Keywords: Stroke - Child - Self-Care - Locomotion - Social Skills
Palavras-chave: Acidente Vascular Cerebral - Criança - Autocuidado - Locomoção - Habilidades Sociais
INTRODUCTION
Stroke, once considered a health problem in adults, is increasingly recognized as
an important morbidity and mortality factor in neonates and children[1 ]. The annual incidence of pediatric strokes (ischemic and hemorrhagic), considering
the neonatal period and childhood, varies from 3 to 25 per 100,000 children in developed
countries[1 ]. The incidence is higher in neonates: 1 in 4,000 live births[1 ]. While the predominant risk factors in adults include hypertension, diet, diabetes
mellitus, obesity, and smoking, among others[2 ], children have different and more varied risk factors. Risk factors for childhood
stroke (CS) include vasculopathies (such as sickle cell anemia, Moyamoya syndrome
and autoimmune disorders), prothrombotic conditions (such as polycythemia, antiphospholipid
antibody), heart disorders, genetic and metabolic disorders (such as homocystinuria,
Fabry disease), infections, vascular abnormalities, coagulation disorders and tumors[3 ].
Stroke may compromise children's functioning. According to the International Classification
of Functioning, Disability and Health (ICF), the concept of functioning includes all
body functions and those related to activity and participation[4 ]. After stroke, the following body functions may be compromised: mental function
(attention, information processing)[5 ], working memory, visuomotor processing speed[6 ], intellectual function[7 ], and neuromusculoskeletal/movement-related functions (such as muscle tone)[8 ]. Activities and participation functions that may be altered include personal care[9 ],[10 ], learning and knowledge application (school problems)[10 ]
-
[12 ], interpersonal relationships (behavioral)[11 ], and mobility[13 ]. After stroke, the child's functionality may be influenced by contextual factors
(personal and environmental) such as the child's age and age at stroke, parental education,
socioeconomic conditions, family support network, and rehabilitation[8 ].
Most previous studies have focused on limitations in body functions and structures
after a childhood stroke. Few studies have focused on activities and participation
functional outcomes and on the influence of the contextual factors on the child's
functioning[8 ]. The few available data (mentioned above) are from international studies[9 ]
-
[13 ], which may not reflect the reality of functional outcome after childhood stroke
in developing countries due to socioeconomic and cultural differences. To the best
of our knowledge, there are only four studies on functional outcomes after childhood
stroke in Brazil. They reported impairments in motor skills, writing, reading, memory[14 ],[15 ], and language[16 ]; one study on quality of life reported decreased functional capacity[17 ]. We found no Brazilian studies on functional outcomes in activities of daily living
(ADLs) and participation after childhood stroke. There is a need to know the functional
outcome of children after stroke to provide the most appropriate intervention focusing
on activity and participation skills rather than just improving impairments in body
structure/function levels. Thus, the objective of this study was to investigate the
functionality of children after a stroke in terms of social function, mobility, and
self-care skills.
METHODS
This was a retrospective longitudinal observational cohort study. We used the STROBE
checklist (https://www.strobe-statement.org ).
Participants
The inclusion criteria were: stroke diagnosis (ischemic and hemorrhagic) and age between
6 months and 7.5 years* (*age covered by the evaluation instrument used in the study
(PEDI) for the normative score). The exclusion criteria were: no signed informed consent,
presence of traumatic brain injury or diffuse brain injury, peri-intraventricular
hemorrhage, other causes of cerebral ischemia, associated pathologies with a significant
neuropsychomotor development delay such as Down syndrome, West syndrome, and others.
Instruments
Pediatric evaluation of disability inventory (PEDI)[18 ],[19 ]
The PEDI is administered as a structured interview with one of the child's parents/guardian
and informs about the children's profile in three functional domains: self-care, mobility,
and social function. The PEDI's functional profile consists of three parts; in this
study, we applied part I, referring to the child's functional skills. We used the
raw score to calculate the continuous score and normative score according to each
child's age. The normative score reflects a child's performance concerning a reference
sample; it must be between 30 and 70 to be considered age-appropriate. The item maps
show the functions of which the child is capable or incapable. The items are arranged
on the map in ascending level of difficulty, being the most complex closest to 100.
