Abstract
Purpose
Traumatic brain injury (TBI) can cause significant morbidity and mortality in the pediatric population. Brain CT is the mainstay in the diagnosis of intracranial hemorrhage (ICH). The aim of this study was to explore the clinical characteristics that can predict ICH on brain CT in pediatric TBI patients, to assist physicians in deciding on the use of brain CT.
Methods
A total of 475 pediatric TBI patients who underwent brain CT within 24 h after injury from January 2012 to December 2021 in the level 1 trauma center in Thailand were included in this cross-sectional study. Clinical data and brain CT findings were collected. Logistic regression analysis was applied to evaluate clinical characteristics that could predict ICH on brain CT in pediatric TBI patients. A p value was less than 0.05 being indicated that the difference is statistically significant. R software version 3.6.1 was used to statistical analysis.
Results
The included cases have a median (Q1, Q3) age of 7.7 (3.5, 12.6) years. ICH was found in 98 (20.6%) pediatric patients based on brain CT findings. On multivariable analysis, high blunt energy injury (odds ratio (OR) = 2.79, 95% CI 1.27 – 6.11, p = 0.010), motor vehicle accidents (OR = 2.04, 95% CI: 1.14 – 3.67, p = 0.017), Glasgow coma scale score <13 (OR = 4.28, 95% CI: 1.87 – 9.78, p < 0.001), palpable skull fractures (OR = 7.30, 95% CI: 1.44 – 37.04, p = 0.016), signs of basilar skull fracture (OR = 6.10, 95% CI: 2.16 – 17.24, p < 0.001), and vomiting ≥ 3 times (OR = 2.60, 95% CI: 1.17 – 5.77, p = 0.022) were statistically significant predictive factors for ICH in pediatric TBI patients.
Conclusion
These factors might aid clinicians in making an appropriate decision regarding the use of brain CT in pediatric TBI cases.
Keywords: Children, Pediatrics, Traumatic brain injury, Intracranial hemorrhage
1. Introduction
Traumatic brain injury (TBI) is a common condition that leads to emergency department visits in the pediatric population. In 2017, it caused nearly 17,474 cases of hospitalization in the United States.1 It is the leading cause of death among the pediatric population, accounting for approximately 2745 deaths in 2017.1 Although most cases are mild head injury (MHI), significant intracranial injury can occur in those initially diagnosed with MHI, leading to mortality and impaired neurological development. Moreover, a thorough history and physical examination are difficult to conduct in children.2 The use of brain CT as a reference standard to diagnose intracranial injuries has dramatically increased.3, 4, 5 However, for some children keeping still for several minutes throughout CT scans is difficult, and sedation is required to ensure success. Radiologically practical sedation carries some risks. It has been observed that adverse effects of sedation in children include vomiting, aspiration, asphyxiation, and trouble breathing.6,7 The main disadvantages of brain CT include radiation exposure that increases the risk of cancer and the need for procedural sedation.8, 9, 10 Few algorithms to improve clinical decision-making in pediatric TBI have been developed to balance the risks and benefits of brain CT with missed or delayed diagnosis of intracranial injury and unnecessary CT imaging, including the pediatric emergency care applied research network (PECARN) rule11, the Canadian assessment of tomography for childhood head injury12, and the children's head injury algorithm for the prediction of important clinical events13. These algorithms have heterogeneous criteria guiding management of head trauma in children. The primary clinical decision rule used in our institution is PECARN, which aids physicians to determine if pediatric TBI patients require brain CT. The pediatric patients with TBI were divided into 3 groups based on its criteria: CT recommended (CTR), shared decision-making (SDM), and CT not recommended. Unfortunately, the SDM group includes about 40% – 50% of patients.14,15 These patients are either chosen for brain CT or observation based on the physician's judgment. The SDM group includes roughly 13.9% radiographic TBI and 0.8% – 2.5% clinically significant TBI patients.14,15 In addition, because the incidence of intracranial hemorrhage (ICH) is quite low and most pediatric TBIs are MHIs, surveillance is probably more beneficial and can minimize the need for brain CT.14, 15, 16 Understanding the considerable risks of ICH among children with TBI is crucial.
