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Burgess 2020
Burgess 2020
Burgess 2020
Andrea Burgess, Roslyn Nancy Boyd, Mark David Chatfield, Jenny Ziviani &
Leanne Sakzewski
To cite this article: Andrea Burgess, Roslyn Nancy Boyd, Mark David Chatfield, Jenny Ziviani &
Leanne Sakzewski (2020): Hand Function in 8- to 12-Year-Old Children with Bilateral Cerebral
Palsy and Interpretability of the Both Hands Assessment, Physical & Occupational Therapy In
Pediatrics, DOI: 10.1080/01942638.2020.1856286
Article views: 86
CONTACT Andrea Burgess a.burgess@uq.edu.au The University of Queensland Faculty of Medicine, QCPRRC, 62
Graham Street, South Brisbane, 4101, Australia.
Supplemental data for this article is available online at https://doi.org/10.1080/01942638.2020.1856286.
This article has been republished with minor change. This change do not impact the academic content of the article.
ß 2020 Taylor & Francis Group, LLC
2 A. BURGESS ET AL.
with cerebral palsy stated, “Parents want assessments which highlight abilities, and focus
on the possibilities” (Stanley, 2020).
For children with cerebral palsy (CP), upper limb activity measures are used to
inform discussion regarding a child’s upper limb strengths, intervention priorities and
progress. Systematic reviews have identified the Assisting Hand Assessment (AHA)
(Krumlinde-Sundholm & Eliasson, 2003) and the Both Hands Assessment (BoHA)
(Elvrum et al., 2018) as the most suitable tools to measure hand performance for chil-
dren with unilateral and bilateral CP respectively (Burgess et al., 2019; Gilmore et al.,
2010; Klingels et al., 2010). The AHA, published in 2003 has well-established psycho-
metric properties (Holmefur et al., 2007; 2009; Krumlinde-Sundholm et al., 2007),
whereas the BoHA is a relatively new outcome measure, published in 2018 (Elvrum
et al., 2018).
The BoHA provides therapists with the means of measuring and describing spontan-
eous bimanual activity performance in children with bilateral CP, classified in Manual
Ability Classification System (MACS) levels I-III, aged between 18 months and 12 years
(Elvrum et al., 2018). The BoHA was developed through adaptation of the AHA
(Krumlinde-Sundholm & Eliasson, 2003) using similar theoretical concepts and Rasch
modeling to construct a measure which enables observations to be quantified (Elvrum
et al., 2018). The BoHA uses carefully chosen toys to elicit bimanual handling during a
semi-structured play session. The assessment is video recorded and later scored from
video recording according to specified criteria (Elvrum et al., 2017). Eleven unimanual
items are scored for each hand separately and cover categories of initiation, movements
of the arm and hand, grasp and release, and fine-motor adjustment. Five bimanual
items are scored for both hands together (one common score for both hands) and cover
categories of coordination and pace. Each unimanual and bimanual test item is given a
performance rating between 1 (does not do) and 4 (effective) which best describes per-
formance on the item. The total raw sum score (27–108) is converted to a BoHA-unit
(0–100 scale). The total BoHA-unit is a measure of bimanual hand use, with higher
scores reflecting better manual performance (Elvrum et al., 2018).
A feature of the BoHA is that it contains an asymmetry index which reflects the
asymmetry of hand use demonstrated by the child in the play session. The performance
rating scores of the 11 unimanual items for the left and right hand are used to calculate
the asymmetry index. The percentage difference between the two hands is higher for
those children who have a greater difference between hands on the 11 unimanual items
(Elvrum et al., 2018). The BoHA contains two linked unidimensional subscales: one for
children with asymmetrical use of the hands (BoHA-A) and one for children with more
symmetrical hand function (BoHA-S) (Elvrum et al., 2018). The BoHA-A is used for
children with 20% difference between the hands in the unimanual items as recom-
mended by the test developers. Asymmetry or symmetry of hand use as measured by
the BoHA is not to be confused with hand dominance. Hand dominance is the clear
and consistent preference for one hand to perform skilled movements, particularly in
bimanual activities (Kraus, 2006). The asymmetry index provides a measure of fre-
quency and quality of hand use during activities (Elvrum et al., 2017). A person with
typical hand function would be regarded as having symmetrical hand function when
measured by the BoHA.
PHYSICAL & OCCUPATIONAL THERAPY IN PEDIATRICS 3
A secondary aim was to examine the interpretability of the BoHA, to assist clinicians
and researchers to become more familiar with this upper limb activity measure.
