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Assessment of Unilateral spatial neglect (USN) in children was described fairly

recently (Hécaen 1976). Few cases (Ferro et al. 1984, Johnston


and Shapiro 1986, Ferro and Martins 1990, Thompson et al.
unilateral spatial 1991, De Agostini 1992, Manly 1997, Billingsley et al. 2002)
had been reported before recent articles demonstrating
neglect in children neglect in 12 children with acquired brain injury (ABI;
Laurent-Vannier et al. 2003) and in a group of children with

using the Teddy Bear perinatal brain lesions (Trauner 2003). Possible reasons for
the paucity of research on USN in children include its confu-
sion with hemianopia or dyslexia, and a lack of specific evalu-
Cancellation Test ation tests. Only a few tasks have been designed specifically
to assess USN in children. Thompson et al. (1991) proposed
the Pre-school Measure of Unilateral Neglect, a bingo-type
game of line drawings of animals. Recently, Trauner (2003)
Anne Laurent-Vannier* MD; introduced another task to measure objectively neglect behav-
Mathilde Chevignard MD, Department of Rehabilitation for iour in infants, toddlers, and preschool children in which
Children with Acquired Brain Injury, Hôpital National de children have to remove objects placed in front of them. The
Saint Maurice, St Maurice; order of object removal and the total time taken to remove all
Pascale Pradat-Diehl MD, UPMC/INSERM 731 – Department objects are recorded on videotape. However, the equipment
of Physical Medicine and Rehabilitation, Hôpital de la required for this task precludes its widespread use in every-
Salpêtrière, Paris; day clinical practice.
Geneviève Abada OT, Department of Rehabilitation for In our clinical practice in a department specializing in chil-
Children with Acquired Brain Injury, Hôpital National de dren with acquired brain lesions (Laurent-Vannier et al. 1998,
Saint Maurice, St Maurice; 2000), USN appeared to be more frequent than described in
Maria De Agostini PhD, INSERM U 472, Villejuif, France. the literature. To study USN in children aged over 2 years, we
designed the Teddy Bear Cancellation Test (TBCT; [Test de
*Correspondence to first author at Service de rééducation Barrage des Nounours] Laurent-Vannier et al. 2001, 2003). A
des pathologies neurologiques acquises de l’enfant, Hôpital cancellation test was chosen because such tests are easy to
National de Saint Maurice, 14 rue du Val d’Osne, 94415 Saint perform in clinical practice, and because cancellation tests
Maurice Cedex, France. are known to detect USN in adults (Halligan et al. 1989,
E-mail: a.laurentvannier@hopital-saint-maurice.fr Azouvi et al. 2002).
Therefore, the aims of the current study were: (1) to pro-
vide normative data for the TBCT and (2) to evaluate in a
The purpose of the study was to provide normative data for the prospective study the frequency of USN in children with ABI.
Teddy Bear Cancellation Test (TBCT) and to evaluate
prospectively the frequency of unilateral spatial neglect (USN) Method
in children with acquired brain injury (ABI). In the control MATERIAL
group (n=419; 218 males, 201 females; mean age 5y 1mo [SD 1y The TBCT was developed according to the same principles
4mo]; range 3 to 8y) omissions were rare and decreased with as the Bells Test (Gauthier et al. 1989) for adults. A sheet of
age. A left displacement of the first three teddy bears cancelled paper (21×29.7cm) included different pictures of objects
was observed with increasing age. This preferential left-to-right that are of interest to children. The teddy bear was chosen as
cancelling strategy was interpreted as learned under the the target because it is sex-neutral. Fifteen targets and 60 dis-
influence of reading habits. The same test was used prospectively tractors were distributed proportionately in a pseudo-ran-
in 41 children with ABI (24 males, 17 females; mean age 5y 5mo dom array in five columns. Each column was numbered from
[SD 2y]; range 3 to 8y) admitted to a paediatric rehabilitation 1 to 5 from left to right (Figs 1a,b).
department specializing in acquired brain lesions. In patients The examiner sat in front of the child and presented the
and controls, children under 6 years of age omitted more items child with a sheet showing a teddy bear crossed out. The child
than older children. The localization of omissions was skewed was then asked to cross out all the teddy bears. If the child
significantly to the left in children with right-sided lesions stopped before all the teddy bears were cancelled, the child was
compared with children with left-sided lesions. USN was asked once if the task had been finished. The task was com-
observed in seven patients with ABI. Left USN was found in pleted when the child stopped or said he had finished.
three of the 10 patients with right-sided ABI. Right USN was The following variables were used: number of omissions
present in two of the patients with 15 left-sided ABI and two of (out of 15), ‘location of omissions’ score (LO-S), and ‘loca-
the 16 patients with non-lateralized ABI. Left USN is frequent in tion of the first three teddy bears crossed out’ score
children after right-sided brain injury. The relatively high (START-S). LO-S was calculated according to the columns of
incidence of right spatial neglect in children is discussed in omitted items: –1 point for each omission in columns 1 and 2, 0
relation to the development of hemispheric specialization. for omissions in column 3, and +1 for each omission in columns
4 and 5 (Figs 1a,b). This score reflects the lateralization of
omissions. START-S was calculated with the same method.
This score can range from –3 for three items crossed out on
the left side to +3 for three items crossed out on the right
See end of paper for list of abbreviations. side. Children with ABI exhibiting a pathological number of

