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The dyskinesia impairment scale: a new instrument to measure dystonia and choreoathetosis in dyskinetic cerebral palsy

DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY The Dyskinesia Impairment Scale: a new instrument to measuredystonia and choreoathetosis in dyskinetic cerebral palsy ELEGAST MONBALIU1,2 ELS ORTIBUS3 JOS DE CAT3,4 BERNARD DAN5,6 LIEVE HEYRMAN1 PETER PRINZIE2,7 PAUL DE COCK8,9 HILDE FEYS1 1 Department of Rehabilitation Sciences, Katholieke Universiteit Leuven, Leuven. 2 Dominiek Savio Institute, DC GID(t)S Gits. 3 Department of Paediatric Neurology, UniversityHospitals Leuven, Leuven. 4 Clinical Motion Analysis Laboratory Leuven, University Hospital Pellenberg, Leuven. 5 Department of Neurology, Hpital Universitaire des EnfantsReine Fabiola, Brussels. 6 Faculty of Medicine, Universit libre de Bruxelles, Brussels, Belgium. 7 Department of Child and Adolescent Studies, Utrecht University, Utrecht, theNetherlands. 8 Centre for Developmental Disabilities, University Hospitals Leuven, Leuven. 9 Faculty of Medicine, Katholieke Universiteit Leuven, Leuven, Belgium.
Correspondence to Mr Elegast Monbaliu at Dominiek Savio Instituut, Koolskampstraat 24 8830 Gits, Belgium. E-mail: [email protected] This article is commented on by Smith on pages 205–206 of this issue.
AIM The aim of this study was to examine the reliability and validity of the Dyskinesia Impairment Accepted for publication 25th September 2011.
Scale (DIS). The DIS consists of two subscales: dystonia and choreoathetosis. It measures both Published online 16th January 2012.
phenomena in dyskinetic cerebral palsy (CP).
METHOD Twenty-five participants with dyskinetic CP (17 males; eight females; age range 5–22y; mean age 13y 6mo; SD 5y 4mo), recruited from special schools for children with motor disorders, BADS Barry–Albright Dystonia Scale were included. Exclusion criteria were changes in muscle relaxant medication within the previous Dyskinesia Impairment Scale 3 months, orthopaedic or neurosurgical interventions within the previous year, and spinal fusion.
Intraclass correlation coefficient Interrater reliability was verified by two independent raters. For interrater reliability, intraclass Minimal detectable difference correlation coefficients were assessed. Standard error of measurement, the minimal detectable Surveillance of Cerebral Palsy in difference, and Cronbach's alpha for internal consistency were determined. For concurrent validity of the DIS dystonia subscale, the Barry–Albright Dystonia Scale was administered.
RESULTS The intraclass correlation coefficient for the total DIS score and the two subscalesranged between 0.91 and 0.98 for interrater reliability. The reliability of the choreoathetosissubscale was found to be higher than that of the dystonia subscale. The standard error of themeasurement and minimal detectable difference values were adequate. Cronbach's alpha valuesranged from 0.89 to 0.93. Pearson's correlation between the dystonia subscale and Barry–AlbrightDystonia Scale was 0.84 (p<0.001).
INTERPRETATION Good to excellent reliability and validity were found for the DIS. The DIS maybe promising for increasing insights into the natural history of dyskinetic CP and evaluatinginterventions. Future research on the responsiveness of the DIS is warranted.