4 A. BURGESS ET AL.
Methods
Participants
This cross-sectional study analyzed BoHA data from two research studies: (i) Predict-
CP (NHMRC 1077257 Partnership Project: Comprehensive Surveillance to Predict
Outcomes for School age Children with CP) (Boyd et al., 2017) and (ii) baseline data
from the Hand Arm Bimanual Intensive Training Including Lower Extremity Training
(NHMRC 144846) (HABIT-ILE) project (Sakzewski et al., 2019). Predict-CP was a rep-
resentative population-based cohort study (Boyd et al., 2017) which undertook compre-
hensive surveillance of children, born in Queensland, Australia (birth years 2006–2009)
with a confirmed diagnosis of CP (Rosenbaum et al., 2007). All children in the Predict-
CP study were assessed once between 8 and 12 years of age. Ethics approvals for
Predict-CP were gained through the Children’s Health Queensland Hospital and Health
Service Human Research Ethics Committee (HREC/14/QRCH/329) and The University
of Queensland’s Human Research Ethics Committees (2014001487) (Boyd et al., 2017).
The HABIT-ILE project included children aged 6–16 years with bilateral CP. Baseline
HABIT-ILE data of children aged 8–12 years only were used in this study (Sakzewski
et al., 2019). Ethics approvals were granted from Children’s Health Queensland Hospital
and Health Service Human Research Ethics Committee (HREC/17/QRCH/282), the
Medical Research Ethics Committee of The University of Queensland (2018000017/
HREC/17/QRCH/2820), and Cerebral Palsy Alliance (2018_04_01/HREC/17/QRCH/
282). Informed written consent was gained from the primary caregiver for their child to
take part in the respective studies.
Fifty-four children (33 males, 21 females) with a mean age of 10.0 (SD ¼ 1.1) years
participated in the study. All children had a confirmed diagnosis of bilateral CP (diple-
gia, triplegia, or quadriplegia), where both sides of their body were impaired, and
included the motor types of spasticity, ataxia, dyskinesia and hypotonia (Rosenbaum
et al., 2007). Of the 54 children, 44 were from the Predict-CP study, and 10 were from
the HABIT-ILE study. Children were classified in MACS levels I (n ¼ 20), II (n ¼ 18)
and III (n ¼ 16). Eighty-three percent of children had spasticity as their primary motor
type. The majority of children had symmetrical hand use, with only 10 of the 54 exhib-
iting asymmetrical hand use. Characteristics of the children are summarized in Table 1.
Measures
The BoHA measures effective use of the hands in bimanual activities for children with
bilateral CP (Elvrum et al., 2018). The BoHA is a standardized criterion-referenced test
for children who are classified in MACS levels I-III, aged between 18 months and
12 years (Elvrum et al., 2018). Information regarding the development, administration
and scoring of the BoHA was provided in the introduction of this paper.
The Manual Ability Classification System (MACS) is a five-level ordinal classification
system used to classify the manual ability of children with CP, aged four to 18 years
(Eliasson et al., 2006). The MACS describes how both hands are used together when
engaged in daily activities with respect to what is expected for a child’s age (Eliasson
et al., 2006; 2017). ; MACS level I represents the highest level of manual ability where
objects are handled easily, MACS level V the lowest level where objects are not handled,
and total assistance is required (Eliasson et al., 2006).
Procedure
Two experienced physical therapists performed the ratings of motor type and Gross
Motor Function Classification System (GMFCS) (Palisano et al., 1997; 2008). The
MACS level was rated by an experienced occupational therapist (AB) in consultation
with the child’s primary caregiver.
Assessments were completed at the Queensland Cerebral Palsy Research and
Rehabilitation Center, Center for Children’s Health Research, Brisbane, Australia.
Assessments were performed according to BoHA test guidelines. A height-adjustable
table and chair was used to provide appropriate seating for each child. The video cam-
era was placed high, diagonally opposite the non-dominant hand to enable a clear view
of the child’s hands. Assessment time varied between 15 and 25 minutes, depending on
a child’s level of impairment. All BoHAs were scored by the first author (AB), who
achieved certification for the measure from the BoHA developers in 2017. When scor-
ing, the assessor frequently paused and re-played the recording. Each video varied in
the time required for scoring (range from 35 minutes to 1 hour 30 minutes, commonly
about one hour).
Data analysis
Statistical analyses were performed using Stata 16 (Stata Statistical Software: Release 16;
StataCorp LLC, College Station, TX, USA). Summary statistics were described using
mean (95% confidence interval) or median (25th–75th percentile) for continuous varia-
bles, or frequency (percentage) for categorical variables. Linear regression (including
ANOVA) and t-tests (unequal variances) were used to examine the differences between
the mean BoHA-units of groups of children based on MACS levels and on symmetry/
asymmetry of hand use.
