Document Type : Original Article
Author
Abstract
Keywords
Developmental Outcomes and Risk Factors in Traumatic Brain Injury Among Infants and Young Children: A Comparative Study of ASQ-3 and Bayley-III"
Batoul M. Abdel Raouf 1, Shaymaa A. Deif-Allah1, Walid A. Abdel Ghany2
Esmail K. Abdelaziz 1, Hani A. Elmikaty3, Marwa Salah1
1Pediatric, and neurosurgery2 Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt
3Pediatric Department, National Research Center
Corresponding Author:Marwa Salah
Mobile: 01014413948 Emails: elsherifmarwa@ymail.com
Abstract
Background: Children's traumatic brain injury (TBI) is a serious worldwide health issue. Among people who are not elderly, children ages 0–4 have the highest rate of TBI. These children have chronic neurological conditions that drastically affect their everyday lives and general well-being.
Aim of the study: to identify factors that affect developmental outcomes after TBI and to compare two tools used for assessing these outcomes: the Ages and Stages Questionnaire (ASQ-3) and the Bayley Scales of Infant and Toddler Development, Third Edition (Bayley-III).
Subjects and methods: A comparative descriptive study was carried out on 85 children and infants who had traumatic brain injury and are recruited from Emergency room, Intensive care units and general clinic of the Children’s Hospital and Surgery Hospital, Ain Shams University, Cairo, Egypt. The study spanned six months, from August 2021 to January 2022, with the sample selected through randomization. The Age and Stage Questionnaire 3rd edition (ASQ-3) was used to measure developmental outcomes twice: once upon hospital discharge and again three months later. Additionally, the second visit was the only time the Bayley scales of infants and toddlers' development III were evaluated. Results were compared and associated between follow-up and discharge.
Results: Better developmental outcomes were indicated by the statistically significant difference between the ASQ-3 at discharge and follow-up, which was greater at follow-up than at discharge (P<0.001 for all elements). At follow-up, a comparison of the Bayley Scale and ASQ-3 revealed no statistically significant difference. This indicates that both tests were similar.
Conclusions: Following TBI, the majority of children continued on their normal developmental path. Prior to referral to the third edition of the Bayley scales of infants' and toddlers' development, Following traumatic brain damage, children can be screened using the ASQ-3. Convulsions, aberrant head CT results, lower GCS, the need for neurosurgical intervention, and hospitalisation were among the factors that negatively impacted development after traumatic brain injury.
Keywords: Traumatic Brain damage, Ages and Stages Questionnaire 3rd Edition.
Introduction:
Traumatic brain injury (TBI) in children is a major global health concern. Incidences of paediatric TBI range from 47 to 280 per 100,000 children, with significant country-to-country variation (1). Among the non-elderly, children ages 0 to 4 have the highest prevalence of TBI, accounting for almost 300,000 Emergency Department visits, 9,250 hospitalisations, and 760 fatalities every year (2).
As the baby brain is going through a period of fast development, it may be especially vulnerable to injury, making infants and toddlers especially susceptible to the effects of traumatic brain injury. The primary white matter connections are established in term infants at birth, but as they grow into toddlers, the baby brain is actively going through a period of intense fibre myelination, synapse creation (3).
White matter myelination and refinement are associated with improvements in motor, cognitive, and socioemotional functioning. The timing of the injury during a time of fast brain and behavioural development may contribute to the poor outcomes of TBI in early childhood. To raise awareness about appropriate referrals for school-based services and rehabilitation, it is essential to identify times when people are most vulnerable to the effects of traumatic brain injury (4). Few studies have evaluated risks and monitored developmental trajectories, despite the high prevalence of TBI in newborns and toddlers. Despite these drawbacks, research indicates that, in comparison to children who are usually developing, infants and preschoolers with moderate-to-severe TBI exhibit long-term deficits in intellectual, academic, adaptive behaviour, social, and certain attentional domains (5). The social context, which includes family dynamics, socioeconomic standing, and Positive home environments are linked to better recovery outcomes for older children, and to influence these outcomes (6).
Aim of the study: to compare the Ages and Stages Questionnaire (ASQ-3) and the Bayley Scales of Infant and Toddler Development, Third Edition (Bayley-III), two instruments used to evaluate developmental outcomes following traumatic brain injury (TBI), and to determine the factors that influence these outcomes.