According to the child's raw score and age, the continuous score and standard deviation
are plotted on the map. The items to the left of this range are less complex, so we
expected the child to be able to perform them.
Brazil economic classification criterion[20 ]
The Brazil Economic Classification Criterion (BECC) is an economic segmentation instrument.
This Criterion differentiates the population in economic classification strata (A1,
A2, B1, B2, C1, C2, D, and E). The A1 stratum refers to the best financial condition
and the E stratum, the worst economic situation. The classification is based on the
family provider's educational level and household characteristics (presence and quantity
of some household comfort items).
Data collection procedures
The Research Ethics Committee of the Ribeirao Preto Medical School of the University
of São Paulo approved this study. All participants' parents/guardians were informed
about the study and provided a signed informed consent form.
We performed a review of medical data of all childhood stroke cases admitted to the
Clinical Hospital of Ribeirao Preto Medical School of the University of São Paulo
between 2005 and 2012. This is a tertiary-level university hospital. Then, we reviewed
the medical records of selected children to identify childhood strokes. We scheduled
the children's assessment for the exact date they would return for a clinical follow-up
appointment. Based on the family's preference, children that were not scheduled to
return by April 2013 were assessed at home.
We applied the PEDI's part 1 questionnaire in an in-person structured interview with
the children's parents/guardians.
Data analysis
We analyzed the correlation between the PEDI's normative scores in self-care, mobility
and social function domains with the following categorical variables: age at stroke
(≤1 /> 1 year), injury site (lobar/infratentorial/deep), presence of hydrocephalus
(yes/no), presence of intraventricular hemorrhage (yes/no), sex (female/male), stroke
type (ischemic/hemorrhagic), affected hemispheres (unilateral/bilateral), and socioeconomic
status (Brazil Economic Classification Criterion) using the Mann-Whitney non-parametric
test. We also correlated such categorical variables with the child's current age and
hospital stay (numerical variables) using the Spearman correlation coefficient.
RESULTS
[Figure 1 ] describes the participants’ screening and selection process.
The mean age at stroke was 1.5 ± 1.4 years (range: 2 days to 4.4 years). The average
age at assessment was 3.6 ± 1.4 years (range: 2.2 to 6.3 years). [Table 1 ] describes the participants’ characteristics.
Figure 1 Flowchart for the selection of childhood stroke participants.CRA: cardiorespiratory
arrest; NPMDD: neuropsychomotor development delay.
Table 1
Participants’ characteristics (n=14).
Patients characteristics
Number of patients (n)
Age at stroke
< 1 year
6
> 1 year
8
Sex
Female
8
Male
6
Lesion location
Deep
5
Lobar/Infratentorial
9
Stroke Type
Ischemic
8
Hemorrhagic
6
Side
Unilateral
10
Bilateral
4
Intraventricular Hemorrhage
No
12
Yes
2
Hydrocephalus
No
12
Yes
2
Socioeconomic status
B1
1
B2
1
C
12
School
Yes
9
No
5
Brothers/sisters
0
4
1
8
2
2
We applied the PEDI after an average interval of 2.5 ± 1.3 years post-stroke (range:
1 to 5.5 years). Of 14 children, 7 had another comorbidity in addition to the underlying
disease: 6 (42.9%) had epilepsy and 1 (7.1%) had strabismus. Only 4 (28.6%) children
underwent physical therapy rehabilitation (one of them had only 10 sessions before
discharge). Of these, 2 (14.3%) also received occupational therapy and 1 (7.1%) received
speech therapy. At the time of assessment, no child was receiving any type of rehabilitation
intervention.