An asymmetry index score of greater than 20% difference between hands was used as
the cutoff for determining categories of symmetry and asymmetry as per the guidelines
in the BoHA manual. Linear regression was used to examine association between
bimanual performance on the BoHA and age, gender, symmetry/asymmetry of hand
6 A. BURGESS ET AL.
function, and MACS levels. Age was entered as a continuous variable; gender, sym-
metry/asymmetry and MACS levels were entered as categorical variables. The signifi-
cance level used was 5%. Linear regression coefficients were presented with 95%CI.
Model fit was examined using Bayesian information criterion. T-tests were used to
examine the difference between the mean BoHA-units of the 8–12 year old children in
this study and mean BoHA-units of children aged 18 to 58 months from a cross-sec-
tional Norwegian study (Klevberg et al., 2017).
The interpretability of the BoHA was considered through examination of: (i) the dis-
tribution of scores of the study sample with respect to floor and ceiling effects, (ii) the
scores of children in well-known groups (MACS levels), and (iii) the mean performance
ratings for each BoHA item for each MACS level.
Results
The mean BoHA-unit for all 54 children was 71, with a standard deviation (SD) of 15.
The distribution (median, 25th and 75th percentiles) of BoHA-units for MACS levels I-
III are reported in Figure 1. There were significant differences in bimanual performance
as measured by the BoHA across MACS levels I–III (F(2,51) ¼71.44, p < 0.001). The
mean BoHA-unit (and 95%CI) for children classified according to each MACS level was
I ¼ 84 (81–89), II ¼ 72 (68–76) and III ¼ 53 (49–56). The MACS levels accounted for a
large proportion of the variance in the BoHA-units (Adjusted R-squared ¼ 0.73).
The mean (SD) BoHA-unit for children with symmetric and asymmetric hand use
are provided by MACS levels in Table 2. Children with symmetrical hand use had a
median BoHA-unit of 76 (range 42–100) and those with asymmetrical hand use 55
(range 46 to 74). Children with asymmetrical hand use had significantly lower BoHA
score than those with symmetrical hand use (mean difference¼ 18, 95%CI 25, 10,
p < 0.001, unequal variance used). Children with asymmetrical hand use (n ¼ 10) were
Figure 1. Boxplot showing bimanual performance of children with bilateral CP aged 8–12 years, as
measured with the Both Hands Assessment (BoHA), by Manual Ability Classification System
(MACS) levels.
PHYSICAL & OCCUPATIONAL THERAPY IN PEDIATRICS 7
Table 2. Bimanual upper limb activity performance of children with bilateral CP aged 8–12 years, by
symmetrical and asymmetrical hand use, and Manual Ability Classification (MACS) level – measured
using the Both Hands Assessment (mean BoHA-unit, (95%CI)).
BoHA-units
MACS Asymmetrical Mean (95%CI) Symmetrical Mean (95%CI) Total Mean (95%CI)
I – 84 (81–88) 84 (81–88)
II 66 (49–83) 73 (68–77) 72 (68–76)
III 54 (49–59) 51 (46–57) 53 (49–56)
Total 56 (51–62) 74 (70–79) 71 (67–75)
Table 3. Results from univariable linear regression with bimanual activity performance (BoHA-units
0–100 logit scale) as the outcome for children aged 8–12 years with bilateral cerebral palsy classified
in Manual Ability Classification levels I–III.
Effect Estimate Standard Error 95%CI p value
Age (years) 2 2 2, 6 0.25
Gender
Ref: Female
Male 2 4 10, 7 0.69
Asymmetry
Ref: Asymmetrical
Symmetrical 18 5 8, 28 <0.01
MACS levels
Ref: level I
II 13 3 18, 8 <0.01
III 32 3 37, 27 <0.01
Table 4. Results from multivariable linear regression with bimanual activity performance (BoHA-units
0–100 logit scale) as the outcome for children aged 8–12 years with bilateral cerebral palsy classified
in Manual Ability Classification levels I-III.
Effect Estimate Standard Error 95%CI p value BIC
Asymmetry
Ref: Asymmetrical
Symmetrical 0.36 3.3 6, 7 0.9 383.37
Age (years) 2 1.0 0.13, 4.0 0.04 383.37
MACS levels# 384.12
Ref: level I
II 13 2.5 18, 7 <0.001
III 32 2.5 37, 27 <0.001
modelled with MACS.
#
modelled with age.