Ethical consideration:
Sample size: the sample size was calculated using the PASS 11 programme, establishing power at 95%, alpha error at 5%, and examining the findings of prior research of (Keenan et al., (2019). (7)
Inclusion Criteria: Infants and children with traumatic brain injury who were previously developmentally normal and between the ages of 0 and 42 months of both sex will be the subjects to the study.
Exclusion criteria: Children and infants whose parents had any concerns regarding their development prior to the head injury.
Study procedures
This comparative prospective study included 85 children and infants after TBI recruited from Emergency room, Intensive care units and general clinic of the Children’s Hospital and Surgery Hospital, Ain Shams University, Cairo, Egypt, The study spanned six months, from August 2021 to January 2022, with the sample selected through randomization.
All the studied cases were subjected to:
1) Full history taking: including
Whether surgical intervention was required during hospital admission.
2) Clinical assessment comprising:
- General assessment (vital signs, anthropometric measurement)
- Pediatric Glasgow Coma scale
- Systemic examination:
Cardiovascular
Chest
Abdominal examination.
Complete neurological examination
3) CT scan of brain.
4) Outcome measures
Results
Table (1): Demographic data of the studied cases
Gender |
Male Female |
54 (63.5%) 31(36.5%) |
Age (ms.) |
Median (IQR) Range |
24(12-34) 1-39 |
Table (1) shows there were more boys (63.5%) than girls (36.5%) in the study. The average age was 24 months, with most children between 12 and 34 months old.
Table (2): Clinical and Radiological Findings post Head Trauma
|
No.= 85 |
|
GCS |
Mean±SD |
13.13 ± 1.94 |
Range |
7 – 15 |
|
Convulsion |
Positive |
14 (16.5%) |
|
|
|
Hospital admission |
Positive |
55 (64.7%) |
CT brain finding |
Free |
30 (35.3%) |
Positive |
55 (64.7%) |
|
Brain edema |
11 (12.9%) |
|
Skull fracture |
7 (8.2%) |
|
Intraparenchymal injury |
3 (3.5%) |
|
Extra parenchymal injury |
15 (17.6%) |
|
Skull fracture +Intra parenchymal injury |
2 (2.4%) |
|
Skull fracture +Extra parenchymal injury |
15 (17.6%) |
|
Intra parenchymal injury +Extra parenchymal injury |
2 (2.4%) |
|
Surgery |
Positive |
15 (17.6%) |
Significant if the P-value is less than 0.05, non-significant if it is greater than 0.05, and highly significant if it is less than 0.01: paired t-test
Table (2): This table shows that the most prevalent CT brain finding was extra parenchymal injury, (17.6%) of cases. Regarding hospital admission, 64.7% of cases required inpatient care,. Convulsions were reported in 16.5% of cases., surgical intervention was necessary in 17.6% of cases
Table (3) Comparison between hospital admitted and non admitted patients regarding clinical and CT finding.
|
Hospital admission |
Test |
P- value |
Sig. |
||
Negative |
Positive |
|||||
No.= 30 |
No.= 55 |
|||||
GCS |
Mean±SD |
14.73 ± 0.64 |
12.25 ± 1.86 |
7.066• |
0.000 |
HS |
Range |
13 – 15 |
7 – 15 |
||||
CT |
Free |
27 (90.0%) |
3 (5.5%) |
60.757 |
0.000 |
HS |
Positive |
3 (10.0%) |
52 (94.5%) |
||||
Brain edema |
3 (10.0%) |
8 (14.5%) |
0.356 |
0.551 |
NS |
|
Skull fracture |
0 (0.0%) |
7 (12.7%) |
4.161 |
0.041 |
S |
|
Extra parenchymal injury |
0 (0.0%) |
15 (27.3%) |
9.935 |
0.002 |
HS |
|
Intra parenchymal injury |
0 (0.0%) |
3 (5.5%) |
1.696 |
0.193 |
NS |
|
Skull fracture+ |
0 (0.0%) |