The average normative score for PEDI's functional skills in the self-care domain was
37.6 ± 15.4; in the mobility domain, it was 36.2 ± 15.4, and in the social function
domain, it was 48.7 ± 11.1. Most children scored between 30 and 70 on the normative
score profile. Only 4 (28.6%) children did not perform adequately in the self-care
domain, 4 (28.6%) in mobility, and only 1 (7.1%) in social function. Among children
with age-appropriate functional outcome, the average of normative scores for PEDI's
functional skills in self-care, mobility and social function were, respectively, 46
± 6.8, 43.7± 9.5, and 50.7 ± 8.7. [Table 2 ] presents the children's normative score in self-care, mobility and social function
skills.
Table 2
Participants’ characteristics and normative scores in the three PEDI functional domains.
P (n=14)
Age at stroke
Age at assessment (years)
Stroke type
Lesion location
SCFS score
MOFS score
SFFS score
P1
2 d
5
H
Lobar
42.2
29.3*
54.3
P2
1.4 m
2
H
Deep
42.4
39.5
55.6
P3
2.0 m
2
I
Lobar
34.6
41
63.3
P4
4.9 m
4
I
Deep/Infratentorial
21.2*
31
46.6
P5
6.8 m
2
I
Lobar
41.6
36.4
53.1
P6
11.2 m
3
I
Lobar
44.9
43.8
45.2
P7
12.9 m
2
H
Lobar
59.1
57.1
43.1
P8
13.2 m
5
I
Deep
23.3*
<10*
67.3
P9
18.6 m
3
I
Deep
47.3
39.4
45.2
P10
21.1 m
3
I
Lobar/Deep/Infratent.
12.1*
<10*
23.3*
P11
24.3 m
3
I
Infratentorial
46.8
36.2
42.5
P12
38.8 m
6
H
Infratentorial
54.2
56.3
58.3
P13
46.9 m
6
H
Lobar
47.2
56.2
45.3
P14
52.8 m
5
H
Lobar
<10*
22.6*
38.9
P: participant; SCFS: Self-Care Functional Skills; MOFS: Mobility Functional Skills;
SFFS: Social Function Functional Skills; I: Ischemic; H: Hemorrhagic; d: days; m:
months; *score below that expected for the age (between 30-70).
The self-care functional skills item maps of child P4 ([Figure 2 ]) showed that she performed below average compared to the normative sample on tasks
related to personal hygiene (3 of 20 items), bathing (1 of 5 items) and dressing (3
of 21 items), especially on bimanual tasks or tasks that required movements of the
upper limbs up to shoulder level. Similarly, the item map of child P8 showed inadequate
performance in feeding (2 of 15 items) and dressing (7 of 21), especially bimanual
task items ([Figure 3 ]). Child P10’s item map ([Figure 4 ]) showed an age-inappropriate performance on personal hygiene (3 items out of 20),
dressing (4 of 21 items), and toiletries (9 of 15 items). This child's tasks limitations
were related to the neuromotor and cognitive demands of the task's items. Child P14
showed inadequate performance on some feeding (2 items out of 15), personal hygiene
(2 of 20 items), and toiletries items (3 of 15 items) and on most bathing (4 of 5
items) and dressing tasks (9 of 21 items), mainly related to routine care with the
hemodialysis catheter ([Figure 5 ]).
Figure 2 PEDI Item Maps in Self-Care Functional Skills of child P4.⃝ >90% of the children
in the age group can do the task; ◌ >75% of the children in the s age group already
can do the task; CS: Continue Score; PEDI: Pediatric Evaluation of Disability Inventory.
Figure 3 PEDI Items Map in Self-Care Functional Skills of the child P8.⃝ >90% of the children
in the age group can do the task; ◌ >75% of the children in the age group can do the
task; CS: Continue Score; PEDI: Pediatric Evaluation of Disability Inventory.
