion of patient’s muscle tone and the impact on daily function,
ITB of 400 µg/d results in cerebrospinal concentration of 380 frequent feedback of the PT to the pump manager is
µg/L and a plasma concentration of less than 5 µg/L.87 recommended.83,87
Recommendations plead for a trial of ITB prior to implanta-
tion and this with an initial bolus of 50 µg.87 After this initial Conclusion
50 µg, this bolus is usually adjusted to 100 µg/d. The range of The benefits of tone reduction by means of ITB must be
doses required by individuals with CP is quite broad, from 30 weighed against the risks of intrathecal pump and catheter
up to 1,500 µg/d or more.88,89 Our center generally performs placement in patients considering ITB. Studies evaluating the
a double blind trial with a dosage of placebo or saline, 25, 50, use of ITB combined with functional training are rare but
75, or 100 µg. The pump manager will receive direct feedback strongly recommended for further research and this in
from daily tone assessment, usually performed by the particular in patients with GMFCS III, IV, and V.
trained physical therapist and the applied treatment dosage
will be double of the best trial dosage.83,90
Selective Dorsal Rhizotomy
Side and Adverse Effects Mode of Action
Sedation or lethargy is the most common adverse effect.89,90 The definition of spasticity implies that it involves both the
Also reported are headache, dizziness, hypotonia, and radi- motor and sensory systems, since the externally imposed
culopathy. At our center, these adverse effects are rarely movement, different velocities, and changing joint angles