120 Developmental Medicine & Child Neurology 2006, 48: 120–125

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omissions (number of omissions ≥95th centile; see Table III) could leave the acute care department. Most of the patients
and a LO-S ≥2 were considered to have USN. in this study came from the neurosurgery or neurology
departments at Necker Enfants Malades children’s hospital
Participants in Paris, where they received care during the acute phase of
CONTROL CHILDREN their treatment. Forty-one children with acquired brain
Four hundred and nineteen children (218 males, 201 females; injuries (24 males, 17 females; mean age 5y 5mo [SD 2y];
mean age 5y 1mo [SD 1y 4mo]; range 3 to 8y), divided into range 3 to 8y) carried out the TBCT.
five age groups (Table I), underwent the TBCT. These age Most of the lesions (32/41) were traumatic. Location of
groups encompassed three levels of nursery school and two lesions was assessed by computerized tomography or mag-
grades in primary school. Children were recruited in two dif- netic resonance imaging. Children were divided into three
ferent urban areas corresponding to high and low socio- groups: two groups with right- or left-sided lesions exclusive-
economic status (SES; two schools in the Paris area and two in ly or predominantly, and a group with non-lateralized lesions
the suburbs). Handedness was defined by the hand used for (diffuse brain swelling, subarachnoid haemorrhage, or bilat-
writing. Exclusion criteria were a history of previous neuro- eral lesions; Table II). Children with ABI were divided into
logical or psychiatric disorders, or children who had repeated two age groups: under 6 years (n=22) and 6 to 8 years (n=19).
a grade more than once. Following the standard procedure, Clinical assessment was performed on admission and includ-
school inspectors (Public National Education system) and ed a thorough neurological examination to detect the pres-
school principals gave their approval for pupils to participate ence or absence of motor or sensory deficits and hemianopia.
in the study. Parents and children gave their informed consent. Depending on age, children also underwent cognitive tasks
The children took the test at school in a quiet room. such as drawing (spontaneous and copying) and placing
stickers on a blank sheet of paper. The TBCT was part of the
CHILDREN WITH ACQUIRED BRAIN INJURIES clinical assessment. Neglect behaviour in daily life was also
A prospective study was performed over one year in the investigated through clinical observation of daily life activi-
Department for Rehabilitation of Children with Acquired ties such as moving, eating, and personal care. Thirty of the
Brain Injury at the Hôpital National de Saint Maurice, St 41 children performed the TBCT in the first two weeks after
Maurice, France. Children were referred as soon as they admission to the Department of Rehabilitation, mostly on the