Figure 4 PEDI Items Map in Self-Care Functional Skills of the child P10.⃝ >90% of the children
in the age group can do the task; ◌ >75% of the children in the age group can do the
task; CS: Continue Score; PEDI: Pediatric Evaluation of Disability Inventory.
Figure 5 PEDI Items Map in Self-Care Functional Skills of the child P14.⃝ >90% of the children
in the age group can do the task; ◌ >75% of the children in the age group can do the
task; CS: Continue Score; PEDI: Pediatric Evaluation of Disability Inventory.
In the mobility domain, child P8 only performed inadequately in bus transfers (2 of
5 items), shower transfers (1 of 5 items), indoor locomotion (1 of 13 items), outdoor
locomotion (1 of 12 items) and stair climbing (2 of 10 items). Child P10 showed inadequate
performance in all mobility sets: transfers in bathroom/ chair (5 of 10 items), in
car (1 of 5 item), in shower (4 of 5 items), in bed (1 of 5 item), indoor locomotion
(4 of 13 items), outdoor locomotion (3 of 12 items) and stair climbing (6 of 10 items).
In the social function domain, this child had limitations in the following items:
functional communication use (1 of 5 items), expressive communication complexity (2
of 5 items), interactive social games playing with adults (2 of 5 items), playing
with objects (4 of 5 items), self-information (2 of 10 items), housework (1 of 5 items),
self-protection (2 of 5 items), and community function (1 of 5 items).
There was no correlation between scores in self-care and mobility domains with any
of the analyzed independent variables ([Table 3 ]). The social function domain score was the only one that showed a significant correlation:
the score was higher (better) for children who had a unilateral injury (p = 0.05).
Table 3
PEDI functional domains scores related to patients’ characteristics (categorical)*.
Patients characteristics (n=14)
SCFS score
P-value
MOFS score
P-value
SFFS score
P-value
Age at stroke
< 1 year
37.8 ± 8.9
0.37
36.8 ± 5.7
0.90
53 ± 3.6
0.14
> 1 year
37.4 ± 19.5
35.9 ± 20.2
45.5 ± 13
Sex
Feminine
43.1 ± 11.7
0.37
41.4 ± 10.6
0.20
50.8 ± 7.6
0.56
Male
30.3 ± 17.5
29.5 ± 18.7
45.9 ± 14.9
Injury site
Deep
29.3 ± 14.9
0.26
25.8 ± 15.3
0.10
47.6 ± 16.2
0.79
Lobar/Infratentorial
42.2 ± 14.2
42.1 ± 12.4
49.3 ± 8.2
Stroke type
Ischemic
34 ± 13.5
0.24
30.9 ± 13.7
0.20
48.3 ± 13.6
0.79
Hemorrhagic
42.4 ± 17.5
43.5 ± 15.3
49.3 ± 7.9
Affected side
Unilateral
36.4 ± 13.3
0.37
33.6 ± 14.7
0.48
51.2 ± 12.3
0.05**
Bilateral
40.6 ± 21.5
43 ± 16.7
42.4 ± 2.7
Intraventricular hemorrhage
No
39.5 ± 14.1
0.27
37.1 ± 16
0.58
49 ± 11.5
0.72
Yes
26 ± 23.3
31.1 ± 12
47.2 ± 11.8
Hydrocephalus
No
39.5 ± 14.1
0.27
37.1 ± 16
0.58
49 ± 11.5
0.72
Yes
26 ± 23.3
31.1 ± 12
47.2 ± 11.8
Socioeconomic status
B
22 ± 17.8
0.10
31.8 ± 13
0.72
51.1 ± 17.2
1.00
C
40.2 ± 14
37 ± 16
48.3 ± 10.8
SCFS: Self-Care Functional Skills; MOFS: Mobility Functional Skills; SFFS: Social
Function Functional Skills; I: Ischemic; H: Hemorrhagic; *Mann-Whitney non-parametric
test; **Statistically significant.