registered and are much more commonly reported in rela- depend on the afferent feedback from the proprioceptive
tion to the use of oral baclofen. Several reports warn for system.93 Balanced excitatory and inhibitory influences on
possible complications of pump and catheter placement the α motor neurons result in normal muscle tone. Brain
including cerebrospinal fluid (CSF) leaks, seromas, catheter damage can result in descending tracts not being able to
misplacement, and wound infections.90,91 A long-term fol- provide their inhibitory influence, therefore producing an
low-up study by Thakur et al suggests that a technique of imbalance with an excess of excitatory influence. SDR is
paraspinal subfascial catheter placement translates to long- undertaken to reduce the excitatory input from the afferents,
term decreases in CSF leakage and complications from thereby decreasing the abnormal, increased muscle tone in
erosion, infection, and also catheter malfunctions.91 Rushton CP.94,95
et al showed that ITB pumps do not accelerate progression of Guidelines for the patient selection criteria and surgical
scoliosis in quadriplegic spastic CP.84 A similar matched technique are not uniform. The selection criteria vary from
cohort study by Walker et al, found no difference in the rates place to place and even within an institution.94 Published
of new onset neuromuscular scoliosis for those with CP and guidelines exist for age, diagnosis, tone, ambulatory ability,
ITB pumps and those without ITB pumps. Walker et al did birth history, motor control, specific medical conditions,
register a higher rate of progression as well as an increased orthopedic status, availability of postoperative therapy,
rate of posterior spine fusion surgery in individuals with CP and intellectual development. However, despite the contro-
who had ITB pumps compared with those with CP who did versy, common aspects in the selection criteria are those
not have ITB pumps.85 These conflicting results regarding born preterm with imaging consistent with periventricular
progressive scoliosis after ITB pump placement indicate the leukomalacia, primarily spastic tone, evidence for fair selec-
necessity of adequate and regular monitoring post-ITB pump tive motor control, fair strength, and gait energy inefficiency
and, adequate positioning and training of trunk control and of greater than two times that of speed-matched controls.95
strength and may include orthotic spine treatment when Children selected for an SDR need to be able to cooperate and
indicated.84,85 follow through a rehabilitation program.95
Sommer and Petrides reported a significant increase of Regarding the surgical procedure itself, dorsal rootlets are
depression and behavioral changes under the influence of exposed, after a multilevel laminectomy/laminotomy or
baclofen (orally of intrathecal).92 To the best of our knowl- after a single laminectomy. The rootlets to be transected
edge, this has not been confirmed in other studies. are identified by evaluating the electromyographic response
after electrophysiological stimulation and muscle contrac-
Specific Key Points in PT tion. Literature describes a variation between 25 and 50% of
the rootlets being transected.94 In our center, a percentage of
• As children receiving ITB are often less functional, thera- 25 to 30% of the rootlets are usually transected. Electrodes
pists should more intensively focus the intervention are usually placed on the psoas (L2), vastus lateralis (L3),
following ITB on goals related on comfort and daily tibialis anterior (L4), peroneus longus (L5), and gastrocne-
care.80,83,86 mius (S1).94 Single twitch, decremental, or squared
• As the use of ITB significantly decreases tone, ITB often responses are considered to be normal. Incremental, chronic,
results in the need of a (drastic) change in seating multiphasic, and sustained responses which spread to three
systems and if needed, orthotic spine treatment. The or more muscles beyond the primary level of stimulation or
PT should be actively involved in monitoring spine curve the opposite leg are considered abnormal. Rootlets with
progression.84,85 abnormal response are cut. This is repeated for each sensory
Neuropediatrics
root on both sides (S1 or S2 to L1). Intraoperative monitoring compared with children who only underwent SDR. A better
of the pudendal nerve together with limited division of the alignment increased the hip abduction and extension
S2 nerve root is now commonly practiced to reduce the risk moment during gait, which did not only result in a better
of incontinence and to prevent unmasking excessive gait, but likely also provided a more optimal position for the
weakness.94–96 physical therapist to train hip extension and abduction.105
Using the techniques describe above, the rates of intra-
operative, perioperative, and postoperative complications Specific Key Points in PT after SDR
are low and resolve by the time of discharge. Careful intra-
• Start as soon as possible (after 94 hours, the risk of a dura
operative monitoring, meticulous hemostasis, and surgical
leak is significantly reduced).94,106
decision-making limit the percentage of rootlets cut and
• Start with gentle passive range of motion and build up
contribute to the safety and efficacy of the procedure.94,95
toward an intensive active program until at least
12 months postoperatively. In our center, 3 to 4 months
Effectiveness
of intensive rehabilitation at the hospital, is followed by an
Short-term effects of SDR on spasticity and gait quality are
intensive home program of minimally 1 year.106,107
demonstrated.95,96 For long-term effects, a review by Grunt
• Restrict passive hamstrings stretch and trunk rotation for
et al showed moderate evidence of SDR to have a positive
the first 3 to 6 weeks.106,107
long-term influence on body structure and function, but no
• In further postoperative progression, individually tailored
evidence was demonstrated on activity and participation
exercises should target muscle length (prone positioning,
domains.97 The long-term effects of an SDR were also nicely
hip flexor stretching), strength training (with a high