The main objective of this study was to investigate clinical characteristics that can predict ICH presentations on brain CT in pediatric TBI patients.
2. Methods
This study was a retrospective cross-sectional study conducted in the level 1 trauma center of the University Hospital in Southern Thailand. Children younger than 15 years old with TBI who were admitted to the emergency department and underwent brain CT imaging within 24 h after injury from January 2012 to December 2021 were eligible. Children with any ICH due to other causes such as prematurity, birth trauma, and post-surgical procedures, and those with pre-existing neurological disorders complicating assessment were excluded. Children with any incomplete documentation from the hospital information system were also excluded. The study protocol was approved by the Human Research Ethics Committee (approval number: REC.61-343-7-4).
The main outcome of this study was ICH in brain CT images. ICH was defined as the CT presentation of acute epidural hematoma, acute subdural hematoma, traumatic subarachnoid hemorrhage, intraventricular hemorrhage, or intracerebral hemorrhage.
Individual parameters comprising age and sex were collected. History of altered mental status, loss of consciousness, vomiting ≥ 3 times, abnormal per parent, severe headache, associated chest injury, associated abdominal injury, and associated skeletal injury were also included. The pediatric Glasgow coma scale (GCS) score served as a physiological parameter. Injury parameters consisted of injury types including penetrating, blunt high energy, and blunt low energy and the injury mechanism including motor vehicle accident, pedestrian struck, falling, and other. Focal neurological deficit, palpable skull fracture, signs of basilar skull fracture, and scalp hematoma were diagnosed by physical examination. To manage pediatric patients with TBI at our institution, neurosurgeons used the PECARN criteria to determine if brain CT scan was necessary. All brain CT images were reviewed by a pediatric radiologist. Injuries identified by CT findings were recorded. The information was collected and retrieved from the trauma registry and the hospital information system of our institute. The picture archiving and communication system was used to review brain CT images.
For a predictive model, transparent reporting of a multivariable prediction model for individual prognosis of diagnosis advises a minimum of 10 events for each candidate variable. We hypothesized that there would be 5 relevant variables. A pilot study carried out at our institute found that 10.6% of pediatric TBI patients experienced ICH. Therefore, a sample size of 472 patients for 50 events was estimated.17
The patient characteristics of the ICH group were compared with those of the non-ICH group using the Chi-squared test or Fisher's exact test for categorical data and student t-test or Mann-Whitney U test for continuous data. The impact of risk between groups was assessed using logistic regression. Variables with p < 0.2 in the univariable analysis as well as some significant risk factors from literature reviews18 were entered into the multivariable analysis and p < 0.05 was deemed statistically significant. All data were analyzed using the R software version 3.6.1.
3. Results
During the study period, a total of 475 consecutive cases of pediatric TBI of any severity were included. The median (Q1, Q3) age was 7.7 (3.5, 12.6) years. The majority of patients were older than 2 years and predominantly boys. The most common mechanisms of injury were motor vehicle accidents and high-energy blunt force. Most cases had an initial pediatric GCS score of 13 or more (89.7%). The clinical presentation and physical examination data are shown in Table 1.
Table 1.
Clinical characteristics of pediatric traumatic brain injury (n = 475).