15 (27.3%) |
9.935 |
0.002 |
HS |
|
Intra parenchymal injury+ |
0 (0.0%) |
2 (3.6%) |
1.117 |
0.291 |
NS |
|
Skull fracture+ |
0 (0.0%) |
2 (3.6%) |
1.117 |
0.291 |
NS |
|
Convulsion |
|
|
|
9.142* |
0.002 |
HS |
Positive |
0 (0.0%) |
14 (25.5%) |
||||
Surgery |
|
|
|
9.935* |
0.002 |
HS |
Positive |
0 (0.0%) |
15 (27.3%) |
P-value > 0.05: Non significant; P-value < 0.05: Significant; P-value < 0.01: Highly significant
*: Chi-square test; •: Independent t-test; ≠: Mann-Whitney test
Table (3) Shows Hospital-admitted patients had significantly lower GCS scores and a higher prevalence of abnormal CT findings, particularly extra parenchymal injuries and combined skull fractures with extra parenchymal injuries were observed exclusively in admitted patients,
Table (4): Comparison between ASQ-3 at discharge and follow up
ASQ |
At discharge |
At follow-up |
Test value |
P-value |
Sig. |
|
Communication score |
Mean±SD |
38.88 ± 10.22 |
43.65 ± 8.03 |
-4.698• |
<0.001 |
HS |
Range |
10 – 60 |
10 – 60 |
||||
Gross motor score |
Mean±SD |
38.35 ± 12.78 |
45.47 ± 9.53 |
-5.604• |
<0.001 |
HS |
Range |
0 – 60 |
0 – 60 |
||||
Fine motor score |
Mean±SD |
38.00 ± 11.42 |
44.76 ± 8.16 |
-4.842• |
<0.001 |
HS |
Range |
0 – 60 |
10 – 60 |
||||
Problem solving score |
Mean±SD |
41.82 ± 12.17 |
48.82 ± 9.47 |
-5.637• |
<0.001 |
HS |
Range |
0 – 60 |
5 – 60 |
||||
Personal social score |
Mean±SD |
43.12 ± 13.02 |
51.53 ± 10.72 |
-7.750• |
<0.001 |
HS |
Range |
0 – 60 |
10 – 60 |
P-value > 0.05: Non significant; P-value < 0.05: Significant; P-value < 0.01: Highly significant: Paired t-test.
60 |
48.82 |
51.53 |
50 |
43.65 |
45.47 |
44.76 |
41.82 |
43.12 |
38.88 |
38.35 |
40 |
38 |
30
20
10
0 |
Communication |
Gross |
Fine |
Problem solving Personal social |
At discharge At follow -up |
Figure 1: Comparison between ASQ at discharge and follow up
Table (4) and figure (1) shows that there is highly significant improvement in development at follow up regarding ASQ3 scale.
Table (5): Comparison between ASQ-3 and Bayley Scale at follow up:
|
ASQ-3 follow up |
Bayley Scales |
Test Value |
P- value |
Kappa agreement (95% CI) |
||
|
Problem solving |
Cognitive |
0.4 |
0.819 |
0.527 (0.218 - 0.837) |
||
No. = 85 |
No. = 85 |
||||||
Average |
76 |
89.40% |
76 |
89.40% |
|||
Monitor |
7 |
8.20% |
8 |
9.40% |
|||
Assess |
2 |
2.40% |
1 |
1.20% |
|||
|
Motor |
Motor |
1.770 |
0.413 |
0.285 (0.001 - 0.569) |
||
No. = 85 |
No. = 85 |
||||||
Average |
70 |
82.4% |
76 |
89.40% |
|||
Monitor |
13 |
15.3% |
8 |
9.40% |
|||
Assess |
2 |
2.4% |
1 |
1.20% |
|||
|
Communication |
Language |
1.286 |
0.526 |
0.501 (0.235 - 0.766) |
||
No. = 85 |
No. = 85 |
||||||
Average |
76 |
89.40% |
76 |
89.40% |
|||
Monitor |
6 |
7.10% |
8 |
9.40% |
|||
Assess |
3 |
3.50% |
1 |
1.20% |
Table (5) shows that there was insignificant difference between ASQ3 on follow up and Bayely scale regarding problem solving, motor and communication of ASQ3 and its corresponding cognitive, motor and language of Bayely scale respectively in studied cases.
Table (6): Correlation between ASQ-3 follow up scores and its counterpart Bayley Scales:
ASQ-3 Scores |
Bayely scales |
R |
p-value |
Problem solving |
Cognitive scale |
0.259 |
0.017 |
Motor score |
Motor scale |
0.224 |
0.039 |
Communication score |
Language scale |
0.261 |
0.016 |
This table shows that there was positive correlation between ASQ-3 and its counterpart Bayley Scale.