mapped in a prospective follow-up by Tedroff et al, who
emphasis on hip extensors, knee extensors, and dorsi-
demonstrated a slight recurrence of spasticity at the knee
flexors), core stability training (shoulder and upper back),
and ankle after 10 years and joint range of motion declined
and integration into the required functional context (gait,
from a maximum at 3 years after an SDR to the 10-year
transfers, and other functional activities) with attention
follow-up. Median ambulatory status was best 3 years after
to appropriate lower limb alignment.106,107
SDR and then declined.98 Ailon et al performed a retrospec-
tive review on 45 children and found durable results in Conclusion
spasticity after 10 years in children with GMFCS II and III With specific attention to preoperative selection and appro-
but to a lesser extent in GMFCS IV and V.99 Van Oudenhoven priate postoperative rehabilitation, the effects of SDR are
et al identified selective control during gait as the best considered to be clinically significant.
predictor for improvement at the knee and ankle, which
demonstrates clear window of opportunity for the physical
Tone Reduction and Physical Therapy
therapist. After SDR, when hamstrings spasticity is absent,
children with better motor control can perform this move- Stretching
ment, whereas children with poorer selective motor control Muscle stretching can be performed using manual active and/
can be hindered by the flexion synergy.100 or passive techniques. Theis et al evaluated the effect of
In 2002, a meta-analysis was performed to compare SDR 6-weeks passive ankle stretching on muscle-tendon unit
plus PT versus PT alone.101 Three trials were selected: Stein- parameters in children with spastic CP.108 The results showed
bok et al,102 McLaughlin et al,103 and Wright et al.104 All three an (limited) increase of 3 degree in maximum ankle dorsiflex-
centers confirmed that SDR consistently reduces or elimi- ion, but this was accompanied by a 13% reduction in triceps
nates spasticity. There was a difference in the functional surae muscle stiffness, with no change in tendon stiffness.
outcome with two studies showing a statistically significant Additionally, there was an increase in fascicle strain with no
advantage for SDR101,102 and the third showing no advan- changes in muscle length at resting state, suggesting muscle
tage.103 The applied physiotherapy programs consisted of stiffness reductions were a result of alterations in intra/extra-
stretching, strengthening, and training in functional move- muscular connective tissue. Kalkman et al found increased
ments which intended to enhance mobility. The Toronto ROM as an acute effect of stretching, but no changes in fascicle
protocol by Wright et al called for a stronger emphasis on lengthening or torque, confirming that stiffness of the muscle
strengthening and on postural control for the SDR þ PT group fascicles in children with CP remains unaltered.109 The results
as compared with the PT-only group, based on the rationale of all these studies, however, provide a sound basis for the
that the anticipated weakening effect of the surgery would optimal combination of tone reduction with passive stretching,
provide a negative bias.104 Treatment planning for the PT- as both are complementary addressing the viscoelastic prop-
only group in Toronto was based on written goals set by erties of the muscle as well as the muscle hyperreflexia
community therapists before the randomized group assign- associated with spasticity. This also explains why both day-
ment. Postoperative protocols for the surgical groups in all and night orthoses are better tolerated when combined with
three centers varied in emphasis and timing. Interestingly, tone reduction.
Van Campenhout et al in our center recently found that Stretching by joint manipulation should, however, con-
children who first underwent femoral derotation osteotomy sider the material properties of both, the muscle and tendon.
followed by SDR started with a more complex gait pathology, Higher relative stiffness in the muscle fascicles compared
but showed fewer gait deviations 3 to 5 years post SDR, with the stiffness of the tendon in children with CP reduces
Neuropediatrics
muscle lengthening when rotating the joint. This reduced of 1 repetition maximum and three series of 8 to 12 repetitions
muscle strain during ankle stretch might also explain why at a minimum frequency of training of three times per week
functional improvements, such as gait kinematics after are requirements to obtain a significant increase in muscle
stretching interventions, are inconsistent.108,109 strength. Additionally, it is essential to train for a minimal
Kalkman et al aimed to ascertain whether increasing duration of 8 weeks and crucial to maintain the muscle
tendon stiffness, by performing resistance training, improves strength also after the period of BoNT injections.119
the effectiveness of passive stretching, indicated by an increase
in medial gastrocnemius fascicle length. Sixteen children with Muscle Length, Type of Muscle Contraction, and Loop
CP were randomly assigned to a combined intervention of Single joint resistance training may be more effective for less
stretching and strengthening of the calf muscles (n ¼ 9) or a functional children, particularly at the beginning phases of
control (stretching-only) group (n ¼ 7). Resting fascicle length training, as well as for adults who tend to compensate when
and tendon stiffness increased more in the intervention group performing bilateral, multijoint exercises.120 Children, adoles-
compared with the control group. Maximum dorsiflexion cents, or adults with CP who are not able to walk indepen-
angle increased equally in both groups, providing proof of dently might also benefit from strength training, but they may
principle that a combined resistance and stretching interven- lack the selective motor control needed to perform single joint
tion can increase tendon stiffness and muscle fascicle length in exercises.118,120 The therapist chooses that position where the
children with CP.110 specific amplitude to be improved can be targeted.
An example of a more dynamic training is described by Hösl Muscle strength is joint angle and contraction dependent.
et al, who demonstrated that backward-downhill walking leads Specific attention should be given to the selection of open- or