Cerebral palsy (CP) is worldwide the most common neuromo- due to sustained muscle contractions. Choreoathetosis in CP tor disorder in children, with an incidence of 2 to 3 per 1000 is dominated by hyperkinesia and tone fluctuation (but mainly live births.1,2 CP can be categorized into spastic, dyskinetic, decreased). Chorea refers to rapid, involuntary, jerky, often and ataxic groups. Dyskinetic CP is further differentiated into fragmented movements. Athetosis means slower, constantly dystonia and choreoathetosis.1,3 changing, writhing, or contorting movements.6,7 These SCPE Spastic CP is by far the most common type of CP, with a descriptions are in accordance with the recently published prevalence of approximately 80%,4 and is followed by dyski- definitions of dystonia, chorea, and athetosis by the Taskforce netic CP with a prevalence between 6.5%5 and 14.4%.4 on Childhood Movement Disorders.8,9 The Taskforce defines According to the Surveillance of Cerebral Palsy in Europe dystonia as a movement disorder in which involuntary sus- (SCPE),6 dyskinetic CP is characterized by involuntary, tained or intermittent muscle contraction causes twisting and uncontrolled, recurring, occasionally stereotyped movements, repetitive movements, abnormal postures, or both,8 chorea as in which the primitive reflex patterns predominate and muscle an ongoing, randomly appearing sequence of (one or more) tone varies.6 The SCPE described dystonia in CP as domi- discrete involuntary movements or movement fragments, and nated by abnormal postures that may give the impression of athetosis as a slow continuous, involuntary writhing move- hypokinesia and muscle tone that is fluctuating (but with easily ment that prevents maintenance of a stable posture.9 The defi- elicitable tone increase). Characteristics are involuntary move- nitions of the SCPE and the Taskforce describe dystonia and ments, distorted voluntary movements, and abnormal postures choreoathetosis in a very similar way and are essentially ª The Authors. Developmental Medicine & Child Neurology ª 2012 Mac Keith Press descriptive, based on consensus emerging from experts from What this paper adds different clinical and basic fields of science.
Good to excellent reliability and validity was found for a new clinical scale Over the last few years, there has been continuing develop- evaluating dyskinesia in cerebral palsy.
ment of interventions in children with dyskinetic CP, includ- This is the first scale that independently measures dystonia and choreoathetosis ing intrathecal baclofen,10–12 deep brain stimulation,13,14 oral in dyskinetic cerebral palsy.
The reliability of the choreoathetosis subscale was found to be higher than medication,15–17 ventral rhizotomies,18 and botulinum toxin that of the dystonia subscale.
injections.19 However, objective evidence supporting theseinterventions is only preliminary. Specific assessment of dysto- ited or no differentiation between action and rest or duration nia has mostly relied on the Barry–Albright Dystonia Scale and amplitude, and combined several dyskinesia characteristics (BADS).20 Operationally, the BADS has become a criterion within one score, which may limit the sensitivity of the scales standard for scoring dystonia in CP, but several studies10–17 (see Table I). Additionally, we explored the content and scale have reported the difficulty of measuring dystonia reliably construct of the Toronto Western Spasmodic Torticollis Rat- and ⁄ or questioned the sensitivity of the BADS.
ing Scale25 and the Unified Parkinson's Disease Rating Scale26 In a recent study,21 the reliability and validity of the BADS (Movement Disorder Society). Based on this analysis and the was reassessed and special attention was given to the sensitivity SCPE definitions of dystonia, choreoathetosis, and dyskinetic of the scale. This study showed reliability results similar to CP,3,6,7 the DIS was developed according to the methodologi- those of Barry et al.20 but also revealed limitations in the sensi- cal framework of Kirshner and Guyatt.27 Its content was thor- tivity of the BADS.
oughly discussed with a clinical expert team (EO, JD, HF, PD, Content analysis showed that the BADS included several and FR) from the Cerebral Palsy Reference Centre (University dystonia characteristics over eight body regions. However, the Hospital Pellenberg, Leuven, Belgium).