MACS & Asymmetry model BIC ¼ 388.09.
MACS & age model BIC ¼ 383.37.
MACS BIC ¼ 384.12.
observed to be in MACS levels II and III only. The eight children with asymmetrical
hand use classified in MACS level III had similar scores to the eight children classified
in MACS III who had symmetrical hand use (mean difference ¼ 3, 95%CI 5,
10, p ¼ 0.5).
Univariate associations between the BoHA and variables age, gender, symmetry of
hand use and MACS levels are presented in Table 3. Results from multivariable linear
regression are presented in Table 4. Bimanual performance was not significantly associ-
ated with gender or age in univariate analyses. An overall increase of 2 BoHA-units for
8 A. BURGESS ET AL.
each year of age was noted in univariable analysis, and increased age was associated
with an increase in BoHA-units when considered in a multivariable model adjusting for
MACS levels (95%CI 0.13, 4.0; p ¼ 0.04).
Symmetry of hand use was a significant predictor of higher BoHA scores in univari-
ate linear regression but was not a significant predictor in a multiple regression model
which included MACS levels (Table 4). A model with MACS and age (Bayesian infor-
mation criterion 383.37, df ¼ 4) was similar to a model with MACS only (BIC ¼
384.12, df ¼ 3) in prediction of bimanual performance.
Comparison of the mean BoHA scores between the cross-sectional study of young
Norwegian children (aged 18-58 months) (Klevberg et al., 2017) and the 8-12 year old
Australian children in this study showed significant differences for children classified in
MACS levels I, II and III (mean difference MACS level I¼ 16, II¼ 21, III¼ 16,
all p < 0.001).
The quality description (four-point rating scale) for each BoHA item was examined.
Mean performance ratings for each BoHA item are provided according to MACS level
for bimanual items (Figure 2) and unimanual items (Supplementary Table S1).
Discussion
This study examined bimanual upper limb activity performance of Australian children
with bilateral CP, aged between 8 and 12 years, using the BoHA. Two of the three
PHYSICAL & OCCUPATIONAL THERAPY IN PEDIATRICS 9
hypotheses were supported. Firstly, there were significant differences in bimanual per-
formance across MACS levels I-III. Higher bimanual performance as measured using
the BoHA, was associated with better manual ability classification levels. Secondly, our
results showed similar patterns of bimanual performance as noted in earlier studies
(Elvrum et al., 2018; Klevberg et al., 2017; 2018) where symmetrical hand use was asso-
ciated with higher BoHA scores compared to asymmetrical hand use, and, gender was
not associated with BoHA scores. A relationship between age and bimanual perform-
ance was previously reported in studies on preschool aged children (Klevberg et al.,
2017; 2018) but not in the BoHA validation paper which contained children up to
12 years of age (Elvrum et al., 2018). Our study found weak evidence for an association
between bimanual performance and age, with an increase of 2 BoHA-units for each
year of age seen in this study sample.
The third hypothesis that the BoHA scores of children aged 8–12 years would be
similar to the estimated limits previously reported was not supported. This hypothesis
was based upon the longitudinal paper which used modeling to predict that children
with bilateral CP reached 90% of their estimated BoHA limit at approximately
30 months of age, with negligible increase in mean trajectory after age 50 months
(Klevberg et al., 2018). The mean scores achieved by children aged 8–12 years classified
in MACS levels I and II in our study sample were considerably higher than the esti-
mated mean limit reported previously (Klevberg et al., 2018). Comparison of our study
results with the baseline cross-sectional study of young children (aged 18–58 months)
(Klevberg et al., 2017) showed significant differences between the mean BoHA scores
for children classified in MACS levels I-III. The higher BoHA scores reported in this
study may be different to the previous studies (Elvrum et al., 2018; Klevberg et al.,
2017; 2018) for many reasons, including study sample population, cultural differences,
or rater calibration. Our study results highlight the need for longitudinal studies, which
continue past preschool age, in addition to rater reliability and test-retest reliabil-
ity studies.
There is currently little information regarding the development of bimanual perform-
ance in children with bilateral CP. In the Norwegian longitudinal study (n ¼ 42; median
age ¼ 52.5 months; age range 31–81 months), increased age was associated with
increased BoHA scores (Klevberg et al., 2018), yet, age was not correlated with BoHA
scores in the BoHA development and validation paper which used cross-sectional data
on children between ages 22 months and 13 years (n ¼ 171) (Elvrum et al., 2018). The
higher BoHA scores of the 8- to- 12- year old children in this study may be a result of
increased age, potentially accompanied by refinement of manual skill development.