to a larger single stance dorsiflexion at comfortable walking closed-loop training, depending on the specific needs of the
speed and faster maximally achievable walking velocities com- targeted function.118 Also, the specific type of muscle contrac-
pared with manual stretching. The manual stretching, however, tion is important. In general, for a child with CP, concentric
did reduce knee flexion in swing, particularly at faster walking exercises are easier and are preferable to eccentric exercises.
velocities. Backward downhill training probably improved Eccentric muscle work is more strenuous, requires a higher
coordination and reduced dynamic stretch sensitivity.111 level of body perception, which is usually limited in children
with CP.118,119 However, eccentric muscle work is often
Positioning in Orthoses and Mobility Aids very crucial during functional activities (e.g., coming
Not only are the orthoses better tolerated in combination down the stairs). Whenever possible and indicated, eccentric
with tone reduction, but reversely, the use of day and night muscle work should be used in alternation with concentric
orthoses is crucial to optimize the effects of tone reduc- muscle work.118,119
tion.21–23,28 By using day orthoses, the child takes profit of To stimulate the transfer of muscle strength into function,
the improved base of support with appropriate length con- the use of the same type of muscle contraction as used during
dition of the muscles. Orthoses supply the appropriate and the functional movement is recommended.
symmetrical biomechanical alignment to allow gait training
and support functional carry-over outside periods of tar- Functional Strength Training
geted motor training conducted by the physical therapist.112 The integration of newly acquired analytical muscle strength
Apart from the expected positive effects of standing on into functional activities is known to be particularly difficult
bone mineral density and circulation, positioning in a standing for most children. This implies that training the recruitment
table provides an elongated position of the hip and knee of specific muscle activity during a functional exercise is
flexors.113–115 Benefits are achieved provided that the child crucial, as physiological muscle strength is usually not
is positioned correctly with sufficient attention to the position sufficient.120,121 The child also needs to learn to activate
of the feet, sufficient knee- and hip extension, slight abduction, the muscles in a more functional exercise. Also, providing
and external rotation in the hips and adequate pelvic tilt. improved muscle length does not necessarily imply that the
child will activate its muscle at the improved range. There-
Muscle Strength Training fore, sufficient attention should be given to support the child
The period of selective tone reduction allows specific training in making this transfer to functional activities. Functional
of muscle activation and isolated muscle strength of agonist as strength training can be useful to facilitate this step. Practical
well as antagonistic muscles. Several studies demonstrate examples of functional strength training include sit to stand
positive effects of strength training, both on impairment and repetitions and climbing stairs and when the child is suffi-
activity level.116 In addition, a recent systematic review ciently functional, possibly with a weight belt.119,120
highlighted preliminary evidence that strength training leads
to muscle hypertrophy in children and adolescents with CP.117 Antagonists or Agonists
Improving the physiological condition of the muscles is an Although strength training mainly targets the antagonist
important treatment goal. Sufficient resistance and repeti- muscles, the spastic agonist muscle also requires specific
tions, alternated with periods of rest, are necessary to chal- attention. It is well known that spastic muscles show underly-
lenge the muscle without the risk of overtraining. ing weakness121,122 and additionally, strengthening exercises
There is a common agreement that general training prin- performed in a well-controlled manner in an appropriate
ciples can be applied.118 This implies a resistance of 50 to 80% position do not increase spasticity.
Neuropediatrics
Influencing Activity Limitations and Participation assessment should aim at setting goals for a combined
Selective tone reduction aims to decrease the negative effects treatment plan, taking into account strengths and weak-
of spasticity combined with improved muscle lengths.20 This nesses in the patient’s profile and environment. ►Fig. 2
provides ideal conditions to improve muscle strength. Inte- provides an overview of the specific key points in the clinical
grating this improved muscle tone, strength, and length during reasoning process from assessment to the implementation of
daily functional activities is a crucial step in therapy. However, the integrated treatment plan.
transferring the use of these improved joint and muscle
conditions to functional activities is challenging for most Assessment
children.40,42 Given the heterogeneity in CP, when selecting a tone reduction
For the more functional children, exercises in stance and treatment, it is of utmost importance to carefully evaluate the
transfers from sit to stance, walking and stair climbing are effect that spasticity and other impairments exhibit on motor
appropriate, while for the less functional children, rolling and function and their possible influence on motor development in
sitting activities and active transfer training can be applied. long term.20–22,31 This requires an objective evaluation of
Besides targeting specific training of a selected exercise at muscle length, tone and strength, trunk control, gross and
well-controlled velocities (guided by the therapist), is it also fine motor function as well as an objective overview of the
important to include fast movements. Balance coordination child’s limitations in participation, the barriers and facilitators
and speed are important and these can be practiced for in the environment, and the strengths and limitations of the
example in sports and games, as a preparation for participation primary caretakers. Optimally, assessment needs to be a com-
in group training and social activities.40,42 bination of assessments of clinical symptoms (often referred to