Table (7) comparison regarding Bayley scale at follow-up between negative and positive hospital admission.
Bayley Scale |
Hospital admission |
Test value |
P- value |
Sig. |
||
Negative |
Positive |
|||||
No.= 30 |
No.= 55 |
|||||
Cognitive |
Mean±SD |
94.83 ± 4.04 |
90.45 ± 8.24 |
2.732 |
0.008 |
HS |
Range |
90 – 105 |
55 – 105 |
||||
Language |
Mean±SD |
92.67 ± 4.47 |
90.78 ± 8.53 |
1.126 |
0.263 |
NS |
Range |
79 – 103 |
56 – 112 |
||||
Motor |
Mean±SD |
93.10 ± 3.62 |
88.69 ± 8.83 |
2.612• |
0.011 |
S |
Range |
82 – 103 |
46 – 112 |
P-value > 0.05: Non significant; P-value < 0.05: Significant; P-value < 0.01: Highly significant
Table (7) Regarding cognitive and motor scales, there was significant difference between hospital admitted cases than non-admitted but regarding language scale, there was non-significant difference.
Discussion
In our study, we used the ASQ-3 (Ages and Stages Questionnaires, Third Edition) to assess children's development at hospital discharge and again three months later. We found a significant improvement in ASQ-3 scores at follow-up, suggesting better developmental progress over time.
The original ASQ-3 study, which included over 15,000 North American children, showed that the tool is highly accurate. It has strong specificity and negative predictive value (NPV), meaning that a normal result reliably indicates typical development and reduces the chance of missing children with actual developmental delays(10).
A national study in Canada also supported the ASQ-3's ability to identify children who are not at risk of neurodevelopmental disorders(11). Similarly, other research has shown that the ASQ-3 is useful for screening both children who may need further evaluation and those who are developing normally. This makes it a valuable tool for early developmental assessment (12).
At the three-month follow-up, we also used the Bayley Scales of Infant and Toddler Development, Third Edition (Bayley-III), to assess development and compare its results with the ASQ-3. We found a positive correlation between ASQ-3 domains (problem-solving, language, and motor) and the corresponding Bayley-III scales (cognitive, language, and motor). There were no significant differences between the two tools, supporting the ASQ-3 as a useful screening tool before a more detailed Bayley-III assessment.
The ASQ-3 is recommended by NICE guidelines for identifying children at risk of developmental delay before referring them for a Bayley evaluation (13). Screening tools like the ASQ-3 are preferred in many settings because they take less time to administer compared to Bayley-III, as noted by Del Rosario et al. (14) Bayley-III is the gold standard for assessing children aged 1 to 42 months, covering cognitive, language, motor, social-emotional, and adaptive behaviour skills.
Other study found moderate to strong correlations between ASQ-3 communication and Bayley-III language scores, as well as between ASQ-3 personal-social and Bayley-III social-emotional scores. ASQ-3 gross motor and Bayley-III gross motor scores also showed a moderate correlation, while ASQ-3 fine motor and Bayley-III fine motor scores had a weaker correlation. Additionally, the ASQ-3 problem-solving domain had a low correlation with the Bayley-III cognitive scale (12).
Our study found that certain factors negatively affected development after traumatic brain injury. Children who were hospitalized, had lower Glasgow Coma Scale (GCS) scores, experienced convulsions, had abnormal head CT scans, or required neurosurgery were at higher risk for delayed development.
A study of 1,438 children with TBI reported that 258 (17.9%) had a GCS of 13 or lower. It also found that 30.3% had abnormal CT scans, and 15.4% experienced serious outcomes such as death, intubation, or neurosurgery (15). Another study on the same group showed that 7.5% of children under 2 years and 8.2% of those over 2 years required neurosurgery, with significantly lower GCS scores than those who did not need surgery (16).
Conclusion:
Before being referred to the Bayley scale, infants and children who have experienced traumatic brain injury can be screened using the ASQ-3. Most newborns and toddlers with TBI showed improvements in developmental milestones at follow-up.
Factors that negatively impacts on development after TBI were need for hospital admission, lower GCS, convulsion, abnormal head CT finding and need for neurosurgical intervention.
Recommendations
Before referring children and infants with traumatic brain injury to the third edition of the Bayley Scales of Infant and Toddler Development, we advise using the ASQ-3 as a screening tool. Also recommend to follow up infants and children with TBI especially those with risk factors (hospital admission, low Gcs, CT brain finding) as they at risk for developmental delay.