items are a combination of several different dystonia charac- In a second step, the interrater reliability of this scale was teristics within one score (e.g. duration and amplitude) and no assessed in a pilot study. Four physical therapists with exten- differentiation is made between rest and activity. Also, for the sive clinical experience of children with CP (UH, IV, ES, and first time, the measurement error of the BADS was assessed ED) underwent a training session with the reference and train- and a high standard error of measurement (SEM) and minimal ing DVD of the SCPE6 and were instructed on how to use the detectable difference (MDD) were found, respectively 6% and preliminary constructed scale. They then scored 10 videotaped 18%. In clinical practice, this means that a score difference of children with dyskinetic CP independently. Afterwards, the 18% is necessary to ascertain that ‘true' improvement has content of the scale, the included items, and the scoring crite- occurred, as lower values might be ascribed to measurement ria were discussed with these four raters and the clinical expert errors. Also in this study,21 two primary dystonia scales were team. Subsequently, the discussion together with (1) the num- evaluated in dyskinetic CP, namely the Burke–Fahn–Marsden ber of participants able to accomplish the task, (2) the reliabil- Movement Scale22 and the Unified Dystonia Rating Scale.23 ity of the item scores, and (3) the participants' clinical For these scales, even higher MDDs were found, 27% and experience, ensured that an item reduction was obtained and 25% respectively.21 Finally, several groups have emphasized that the scoring criteria and instructions were revised.
that dystonia and choreoathetosis often occur concurrently in The final DIS (Appendix I, supporting information pub- dyskinetic CP9,21,24 However, to our knowledge no standard- lished online) consists of two subscales, one for dystonia and ized tools for measuring choreoathetosis in CP have been one for choreoathetosis (see Fig. 1). Both subscales evaluate duration and amplitude in 12 body regions including the eyes, For these reasons, we have strived to develop a new assess- mouth, neck, trunk, and limbs. For the limbs, a distinction is ment tool to score dystonia and choreoathetosis at rest and made between the proximal and distal region and between the during activity in individuals with dyskinetic CP. We right and left side. For each of the assessed body regions, the attempted to enhance the sensitivity of this tool in comparison duration refers to the amount of time that dyskinesia is pres- with the commonly used dystonia scales. In this paper, we ent, whereas the amplitude aspects refer to the range of describe how we developed the DIS and assessed its reliability motion of the dyskinetic movements. All body regions are and validity.
scored during two activities (action) and one resting posture(rest). Summation of the region scores gives a total action score (range 0–192) and a total rest score (range 0–96) for both Development of the dyskinetic impairment scale subscales. The action and rest scores add up to a total One of the first steps in the development of the DIS consisted score for dystonia and choreoathetosis, each with a range from of a content analysis of the three available secondary and pri- 0 to 288. The total DIS score is the sum of the dystonia and mary dystonia scales.20,22,23 In accordance with Sanger et al.,9 movements can be described by the context in which theyoccur, for example postural, rest, action, or associated with spe- Reliability and validity cific tasks.9 Dyskinesia characteristics can be assessed at rest and during activity and in terms of duration, amplitude, and This study included 25 participants aged between 5 and 22 influence on functional activities. From this point of view, con- years (17 males; eight females; mean age 13y 6mo; SD 5y tent analysis revealed that the three scales analysed made lim- 4mo). All participants were diagnosed by a paediatric neuro- The Dyskinesia Impairment Scale Elegast Monbaliu et al.
Table I: Characteristics of the Burke–Fahn–Marsden Movement Scale (BFMS), the Unified Dystonia Rating Scale (UDRS) the Barry–Albright Dystonia Scale (BADS), and the Dyskinesia Impairment Scale (DIS) Secondary dystonia aNumber of items. +, present; ), absent.
Dystonia subscale Choreoathetosis subscale Figure 1: Diagram of the Dyskinetic Impairment Scale.
logist and were recruited from special schools for children the presence of their own physiotherapist. The duration of with motor disabilities. Individual participant characteristics videotaping was similar to the duration in other dystonia are presented in Appendix II (supporting information pub- scales (e.g. Unified Dystonia Rating Scale, BADS, Burke– lished online). Exclusion criteria were changes in muscle relax- Fahn–Marsden Movement Scale), with a maximum of 30 ant medication within the previous 3 months, orthopaedic or minutes. The passive range of motion of the upper and lower neurosurgical interventions within the previous year, and spine limb joints was measured with a goniometer to serve as a fusion. Ethical approval was obtained from the Ethical Com- baseline for the amplitude assessment of the DIS. Afterwards, mittee of the Katholieke Universiteit Leuven. All participants a video montage was made in accordance with the scoring and ⁄ or their parents provided informed consent.
order of the DIS.