as “clinical measures”), which are preferably performed in an
objective (i.e., instrumented) way and more in-depth technical
Clinical Reasoning and Selection of the
investigations, such as gait analysis and 3D upper limb
Appropriate Modality of Tone Reduction
analysis.123–128
The wide variety of tone reduction modalities as well as the It should be noted that reported spasticity measures may
large array of accompanying PT techniques makes the choice reflect overestimations due to the frequent incorrect assign-
of an appropriate treatment combination extremely chal- ment of spasticity whenever a joint exhibits high resistance
lenging for the clinician. A first important step in clinical to passive movement.123,124 Many scientists as well as
reasoning is a profound evaluation of the child. Above all, clinicians use clinical spasticity grading scales such as the
Fig. 2 Clinical reasoning process and key points in the selection of the integrated treatment plan.
Neuropediatrics
Modified Ashworth scale to assess outcome. However, clini- ranging from rolling, kneeling to walking, running, and hopping
cal scales are not objective and fail to isolate spasticity from on one leg. It fulfills the criteria of reliability and validity with
nonneural components.35,124 The perceived resistance to the respect to responsiveness to change.133–135 For upper limb,
performed passive movement during these tests may be a the Melbourne Assessment,136 the AHA,137 and the Jebsen–
result of reflex muscle activity (spasticity), but also of Taylor138 are commonly used. The Melbourne Assessment is
nonneural mechanical properties such as changes in visco- based on 16 items comprising tasks that are representative of
elastic properties of joint structures and soft tissues.124 Even the most important components of unilateral upper limb
though this is particularly important in clinical trials evalu- function (reach, grasp, release, and manipulate). Most items
ating tone reduction, this aspect is often neglected. Although are further subdivided in two to four subitems that represent
objective evaluation of spasticity is challenging, our recent an aspect of the required movement, such as range of
research in the establishment of an instrumented spasticity movement, fluency, target accuracy, speed, and quality of
assessment, has been a major contributor in selecting both movement. The AHA measures how effectively the involved
the muscles to be targeted, as well as the appropriate means hand is spontaneously used in bimanual activities. The Jebsen–
to reduce spasticity.124 Taylor test measures movement speed in six unimanual tasks.
Spasticity should optimally be evaluated in static as well These evaluation instruments are examples of standardized
as in functional dynamic situations. In ambulant children, measurements that are commonly used within our center but
three-dimensional gait analysis (3DGA) is a commonly used can be complemented with several other instruments. Goal
measurement modality to help identify the severity of setting and decision making are usually not only based on the
spastic muscles during activities and to support the selection quantitative results but also take into account the movement