Older children have also had more opportunities to develop successful strategies to
accommodate for limited hand function. For example, improved positioning and orien-
tation of objects will increase the pace at which activities proceed. Fine motor skill
development in typically developing children, as measured by the Peabody
Developmental Motor Scales-2, increases up until the test ceiling of 71 months (Folio &
Fewell, 2000). Hand skills progress in a developmental fashion, and typically developing
children make rapid improvement between the ages of 3 and 6 years in areas such as
object manipulation, grip force and complementary (asymmetric) hand task use
(Pehoski, 2006). One item on the BoHA, ‘Proceeds’, does require the assessor to
10 A. BURGESS ET AL.
Recommendations
The BoHA allows for comparison of bimanual performance of the same child on differ-
ent occasions, or between children. Currently there are no studies using the BoHA as
an outcome measure in an intervention trial. Further psychometric studies are required
to build on the usefulness of the BoHA for clinicians and researchers.
Recommendations include future studies on the parameters of reliability (inter-rater,
intra-rater and test-retest reliability studies), measurement error (standard error of
measurement and limits of agreement) and responsiveness (the ability of an instrument
to detect change over time) (de Vet et al., 2011). Smallest detectable change (i.e., the
change beyond measurement error) and the minimal important change (i.e. the smallest
change in score which a child/parent perceives as important) provide clinicians and
researchers with information as to whether a change in scores is statistically significant,
and whether it is clinically relevant (de Vet et al., 2011).
In order to further understand the trajectories of hand skill development for children
with bilateral CP, longitudinal studies across childhood and adolescence are required.
Presentation of data using means, confidence intervals and standard deviations in add-
ition to more complex analyses is recommended to allow straightforward comparison
between studies, and for ease of comprehension by clinicians.
To assist with rater reliability, periodical recalibration for BoHA scoring would be
beneficial, particularly for clinicians working in isolation. This could take the form of
videos accessible online specifically for recalibration purposes by certified clinicians. A
range of scored videos, which reflect the heterogeneity of children with bilateral CP,
would assist clinicians to remain faithful to the intended scoring criteria.
Limitations
Limitations of this study include the modest sample size. The BoHA has been developed
for children with bilateral CP, and children with diplegia or very mild CP may complete
all items to the maximum level of the measurement tool. As this is a research project
undertaken with a representative population cohort, all children with bilateral CP were
seen; whereas in the clinical setting some of these children would not be seen for assess-
ment of hand function as it would not be necessary.
Conclusion
The BoHA is a new measure of bimanual activity performance, and this is the first
study to document bimanual performance of children with bilateral CP aged between 8
and 12 years. This study confirmed interpretability of the BoHA in this Australian
12 A. BURGESS ET AL.
sample. The BoHA quantified observations of bimanual performance for children with
bilateral CP and differentiated between MACS levels I–III. Children with higher manual
ability achieve the highest scores on the BoHA, and children with asymmetrical hand
use performed significantly worse than those with symmetrical hand use. The mean
BoHA scores in this study of 8–12 year old children were considerably higher than pre-
viously reported in a cohort of young Norwegian children with bilateral CP. Research
recommendations include further evaluation of measurement properties and use of the
BoHA to examine longitudinal trajectories of bimanual performance development in
preschool and primary school aged children. The BoHA provides clinically meaningful
information and is of value to tailor upper limb interventions.
Acknowledgements
The authors give thanks to Dr Ann Kristin Elvrum for giving of her time and expertise to pro-
vide feedback to Andrea Burgess on her rating of five videos used in this study.
Disclosure statement
The authors report that no financial interest or benefit has arisen from the applications of
this research.
Funding
This project was supported by the National Health and Medical Research Council (NHMRC)
under grant Predict-CP 1077257; Australian Government Research Training scholarship (AB);
Children Hospital Foundation – Lola Hughes Efstathis Top-Up scholarship (AB); NHMRC CDF1
Fellowship (LS 1160694); Children’s Hospital Foundation Mary McConnel Career Boost for
Women (LS); and NHMRC Research Fellowship (RB 1037220)
improve motor, social and participation outcomes of infants, children and adolescents with cere-
bral palsy and acquired brain injuries.
ORCID
Andrea Burgess http://orcid.org/0000-0001-8697-5156
Roslyn Nancy Boyd http://orcid.org/0000-0002-4919-5975
Mark David Chatfield http://orcid.org/0000-0002-0004-6274
Jenny Ziviani http://orcid.org/0000-0002-8185-3405
Leanne Sakzewski http://orcid.org/0000-0001-5395-544X
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