When analyzing the PEDI's domain scores concerning hospital stay and current age,
the social function domain score showed a strong negative correlation with hospital
stay (r = -0.79; p = 0.001), as shown in [Table 4 ].
Table 4
PEDI functional domain scores related to patients’ characteristics*.
Patients characteristics
SCFS
p-value
MOFS
p-value
SFFS
p-value
Age at assessment (years)
-0.34
0.91
-0.18
0.54
0.08
0.8
Hospital stay (days)
-0.12
0.7
-0.84
0.78
-0.79**
0.001**
SCFS: Self-Care Functional Skills; MOFS: Mobility Functional Skills; SFFS: Social
Function Functional Skills; I: Ischemic; H: Hemorrhagic; *:Spearman's correlation
coefficient; **: Statistically significant.
DISCUSSION
We analyzed the functional outcome of 14 children diagnosed with stroke in early childhood.
Overall, the children showed age-appropriate functional outcomes measured by the PEDI's
functional domains: over 70% of them in self-care and mobility and 90% in social function.
Children with bilateral injuries and longer hospital stays showed the worst scores
in PEDI's social function domains.
Of the 4 children with age-inappropriate self-care performance (P4, P8, P10, P14),
two (P4, P8) had typical hemiparetic sequelae limitations. Child P10 showed limitations
related to neuromotor and cognitive demands on self-care tasks; this is the only child
with age-inappropriate social function. The child had multiple lacunar infarctions
and microangiopathy due to hemolytic-uremic syndrome (HUS) during hospital stay. Previous
case reports of post-HUS children aged 15 and 21 months (the same age as the child
in our study) also described neuromotor and language impairments[21 ]. On the other hand, child P14 had no evident motor deficit; most of its limitations
in self-care were related to routine care of the hemodialysis catheter due to chronic
kidney disease.
Among the children with age-inappropriate mobility (P1, P8, P10, P14), children P8
and P10 had neuromotor limitations to a lesser or greater degree. However, the low
scores of children P1 and P14 may be due to a limitation on the normative scale. At
the time of data collection, both children were between 5 years and 5 years and 5
months old. Within this age range, raw scores of P1 and P14 reflect an age-inappropriate
performance when compared to normative scores (below 30). However, similar scores
in the following age range (5 years and 6 months to 5 years and 11 months) reflected
an age-appropriate performance, with normative scores greater than 30. Considering
that certain scores are considered age-inappropriate in a certain age range, but identical
scores are considered age-appropriate in an older age range, it is possible that the
normative scores are a limitation and may require further investigation.
To the best of our knowledge, only Galvin et al.[9 ] used the PEDI to assess functional outcomes after childhood stroke. However, the
authors only presented each domain's average score (not the children's frequency of
appropriate outcomes), precluding the comparison with our results. The children in
our study presented age-appropriate average scores in self-care, mobility, and social
function domains, although scores were close to the lower limit of normality. This
is in accordance with previous childhood stroke studies showing good mobility, even
with hemiparesis and requiring orthoses[13 ],[22 ]. Cooper et al.[23 ] found good motor recovery (fine and gross motor function) in children (0-19 years)
over the first year after stroke, with more pronounced improvement in preschool-age
children[23 ].
Conversely, Galvin et al.[9 ] observed that children with ischemic stroke showed lower levels of functional skills
in all domains: self-care (70.36 ± 30.82), mobility (77.97 ± 27.58) and social function
(74.88 ± 30.57). Previous studies have demonstrated that children with stroke showed
unsatisfactory performance for ADLs, communication, and social function activities[12 ],[22 ], especially in early-age stroke children[22 ], which does not corroborate with our results. However, the age range of our sample
may explain such discrepancy. Specifically, the studies mentioned above involved children
up to 16 [9 ] and 18 years of age[12 ],[22 ], while our study included children up to 7.5 years of age. In this age range, deficits
in complex communication, ADLs, and social skills may not be as obvious. Also, the
development of each of these skills influences that of the other; Cooper et al.[23 ] described that communication skills may influence ADL throughout children's development[23 ].