of target muscles for BoNT injections, multilevel surgery, quality, effort, and compensation strategies.
SDR, and for the fine-tuning of orthotics.125–127 It is consid- Comprehensive assessments in children with CP, using a
ered as an important additional measure to identify key set of evaluation instruments, are a prerequisite to clarify the
problems, to link gait features to the levels of spasticity, functional problems and thus, to tailor tone reduction treat-
muscle weakness, lack of muscle control and/or secondary ment to the specific patient.139,140
impairments. Improved insight in the interaction between
these impairments and gait provides a basis for clinical Goal Setting
decision, which aids in explaining the specific problems of Carefully selected treatment goals need to be set and the
the child and as such, helps in delineating the therapy goals. appropriate treatment adjusted to meet these goals. Successful
Also, it is crucial to distinguish primary problems from treatment relies on realistic and achievable goal setting, and this
compensations.127 should be planned at the appropriate time for the individual
Upper limb movements in children with CP can be assessed child, keeping in mind the long-term expectations. The goals of
using 3D motion analysis. Children can be evaluated during treatment should be agreed between the child, the family, and
reaching, grasping, and gross motor tasks. Jaspers et al identi- the health professionals involved in care. Multidisciplinary
fied distinct spatiotemporal characteristics with specific devi- assessment should precede these decisions and the information
ations at the trunk, proximal, and distal joints. Usually, and views provided by the patient’s family and caregivers
children with unilateral CP used more trunk flexion and had should be taken into consideration.27,31,43–45,83 The timing of
a significant increased scapular protraction. They showed a intervention should not only take into account the progress of
more frontally oriented upper arm position and less end point the child, the severity, and the risk of contractures, but also the
shoulder elevation. At the wrist, there was usually more wrist age, the school situation, and the impact on the family at that
flexion and more radial deviation. As such, 3D analysis can particular moment in time. Patient characteristics, including
reveal the specific patterns of movement and identify the capacity, family support, and the availability of therapy and
specific target muscles and appropriate dosages for injection. other health professionals’ support should be considered.43,44,83
Moreover, the severity of spasticity can be objectively assessed
during a functional situation.128–130 Selection of Tone Reduction Modality and the Set-Up of
In addition, trunk control in children with CP is impaired to the Accompanying PT Program
a various extent, depending on the topography and severity of The choice between selective or general tone reduction
the motor impairment. Objective evaluation of trunk control depends on the underlying strength and selective muscle
can be particularly essential in children with prematurity or control of the child, the viscoelastic properties of the muscle,
children with severe and multiple disabilities. The Trunk the axial tone, and timing.
Control Measurement Scale can give insight into the strengths A review paper by Roberts et al describes gait analysis as a
and weaknesses of the child’s trunk performance and therefore tool to guide the selection of candidates for SDR.139 Features
can have valuable clinical use in the identification of an such as consistency of the gait pattern, pure spasticity, and
appropriate treatment plan.131,132 good selective control are identified as positive outcome
An assessment of the functional impact of spasticity can be predictors.139 In our experience, a positive trial with BoNT
performed using standardized testing. The Gross Motor Func- can be a good predictor for SDR outcome. In BoNT treatment,
tion Measure (GMFM-66 or GMFM-88) is a standardized Bar-On et al demonstrated that, when using instrumented
clinical instrument to evaluate change in gross motor function spasticity measurement, baseline muscle activity (expressed
in children with CP. It evaluates a set of gross motor activities as root mean square electromyography values) and joint
Neuropediatrics
torque were good predictors for a positive response to Conflict of Interest

BoNT.123 Sätilä and Huhtala found that children with less None.
severe functional deficits, good selective control, and mild
equinus are the optimal candidates for BoNT treatment at the
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Review Article

Tone Reduction and Physical Therapy: Strengthening

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Introduction to 4 per 1,000 newborn children, it is the most common cause

received © Georg Thieme Verlag KG DOI https://doi.org/

“a velocity-dependent increase in muscle tone.”4 It is, however,

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Mode of action Effectiveness Side and Dosage Peak level

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Abbreviations: GABA, gamma-aminobutyric acid; pROM, patient-reported outcome measures.

Dantrolene Speciﬁc Key Points in PT

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Dose • As the PT is usually very familiar to the patient and the

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torque were good predictors for a positive response to Conﬂict of Interest

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