To assess interrater reliability, two physical therapists (EM, JV) scored all videos in series within 15 days. The two raters Based on the recommendations of the Dystonia Study had experience in discriminating dystonia and choreoathetosis Group,23 the 25 participants were videotaped (by ES and in CP and were trained in scoring with the DIS.
MV) according to a standard video protocol. It contained all To assess concurrent validity, the second rater (JV) postulated activities and rest postures of the DIS (see Appen- scored the BADS for all 25 participants. The BADS evalu- dix III, supporting information published online). An effort ates dystonia over eight body regions on a five-point ordi- was made to provide relaxing surroundings. All participants nal scale. The video protocol was also used to assess the were filmed in their habitual environment at school and in Developmental Medicine & Child Neurology 2012, 54: 278–283 Statistical analysis were 0.87, 0.87, and 0.88, respectively, during action and 0.90, Rigby's statistical recommendations28 were applied. For in- 0.94, and 0.93 respectively, during rest. ICCs for the body terrater reliability, the intraclass correlation coefficients (ICCs) regions of the duration factor during action were moderate to and 95% confidence intervals (CIs) were used for the total excellent except for the eyes, neck, and trunk regions. The scores and item scores of the DIS. Portney and Watkins29 amplitude aspect showed moderate to excellent reliability for considered an ICC higher than 0.90 as excellent, an ICC 7 of the 12 regions and lower reliability for the neck, trunk, between 0.75 and 0.90 as good, and an ICC<0.75 as poor to right proximal arm, and both proximal legs. During rest, mod- moderate. To interpret the ICC scores<0.75, we considered erate to excellent reliability was found for the duration aspect ICC values between 0.60 and 0.75 as moderate and less than for nine regions and lower reliability for the neck, right proxi- 0.60 as poor. The SEM and MDD were calculated using the mal leg, and left distal leg. The amplitude aspect presented formula SEM=SD·(1)ICC) and MDD=SEM·1.96·2.29 moderate to high reliability for all regions. For the choreo- The internal consistency was evaluated by Cronbach's alpha.29 athetosis subscale, the ICC of the total scores of the duration Concurrent validity was determined by Pearson correlation aspect, amplitude aspect, and the summation of both were coefficients. All statistics were calculated with SPSS 16.0 0.97, 0.94, and 0.96, respectively, during action and 0.96, 0.93, (SPSS Inc., Chicago IL, USA).
and 0.96 respectively, during rest. ICC region scores of theDIS choreoathetosis subscale ranged from moderate to excel- lent except for the duration of the left distal leg, the eyes Interrater reliability amplitude aspect during activity, and the eyes amplitude dur- The total score of the DIS, the dystonia subscale, and the cho- reoathetosis subscale showed excellent interrater reliabilitywith ICCs of 0.96 (95% CI 0.91–0.98), 0.91 (95% CI 0.91– Standard error of measurement and minimal detectable 0.86), and 0.98 (95% CI 0.95–0.99) respectively.
The ICCs and 95% CIs of the total subscale scores and For interrater reliability, the SEM and MDD values for the region scores are presented in Table II.
total DIS were 3% and 9% respectively. The SEM and MDD For the dystonia subscale, ICCs of the total scores of the were 5% and 15% for the DIS dystonia subscale and 3% and duration aspect, amplitude aspect, and the summation of both 7% for the choreoathetosis subscale.
Table II: Interrater reliability: intraclass correlation coefficients (ICC) with 95% confidence intervals (CI) between raters for the Dyskinesia Impairment Scale Dystonia subscale Choreoathetosis subscale RP, right proximal; LP, left proximal; RD, right distal; LD, left distal.