Table I: Demographic characteristics of control children

Age groups, y:m n Mean age Males:Females, Right:Left SES,


(SD), y:m n handed, n High:Low, n

3:0– 3:11 92 3:5 (0.27) 45:47 70:22 49:43


4:0– 4:11 116 4: 6 (0.28) 62:54 100:16 57:59
5:0– 5:11 115 5:6 (0.27) 65:50 99:16 65:50
6:0– 6:11 47 6:5 (0.29) 24:23 42:5 18:29
7:0– 7:11 49 7:7 (0.46) 22:27 40:9 24:25

SES, socioeconomic status.

a b

Figure 1: (a) Teddy Bear Cancellation Test. (b) Location of target in five columns.

The Teddy Bear Cancellation Test Anne Laurent-Vannier et al. 121

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day of admission. Some children admitted to the department to no omission at 7 years of age.
were awakening from coma or were agitated, so the test was No significant effect was found for age group, sex, hand-
administered later. For three of 41 children, the test could not edness, or SES on LO-S.
be administered due to organizational difficulties. START-S was found to be related to age group (F=3.66;
df=411; p<0.01). A left displacement of the first three teddy
Results bears cancelled was observed with increasing age. The effect of
CONTROL CHILDREN SES on the starting score showed a tendency towards signifi-
Table III gives the mean (SD) number of omissions, LO-S, and cance (F=2.96; df=411; p=0.08): the score was negative in
START-S for control children. The number of omissions both groups but greater for high (mean –0.51 SD 1.92) versus
decreased with age: analysis of variance (ANOVA; with age low (mean –0.21, SD 1.98) SES.
groups, sex, handedness, and SES as explanatory variables)
revealed a significant effect only for age group (F=12.6; CHILDREN WITH ACQUIRED BRAIN INJURIES
degrees of freedom [df]=411; p<0.001). The number of omis- Children in the three lesion groups did not differ in terms of
sions in the 95th centiles ranged from two omissions at 3 years age at lesion or at testing, sex, handedness, aetiology, or Verbal

Table II: Demographic and clinical characteristics of children with acquired brain injuries (n=41)

Characteristics Right lesions Left lesions Non-lateralized lesionsa

n 10 15 16
Age at lesion, mean (SD) y:m 5:6 (2:1) 5:5 (2:2) 5:7 (2:0)
Days since onset, mean (SD) 57.8 (71.1) 64.1 (77.4) 35.0 (36.6)
Males:Females, n 6:4 10:5 8:8
Right:Left handed, n 9:1 14:1 15:1
Aetiology, n
Traumatic brain injury 8 12 12
Tumours 2 1 0
Cerebrovascular disease 0 2 1
Infectious disease 0 0 3
Motor deficit, n 8 11 6
Sensory deficit, n 3 4 1
Hemianopia, n 2 2 2
Verbal IQ, mean (SD) 91.6 (16.7) 73.6 (19.9) 79.8 (9)
Performance IQ, mean (SD) 73.9 (13.7) 73.3 (14.6) 75.2 (15.3)
aDiffuse brain swelling, subarachnoid haemorrhage, or bilateral lesions.

Table III: Performance of control children in Teddy Bear Cancellation Test

Scoring variables Age groups


3y–3y 11mo 4y–4y 11mo 5y–5y 11mo 6y–6y 11mo 7y–7y 11mo

n 92 116 115 47 49
Omissions
Mean (SD) 0.61 (0.78) 0.24 (0.50) 0.20 (0.48) 0.13 (0.45) 0.02 (0.14)
Minimum 0 0 0 0 0
Maximum 3 2 2 2 1
95th centile 2 1 1 1 1
LO-S
Mean (SD) 0.09 (0.74) 0.03 (0.36) 0.03 (0.26) 0.06 (0.25) –0.02 (0.14)
Minimum –2 –1 –1 0 –1
Maximum 2 1 1 1 0
95th centile 2 1 1 1 0
5th centile –1 –1 0 0 0
START-S
Mean (SD) 0.04 (1.77) –0.32 (2.04) –0.34 (1.99) –0.45 (2.09) –1.22 (1.61)
Minimum –3 –3 –3 –3 –3
Maximum 3 3 3 3 3
95th centile 3 3 3 3 2
5th centile –2 –3 –3 –3 –3

LOS-S, location of omissions; START-S, location of first three teddy bears crossed out.