Similarly, studies suggest that children present reduced communication skills, as
well as the cognition-related and social functions after stroke. Friefeld et al.[24 ] observed that the quality of life (QoL) related to physical aspects and the domestic
environment was less impaired and the QoL related to school and playing were more
affected, mainly due to cognitive and behavioral elements[24 ]. Based on the literature, about half of the children with childhood stroke present
limitations on school activities and participation and require specialized education[12 ],[22 ],[25 ],[26 ]. Additionally, children present significant impairment on cognition-related functions,
intelligence, memory, language, and social function[6 ],[26 ],[27 ]. Studies have also shown that cognitive social and task performances were worse
in children who had stroke at a younger age[6 ],[26 ],[28 ].
The significant negative correlation between length hospital stay and social function
may be reflecting the impact of the chronic underlying condition on socialization.
Of the four children with longer hospital stays, only one had evident neuromotor sequelae
(P10). However, all of them had a systemic condition (chronic liver or renal disease/
vasculopathy with toes amputation) with potential clinical complications, which could
affect the dynamics of family functioning related to child care. Supporting this speculation,
Christerson and Strömberg[12 ] reported that post-stroke children's outcomes were more dependent on etiology and
recurrences (rebleeding, metabolic diseases, Moya-Moya syndrome) than the age at stroke
or injury site. A weak social competence may not be due solely to brain injuries but
to the child's experience with the particularities of the illness in their social
world[29 ].
The relationship between worse scores in social function and bilateral injury may
be related to the children's interhemispheric neuroplasticity process. Mosch et al.[30 ] observed that, differently from adults, children with right cerebral hemisphere
(RCH) injury did not present reduced social function, suggesting a positive plasticity
process in children. However, children with left cerebral hemisphere (LCH) injury
presented worse social function (and better language function) than adults with an
LCH injury. Authors speculate that after LCH injury in children, the plasticity process
may involve recruiting RCH contralateral areas previously intended for social function
to preserve LCH functions, such as language[30 ]. In our study, social function skills did not correlate with LCH injury. This may
be due to the younger age of our sample. The complexity of preschool social demands
is low and usually related to lower-order skills, which can be attributed to less
complex neural networks and often have good functional recovery[31 ]
-
[33 ]. The more complex skills that are usually impaired after childhood stroke (executive,
cognitive, social skills) are needed as children grow up and move into more socially
complex environments like school, college, and work[6 ],[22 ],[24 ],[26 ],[34 ].
The age-appropriate functional outcomes in childhood after stroke found in our study
should be interpreted with caution and considered especially from a functional perspective.
The finding shows that preschool children can functionally keep up with their peers
despite stroke. The PEDI score is influenced by the ICF model, in which the functionality
in a specific domain results from the interaction between health condition and the
contextual factors (environmental and personal)[4 ]. Functional performance in a given task is influenced not only by the child's characteristics
but also by the task's specific demands and the environmental aspects with which the
child interacts[35 ]. According to the ICF, effective rehabilitation requires going beyond pathological
conditions/sequels and promoting the individual's activity and participation[36 ].
One limitation of our study is the small number of participants. On the other hand,
this allowed rich inferences from the occasional analysis of isolated cases. As an
implication for research, our study reinforces the importance of the interhemispheric
neuroplasticity process in children and the impact of the chronic nature of the underlying
condition/stroke on social functions. Moreover, it has implications for clinical practice
by supporting recovery based on activity/participation levels and increase surveillance
of children with stroke, mainly related to social function, even when there are no
obvious deficits at discharge.
In summary, preschool children showed age-appropriate functional outcomes on self-care,
mobility, and social function domains after stroke. However, children with bilateral
injuries and longer hospital stays had the worst scores in social function domains.
We recommend focusing on functional rehabilitation to promote activities and participation
and to monitor the development of the children's social skills after stroke.