The Dyskinesia Impairment Scale Elegast Monbaliu et al.
Internal consistency found in previous studies.20–23 The choreoathetosis subscale Cronbach's alpha for the dystonia subscale during action was also revealed excellent interrater reliability both during action 0.91 for the duration aspect and 0.92 for the amplitude aspect.
and during rest. For the body regions, almost all ICCs During rest posture, Cronbach's alpha was 0.90 and 0.93 for exceeded 0.60, except for the eyes region. Owing to the lack of duration and amplitude respectively. Similar values were found other choreoathetosis assessments in CP, comparison of these for the choreoathetosis subscale: 0.92 for duration and 0.90 results with other studies is not possible.
for amplitude during action, and 0.94 and 0.89 for duration The DIS dystonia subscale generally showed a somewhat and amplitude respectively, during rest posture.
lower interrater reliability than the choreoathetosis subscale.
This can be explained by the lack of sustained postures in cho- Concurrent validity reoathetosis and the more identifiable nature of choreoatheto- Pearson's correlation between the DIS dystonia subscale and sis,5–9 which makes choreoathetosis easier than sustained BADS was 0.84 (95% CI 0.66–0.92; p<0.001).
postures of dystonia to score on videotapes. Nevertheless, thereliability of the majority of the dystonia region scores was sufficient and total scores showed good to excellent ICCs.
In this study, the DIS was developed to measure both dystonia The SEM and MDD showed small values. The MDD for and choreoathetosis in dyskinetic CP. These movement disor- interrater was 9% for the total DIS, 15% for the dystonia sub- ders are known to be mostly simultaneously present in this scale, and 7% for the choreoathetosis subscale. The measure- participant group.9 The DIS also allows the measurement of ment errors (MDDs) for the DIS are obviously lower than the dystonia and choreoathetosis separately. This is important for measurement errors for the BADS (18%), Burke–Fahn–Mars- further determining the dominant type of movement abnor- den Movement Scale (27%), and the Unified Dystonia Rating mality, as recommended by Rosenbaum et al.3 The descrip- Scale (25%).21 In other studies, MDD values for other mea- tion and definitions of dystonia and choreoathetosis5–7 were surement scales, for example for upper limb function in chil- the starting point of the DIS. In accordance with the clinical dren with CP, have varied between 9% and 13%.32 Low evaluation recommendations of the Taskforce on Childhood MDD values, as presented for the DIS, will benefit the Movement Disorders,9 we have included several components such as action, rest, duration, and amplitude so that dyskinetic Also, the internal consistency was high and indicates a stable movement disorders could be measured in their predominant rating construct in measuring choreoathetosis and dystonia in presence and the context in which they occur. The DIS mea- dyskinetic CP.29 The high internal consistency and the good sures both dystonia and choreoathetosis, thus allowing the MDD values of the DIS support the use of the scale in long- possibility of calculating a ratio between these movement dis- term follow-up and intervention studies, but future studies are orders in dyskinetic CP and thereby increasing our insight needed to assess the responsiveness of the DIS.
into the full clinical presentation and natural history of dys- Finally, the validity of the DIS was assessed. Content valid- kinetic CP. It is well known that the expression of dystonia ity was achieved by analysis of the available measurement and choreoathetosis is mostly linked to brain lesions in the scales for dystonia and by the content discussions with the basal ganglia.30 However, their pathophysiology is complex expert group of the CP Reference Centre and the clinical rat- and not fully understood.31 Therefore, it is hoped that a reli- ers of the special schools for children with motor disabilities.
able, valid, and sensitive clinical measurement of dystonia and Concurrent validity was attained for the dystonia subscale, in choreoathetosis may result in the recognition of dyskinesia which a good correlation was found with the BADS.