122 Developmental Medicine & Child Neurology 2006, 48: 120–125

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or Performance IQ. They did differ in terms of the frequency not observed on the TBCT but right neglect was found in
of motor deficit (χ2=6.19; df=2; p<0.05; Table II). The mean daily life activities and other tasks: omission of the right eye
number of omissions, LO-S, and START-S for each lesion group on the spontaneous drawing of a face, omission of the right
are shown in Table IV. part of a drawing, and displacement of the drawing to the left
For the number of omissions, ANOVA (with lesion groups, in a copying task.
age groups, and sex as explanatory variables) revealed a sig- Eight other children exhibited a pathological number of
nificant effect of age (F=4.18; df=1; 36; p<0.05). Children omissions without pathological LO-S, or neglect behaviours
under 6 years omitted more items (mean 2.59 [SD 3.4]) than in other tasks. It can be speculated that these non-lateralized
children aged 6 to 8 years (mean 1.21 [SD 2.12]). No effect of omissions are related to attention disorders. A double disso-
lesion group or sex was found. ciation was found between neglect and hemianopia. In this
For the LO-S, a significant effect of lesion group was study, three children with neglect had no hemianopia, and
observed (F=3.88; df=2; 36; p=0.02). Post-hoc analyses (t- two children with hemianopia had no neglect (Table V).
test) revealed that the group with right-sided lesions signifi-
cantly differed from the group with left lesions (t=–2.44; Discussion
df=23; p<0.05) and from the group with non-lateralized The TBCT was simple to use for control children and those
lesions (t=–2.34; df=24; p<0.05). No significant effect was with ABI. The omission rate was very low in the controls and
found between left-sided and non-lateralized lesions. Only decreased with increasing age. In 95% of controls, no more
children in the right-sided lesion group had a negative LO-S, than two omissions were observed at 3 years and no omis-
indicating that their omissions were located on the left. No sions were recorded at over 6 years of age. Rousseaux et al.
effect of sex or age was found. (2001) examined cancellation strategies in adults. In the Bells
For the START-S, statistical analysis showed no significant
effect of lesion or age group. Nevertheless, in children with
right brain injury the mean START-S was positive, indicating a
Table IV: Performance of children with acquired brain injury
right to left strategy, whereas it was negative in the other two
in Teddy Bear Cancellation Test
groups (Fig. 2).
Fifteen children exhibited a pathological number of omis- Scoring Right lesions Left lesions Non-lateralized
sions. Eight of them exhibited lateralized omissions and so variables lesionsa
were considered to have USN. Seven out of those eight patients
(Table V) showed concordant USN in daily life activities and n 10 15 16
Omissions
in other tasks. Three children among the 10 with right lesions
Mean (SD) 3.3 (4.1) 1.9 (3.0) 1.1 (1.6)
exhibited left USN and four children (two of 15 with left lesions Minimum 0 0 0
and two of 16 with non-lateralized brain lesions) exhibited Maximum 10 9 5
right neglect. No age difference was found between groups LO-S
of children with left and right neglect (mean 4.3 [SD 2] and Mean (SD) –1.3 (2.3) 0.6 (1.6) 0.4 (1.4)
mean 4.9 [SD 2.5] respectively) whereas children with Minimum –6 –1 –1
neglect were younger than the others (mean 4.5 [SD 2] and Maximum 2 5 4
mean 6.9 [SD 1.9]; t=–2.04; df=39; p<0.05). START-S
Two children showed a dissociation between the results Mean (SD) 0.2 (2.7) –1.0 (1.9) –0.6 (2.2)
in the TBCT and the other tasks (see Method). The first child Minimum –3 –3 –3
Maximum 3 3 3
(male, 3y 4mo with non-lateralized lesions) had three omis-
sions with an LO-S of +2 but did not show neglect behaviour aDiffuse brain swelling, subarachnoid haemorrhage, or bilateral

in the other tasks or in daily life. In the second child lesions. LOS-S, location of omissions; START-S, location of first three
(female, 5y 10mo with non-lateralized lesions) neglect was teddy bears crossed out.