| Variables | Median (Q1, Q3) | n (%) |
|---|---|---|
| Age (year) | 7.7 (3.5, 12.6) | |
| ≤ 2 | 67 (14.1) | |
| > 2 | 408 (85.9) | |
| Male | 296 (62.3) | |
| Injury type | ||
| Penetrating | 2 (0.4) | |
| Blunt, high energy | 332 (69.9) | |
| Blunt, low energy | 141 (29.7) | |
| Injury event | ||
| Motor vehicle accident | 257 (54.1) | |
| Pedestrians struck | 49 (10.3) | |
| Falling | 135 (28.4) | |
| Others | 34 (7.2) | |
| Pediatric GCS score | ||
| ≥ 13 | 426 (89.7) | |
| < 13 | 49 (10.3) | |
| Clinical history and examination | ||
| Focal neurological deficit | 2 (0.4) | |
| Palpable skull fracture | 9 (1.9) | |
| Signs of basilar skull fracture | 22 (4.6) | |
| Scalp hematoma | 161 (33.9) | |
| Altered mental status | 119 (25.1) | |
| Loss of consciousness | 221 (44.4) | |
| Vomiting ≥ 3 times | 74 (15.6) | |
| Abnormal acting per parent | 44 (9.3) | |
| Severe headache | 14 (2.9) | |
| Associated chest injury | 20 (4.2) | |
| Associated abdominal injury | 24 (5.1) | |
| Associated skeletal injury | 89 (18.7) | |
GCS: Glasgow coma scale.
Abnormal brain CT findings are shown in Table 2, which were found in 31.4% of patients. Among the included cases, maxillofacial and skull fractures were the most common findings (76.5%). About 20.6% of patients had ICH, with subdural hemorrhage being the most frequent type, followed by epidural hemorrhage.
Table 2.
Brain CT findings related to pediatric traumatic brain injury (n = 475).
| CT findings | n (%) |
|---|---|
| Abnormal CT finding | 149 (31.4) |
| Intracranial hemorrhage | 98 (20.6) |
| Intraparenchymal hemorrhage | 26 (5.5) |
| Subarachnoid hemorrhage | 33 (6.9) |
| Subdural hemorrhage | 53 (11.2) |
| IVH | 6 (1.3) |
| Epidural hemorrhage | 39 (8.2) |
| Associated maxillofacial and skull fractures | 114 (24) |
| Midline shift | 15 (3.2) |
| Brain herniation | 7 (1.5) |
IVH: intraventricular hemorrhage.
Table 3 shows the comparison of clinical characteristics between patients with and without ICH on CT scans. The variables that had a significant association with ICH included injury type, injury event, altered mental status on history, initial pediatric GCS score, palpable skull fracture, signs of basilar skull fracture on physical examination, associated chest injury, and associated skeletal injury.
Table 3.
Clinical characteristics of patients with intracranial hemorrhage compared to those without intracranial hemorrhage.
| Variables | Patients with ICH (n = 98) | Patients without ICH (n = 377) | p value |
|---|---|---|---|
| Age (year), median (Q1, Q3) | 10.3 (4.6, 13.1) | 7.1 (3.2, 12.4) | 0.012 |
| Age groups | 0.916 | ||
| < 2 years | 13 (13.3) | 54 (14.3) | |
| ≥ 2 years | 85 (86.7) | 323 (85.7) | |
| Male | 57 (58.2) | 239 (63.4) | 0.404 |
| Injury type | < 0.001 | ||
| Penetrating | 0 (0) | 2 (0.5) | |
| Blunt, high energy | 85 (86.7) | 247 (65.5) | |
| Blunt, low energy | 13 (13.3) | 128 (34.0) | |
| Injury event | < 0.001 | ||
| Motor vehicle accident | 71 (72.4) | 186 (49.3) | |
| Pedestrians struck | 12 (12.2) | 37 (9.8) | |
| Falling | 11 (11.2) | 124 (32.9) | |
| Others | 4 (4.1) | 30 (8.0) | |
| Pediatric GCS score | < 0.001 | ||
| ≥ 13 | 68 (69.4) | 358 (95.0) | |
| < 13 | 30 (30.6) | 19 (5.0) | |
| Clinical history and examination | |||
| Focal neurological deficit | 1 (1.0) | 1 (0.3) | 0.370 |
| Palpable skull fracture | 6 (6.1) | 3 (0.8) | 0.003 |
| Signs of basilar skull fracture | 14 (14.3) | 8 (2.1) | < 0.001 |
| Scalp hematoma | 37 (37.8) | 124 (32.9) | 0.432 |
| Altered mental status | 43 (43.9) | 76 (20.2) | < 0.001 |
| Loss of consciousness | 52 (53.1) | 159 (42.2) | 0.069 |
| Vomiting ≥ 3 times | 14 (14.3) | 60 (15.9) | 0.810 |
| Abnormal acting per parent | 5 (5.1) | 39 (10.3) | 0.162 |
| Severe headache | 2 (2.0) | 12 (3.2) | 0.744 |
| Associated chest injury | 8 (8.2) | 12 (3.2) | 0.044 |
| Associated abdominal injury | 7 (7.1) | 17 (4.5) | 0.302 |
| Associated skeletal injury | 26 (26.5) | 63 (16.7) | 0.038 |
Data are presented as n (%).