Limitations:
Relatively small sample size
The study was conducted at a single center, which may limit generalizability.
Reference
1 Dewan, M.C., Mummareddy, N., Wellons, J.C. and Bonfield, C.M., 2016. The epidemiology of global pediatric traumatic brain injury: a qualitative review. World Neurosurgery, 91, pp.497-509.
2 Taylor, C.A., Bell, J.M., Breiding, M.J. and Xu, L., 2017. Traumatic brain injury-related emergency department visits, hospitalizations, and deaths—United States, 2007 and 2013. Morbidity and Mortality Weekly Report, 66, pp.1–16.
3 Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P.S. and Hertz-Pannier, L., 2014. The early development of brain white matter: a review of imaging studies in fetuses, newborns, and infants. Neuroscience, 276, pp.48-71.
4 Rogers, C.E., Smyser, T., Smyser, C.D., Shimony, J., Inder, T.E. and Neil, J.J., 2016. Regional white matter development in very preterm infants: perinatal predictors and early developmental outcomes. Pediatric Research, 79, pp.87-95.
5 Cheong, J.L., Doyle, L.W., Burnett, A.C., Lee, K.J., Walsh, J.M., Potter, C.R., Treyvaud, K., Thompson, D.K., Olsen, J.E., Anderson, P.J. and Spittle, A.J., 2017. Association between moderate and late preterm birth and neurodevelopment and social-emotional development at age 2 years. JAMA Pediatrics, 171(2), p.e164805.
6 Wade, S.L., Zhang, N., Yeates, K.O., Stancin, T. and Taylor, H.G., 2016. Social environmental moderators of long-term functional outcomes of early childhood brain injury. JAMA Pediatrics, 170(4), pp.343-349.
7 Keenan, H.T., Presson, A.P., Clark, A.E., Cox, C.S. and Ewing-Cobbs, L., 2019. Longitudinal developmental outcomes after traumatic brain injury in young children: Are infants more vulnerable than toddlers? Journal of Neurotrauma, 36(2), pp.282-292.
8 Squires, J. and Bricker, D., 2009. Ages & Stages Questionnaires®, Third Edition (ASQ-3™): A parent-completed child-monitoring system. Baltimore: Paul H. Brookes Publishing Co.
9 Johnson, S., Moore, T. and Marlow, N., 2014. Using the Bayley-III to assess neurodevelopmental delay: Which cut-off should be used? Pediatric Research, 75(5), pp.670-674.
10 Meisels, S.J. and Atkins-Burnett, S., 2005. Developmental screening in early childhood: A guide. 5th ed. Washington, DC: National Association for the Education of Young Children.
11 Lamsal, R., Dutton, D.J. and Zwicker, J.D., 2018. Using the Ages and Stages Questionnaire in the general population as a measure for identifying children not at risk of a neurodevelopmental disorder. BMC Pediatrics, 18(1), p.122.
12 Agarwal, P.K., Xie, H., Sathyapalan Rema, A.S., Meaney, M.J., Godfrey, K.M., Rajadurai, V.S. and Daniel, L.M., 2024. Concurrent validity of the Ages and Stages Questionnaires with Bayley Scales of Infant Development-III at 2 years: A Singapore cohort study. Pediatric and Neonatology, 65, pp.48-54.
13 National Institute for Health and Care Excellence (NICE), 2017. Developmental follow-up of children and young people born preterm (NG72). London: NICE.
14 Del Rosario, C., Slevin, M., Molloy, E.J., Quigley, J. and Nixon, E., 2021. How to use the Bayley scales of infant and toddler development? Archives of Disease in Childhood - Education and Practice, 106(2), pp.108-112.
15 Hwang, S.Y., Ong, J.W., Ng, Z.M., Foo, C.Y., Chua, S.Z., Sri, D. and Chong, S.L., 2019. Long-term outcomes in children with moderate to severe traumatic brain injury: A single-centre retrospective study. Brain Injury, 33(11), pp.1420-1424.
16 Chong, S.L., Khan, U.R., Santhanam, I., Seo, J.S., Wang, Q., Jamaluddin, S.F. and Ong, M.E.H., 2017. A retrospective review of paediatric head injuries in Asia–A Pan Asian Trauma Outcomes Study (PATOS) collaboration. BMJ Open, 7(8), p.e015759.