Table V: Characteristics of seven children with unilateral spatial neglect (USN) detected by both Teddy Bear Cancellation Test and
by other tasks sensitive to USN and in daily life activities

Patient number, Aetiology Lateralization Location of Hemianopia Hemiparesis Hypoesthesia Days Number LO-S START-S
sex, age at onset of lesion lesion since of
(y:m), handedness onset omissions

1. F, 3:6, R Tumour R Subcortical Yes Yes Yes 7 10 –4 3


2. M, 6:7, R Traumatic R Subcortical No Yes No 41 9 –3 3
3. M, 3:1, R Traumatic R Hemisphere Yes Yes Yes 249 9 –6 3
4. M, 3:8, R Tumour L Temporal Yes Yes No 80 5 4 –2
5. M, 3:2, R Traumatic L Frontotemporal No Yes Yes 21 9 5 –3
6. M, 3:11, R Traumatic NL Diffuse brain Missing No No 15 3 3 1
swelling data
7. M, 8:6, R Traumatic NL Diffuse brain No Yes No 21 5 2 –3
swelling

LO-S, location of omissions; START-S, location of first three teddy bears crossed out. M, male; F, female; R, right; L, left; NL, non-lateralized.

The Teddy Bear Cancellation Test Anne Laurent-Vannier et al. 123

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Test they studied the location of the first item cancelled, and support the ability of the TBCT to detect USN. Nevertheless,
observed that controls, either right- or left-handed and using as for adults (Azouvi et al. 2002), a single test is not sufficient
their left or right hand, started crossing out on the left side of to rule out or confirm the presence of neglect, and a battery
the sheet. The START-S used in this study, which takes into of tests is needed to prevent USN from being misdiagnosed.
account location of the first three cancellations, seems to Lateralized omissions have sometimes been attributed to
reflect better the cancellation strategy than considering only hemianopia. We observed a double dissociation between USN
the first item cancelled, as the effects of chance are reduced. and hemianopia. Consequently, hemianopia cannot explain
In the present study, the START-S demonstrated a leftward the lateralized omissions in the TBCT and cannot explain USN
displacement with increasing age. The youngest children did behaviour (Halligan et al. 1990; Laurent-Vannier et al. 2001,
not have a left-to-right cancellation strategy. As age increased, 2003; Billingsley et al. 2002). USN has also been confused with
the children, like adults, began cancelling from the left. other disabilities such as dyslexia (Manly et al. 1997).
Reading habits have been shown to influence the exploration The cancellation strategy must also be considered. We
of non-linguistic stimuli as well as visuo-spatial skills (Chokron observed a right-to-left strategy in children with right brain
and De Agostini 1995, 2000). In the present study, the age- injury, and a left-to-right strategy in children with left brain
dependent left-to-right cancellation strategy probably reflects a injury. Although a left-to-right strategy alone cannot detect
learned process underlying visuo-spatial performance (Frith right USN, as it is also the strategy used by control children,
1998). Consistent with this interpretation, children with a high the presence of a right-to-left cancellation strategy could reveal
SES exhibited a tendency to present a more consistent left-to- left USN in children with brain injury. In adults with left USN,
right strategy than children with a low SES (F=2.96; df=411; the right-to-left strategy, different from the normal strategy,
p=0.08) We can assume that these children may have had the was the most sensitive measure in a battery assessing neglect
opportunity to read earlier than the other children. (Azouvi et al. 2002). In children, this abnormal strategy of
Twenty-six of the 41 children with brain injuries performed environmental exploration may persist long after the brain
the TBCT within the age-predicted range, indicating that brain lesion. It has been reported previously (Billingsley et al. 2002,
injury alone does not produce abnormal results. Fifteen of the Laurent-Vannier et al. 2003, Trauner 2003) and interpreted
children with brain injuries exhibited a pathological number as persistent USN.
of omissions. As in the controls, patients under 6 years of age The second objective of this study was to assess the fre-
omitted more items than older children. quency of USN in children with ABI. To our knowledge, this
Half of the children with a pathological number of omis- is the first prospective study assessing USN frequency in chil-
sions exhibited them in a non-lateralized way. This was inter- dren with brain injury acquired after the pre- and perinatal
preted as relating to attention disorders rather than USN. stage. Our findings suggest that the frequency of USN ranges
Gauthier et al. (1989) had the same interpretation in adults. from 13% (in left and non-lateralized lesions) to 30% (in right
The other half of these children exhibited a pathological num- lesions). This study confirms our previous hypothesis that
ber of omissions and lateralized omissions on the left or on left and right neglect are not rare in children (Laurent-
the right, which was interpreted as USN. Only two children Vannier et al. 2003). However, USN does appear to be some-
provided results in the TBCT that were not concordant with what less frequent in children when comparing the current
performances in other tasks. Therefore, there is evidence to results with a systematic review of published reports of
adults with cerebral stroke (Bowen 1999): left spatial neglect
was found in about 43% of adult patients with right brain
injury and in 21% of those with left brain injury.
0.5 In children as in adults, left USN appears to be more fre-
quent and probably more severe than right neglect. Right
0 USN may be more frequent in very young children (Laurent-
Vannier et al. 2003, Trauner 2003). Contrasting with the mature
brain, one may speculate that a transition from bilateral to
–0.5
lateralized representation of spatial awareness can occur dur-
ing the first years of life (Laurent-Vannier et al. 2003).
–1
■ LOS-S In adults (Azouvi et al. 2002, Buxbaum et al. 2004) and chil-
■ START-S dren, USN induces severe disability in daily activities (Laurent-
–1.5 Vannier et al. 2001, 2003), and can have a negative impact on
academic performance in reading, writing, and mathematics.
–2 For this reason, it is important that USN be correctly diagnosed
Right Left Non-laterized Controls so that adequate rehabilitation can be initiated at an early stage.
lesions lesions lesions