ICH: intracranial hemorrhage; GCS: Glasgow coma scale.
The multivariable analysis showed that significant clinical predictors for ICH included blunt high energy (odds ratio (OR) = 2.79, 95% CI: 1.27 – 6.11, p = 0.010), motor vehicle accident (OR = 2.04, 95% CI: 1.14 – 3.67, p = 0.017), moderate to severe degree of initial pediatric GCS (OR = 4.28, 95% CI: 1.87 – 9.78, p < 0.001), palpable skull fracture (OR = 7.30, 95% CI: 1.44 – 37.04, p = 0.016), signs of basilar skull fracture (OR = 6.10, 95% CI: 2.16 – 17.24, p < 0.001), and vomiting ≥ 3 times (OR = 2.60, 95% CI: 1.17 – 5.77, p = 0.022) (Table 4).
Table 4.
Multivariable analysis of clinical characteristics associated with pediatric traumatic intracranial hemorrhage.
| Parameters | Adjusted OR (95% CI) | p value |
|---|---|---|
| Injury type: Blunt high energy | 2.79 (1.27 – 6.11) | 0.010 |
| Injury event: Motor vehicle accident | 2.04 (1.14 – 3.67) | 0.017 |
| Pediatric GCS < 13 | 4.28 (1.87 – 9.78) | <0.001 |
| Palpable skull fracture | 7.30 (1.44 – 37.04) | 0.016 |
| Signs of basilar skull fracture | 6.10 (2.16 – 17.24) | <0.001 |
| Vomiting ≥3 times | 2.60 (1.17 – 5.77) | 0.022 |
OR: odd ratio; CI: confidence interval; GCS: Glasgow coma scale.
Table 5 presents a subgroup statistic evaluation of the MHI group. ICH was identified in 16.0% of the MHI patients. Injury type, injury event, and signs of basilar skull fracture were the variables significantly correlated with ICH in the MHI group's univariable analysis. On the multivariable analysis, the same characteristics from the initial all severity of the pediatric GCS served as significant clinical predictors for ICH. They consisted of injury type, blunt high energy (OR = 2.35, 95% CI: 1.03 – 5.33, p = 0.041); injury event, motor vehicle accident (OR = 2.43, 95% CI: 1.25 – 4.72, p = 0.009); palpable skull fracture (OR = 6.04, 95% CI: 1.09 – 33.61, p = 0.040); signs of basilar skull fracture (OR = 6.74, 95% CI: 2.12 – 21.46, p = 0.001); and vomiting ≥ 3 times (OR = 3.01, 95% CI: 1.36 – 6.68, p = 0.007) (Table 6).
Table 5.