patterns that can be related to the observed brain lesions, and This study has some limitations. A first shortcoming is the subsequently may enhance our insight into the pathophysiol- absence of a concurrent validity assessment for the choreo- ogy of CP in the long term. Such a tool should also help in the athetosis subscale. This could not be investigated owing to the evaluation of existing and emerging treatments for children lack of available choreoathetosis scales in CP and must be with CP. Furthermore, the differentiation of dystonia and cho- assessed in future studies. Another criticism concerns the dura- reoathetosis in the DIS will be particularly important in judg- tion of scoring the DIS scale on videotape. This varied from ing the outcome of medical interventions focusing on one or 30 to 45 minutes per subscale, which may seem long for appli- both clinical symptoms.
cation in routine clinical practice. However, because the DIS In this study, we found excellent interrater reliability for the consists of two subscales, it covers an assessment of both total score of the DIS and the dystonia and choreoathetosis dystonia and choreoathetosis and gives an opportunity to map subscales. All ICCs exceeded 0.90 with a small 95% CI. The the dyskinetic movement disorder in a more comprehensive total score of the dystonia subscale showed higher reliability approach. Furthermore, the video time for the children was 30 than the BADS, Burke–Fahn–Marsden Movement Scale, and minutes maximum, which the participants tolerated very well.
the Unified Dystonia Rating Scale.20,22,23 This is similar to other video-based scales (e.g. the BADS).
The dystonia subscale also showed good interrater reliabil- Item reduction of the DIS may be a possibility for decreasing ity during action and excellent reliability during rest. The reli- the duration score of the scale, but this would require a larger ability of the region scores during action and rest overall was study group and its responsiveness to therapy should first be moderate to good. Reliability for the arms and legs was higher considered. A further consideration involves the complexity of than for the eyes, neck, and trunk regions. Similar results were differentiating between dystonia and choreoathetosis for the Developmental Medicine & Child Neurology 2012, 54: 278–283 different body regions, and therefore application ⁄ implementa- towards increasing insights in the clinical presentation and tion of the scale requires some clinical experience with dyski- natural history of dyskinetic CP. Therefore, we hope that it netic CP and careful application of the operational definitions will be a promising scale for measuring dystonia and choreo- of dystonia and choreoathetosis.
athetosis in long-term follow-up and medical intervention Despite these limitations, this study is the first to present a studies. Future research regarding the validity of the choreo- tool that measures dyskinesia, taking into account the simulta- athetosis subscale and responsiveness of the DIS is warranted.
neous presence of dystonia and choreoathetosis in dyskineticCP. Also, this clinical tool provides a unique contribution to evaluating choreoathetosis in CP, as, to our knowledge, no This work was supported by a grant of the Marguerite-Marie Delac- measurements have previously been available for choreoathe- roix Foundation. We thank all participants and the special schools for tosis in CP. The evaluation of dystonia and choreoathetosis children with motor disabilities: Sint-Jozef Antwerp, Dominiek Savio within one scale presents the prospect of including both Gits, Sint-Gerardus Diepenbeek, Ten Dries Landegem, and Sint- pathological signs in one dyskinetic score as a ratio between Lodewijk Kwatrecht. Special thanks are owed to Jasmien Verschaeve the presence of dystonia and choreoathetosis.
and Ellen Smits for scoring the participants, Mark Vermandere forvideotaping and montage, Filip Roelens, Ulla Huysmans, Els Schrij- vers, Ellen Debock, and Isabelle Vercruysse for clinical feedback and This study developed a new measurement tool to evaluate dys- scoring during the pilot study, and finally the Committee of Flemish tonia and choreoathetosis in dyskinetic CP. The DIS showed Motor Disability Institutes (KOMPAS) for encouraging this research.
high internal consistency and proved to be reliable betweenraters, with a low SEM and MDD. The concurrent validity ONLINE MATERIAL ⁄ SUPPORTING INFORMATION was established for the dystonia subscale. The DIS is a step Supplementary material for this article may be found online.
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The Dyskinesia Impairment Scale Elegast Monbaliu et al.

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