Figure 2: A negative location of omissions score (LO-S) DOI:10.1017/S0012162206000260


indicates that omissions are localized on left, and a
positive score on the right. A negative location of first three Accepted for publication 26th April 2005.
teddy bears crossed out score (START-S) indicates that first
Acknowledgements
three teddy bears cancelled are located on left, and a We are especially indebted to Professor Harvey Levin for his most
positive score on right. Children in right-sided lesions group valuable help. We thank the following therapists and students for
displayed a negative LO-S and a positive START-S. In left and participating in data collection: Adeline Bizouard, Charlotte
non-lateralized children with brain injuries and controls, Chambond, Carole David, Myriam Laurent-le Goff, Claire Léghu,
Clémence Mathat, Clarisse Meyer, and Emeraude Quevillon.
LO-S was positive and START-S was negative.

124 Developmental Medicine & Child Neurology 2006, 48: 120–125

QUELLI Renata bassani - bassaniqre@gmail.com - CPF: 012.477.481-46


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International Symposium
Status Epilepticus in Infants and Young Children
Basic Mechanisms, Clinical Evaluation, Prognosis and Treatment

29–30 April 2006 at the Senri Hankyu Hotel, Osaka, Japan

Notification and Call for Papers

Further information about the Infantile Seizure Society, Japan and the meeting can be obtained from ISS-9 Secretariat,
Toshisaburo Nagai MD, PhD Osaka University, Graduate School of Child and Reproductive Health,
1–7, Yamadaoka Suita, Osaka, Japan
Tel: +00 81 565 0871, Fax: +00 81 6 6879 2531, E-mail: nagai-t@sahs.med.osaka-u.ac.jp

The Teddy Bear Cancellation Test Anne Laurent-Vannier et al. 125

QUELLI Renata bassani - bassaniqre@gmail.com - CPF: 012.477.481-46

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