Clinical characteristics of patients with intracranial hemorrhage compared to those without intracranial hemorrhage in a subset group of pediatric GCS 13.
| Variables | Patients with ICH (n = 68) | Patients without ICH (n = 358) | p value |
|---|---|---|---|
| Male | 43 (63.2) | 227 (63.4) | 1.000 |
| Injury type | 0.011 | ||
| Penetrating | 0 (0) | 2 (0.6) | |
| Blunt, high energy | 56 (82.4) | 231 (64.5) | |
| Blunt, low energy | 12 (17.6) | 125 (34.9) | |
| Injury event | < 0.001 | ||
| Motor vehicle accident | 48 (70.6) | 172 (48) | |
| Pedestrians struck | 7 (10.3) | 36 (10.1) | |
| Falling | 10 (14.7) | 123 (34.4) | |
| Others | 3 (4.4) | 27 (7.5) | |
| Clinical history and examination | |||
| Focal neurological deficit | 1 (1.5) | 1 (0.3) | 0.294 |
| Palpable skull fracture | 3 (4.4) | 3 (0.8) | 0.054 |
| Signs of basilar skull fracture | 7 (10.3) | 7 (2.0) | 0.003 |
| Scalp hematoma | 26 (38.2) | 116 (32.4) | 0.427 |
| Altered mental status | 16 (23.5) | 59 (16.5) | 0.220 |
| Loss of consciousness | 37 (54.4) | 149 (41.6) | 0.069 |
| Vomiting ≥ 3 times | 14 (20.6) | 59 (16.5) | 0.517 |
| Abnormal acting per parent | 4 (5.9) | 37 (10.3) | 0.359 |
| Severe headache | 2 (2.9) | 12 (3.4) | 1.000 |
| Associated chest injury | 3 (4.4) | 7 (2.0) | 0.204 |
| Associated abdominal injury | 3 (4.4) | 11 (3.1) | 0.476 |
| Associated skeletal injury | 14 (20.6) | 57 (15.9) | 0.442 |
Data are presented as n (%).
ICH: intracranial hemorrhage; SD: standard deviation; GCS: Glasgow coma scale.
Table 6.
Multivariable analysis of clinical characteristics associated with pediatric traumatic intracranial hemorrhage in a subset group of pediatric GCS ≥13.
| Variables | Adjusted OR (95% CI) | p value |
|---|---|---|
| Injury type: blunt high energy | 2.35 (1.03 – 5.33) | 0.041 |
| Injury event: motor vehicle accident | 2.43 (1.25 – 4.72) | 0.009 |
| Palpable skull fracture | 6.04 (1.09 – 33.61) | 0.040 |
| Signs of basilar skull fracture | 6.74 (2.12 – 21.46) | 0.001 |
| Vomiting ≥ 3 times | 3.01 (1.36 – 6.68) | 0.007 |
OR: odds ratio; CI: confidence interval; GCS: Glasgow coma scale.
After stratifying the MHI group by PACARN in a total of 426 patients, the CTR group comprised 213 (50.0%) patients, the SDM group comprised 203 (47.7%), and the CT not recommended group comprised 10 (2.3%) patients. Only 68 (16.0%) patients in MHI group had ICH, while 36 (52.9%) patients and 32 (47.1%) patients had ICH in the CTR and SDM groups, respectively. In the CT not recommended group, no ICH was identified. Additionally, 8 of the 32 (25.0%) patients in the SDM group with ICH had isolated factors, while 24 (75.0%) had several factors. Further, 6 of the 8 (75.0%) isolated factor cases involved blunt high energy, 1 (12.5%) involved vomiting, and 1 (12.5%) involved loss of consciousness. Only 6 (1.4%) patients in the MHI group required neurosurgical intervention. Among these 6 cases, 5 (2.3%) cases were from the CTR group, and 1 (0.5%) case was from the SDM group. The single patient from the SDM group who needed neurosurgical intervention had multiple predictive factors, including blunt high energy, scalp hematoma, and loss of consciousness. Moreover, all patient in the MHI group survived.
4. Discussion
Prediction of ICH in children with TBI is challenging. Missed or delayed ICH diagnosis in children can lead to neurological problems and disability.19,20 Although brain CT is the gold standard for diagnosing ICH, it emits radiation and may cause cancer in the future.4,8, 9, 10 Additionally, it might be difficult for children to remain still for a long time during a CT scan. Children must be sedated in order to undergo a CT scan, which is not without risk.6,7
Most children with TBI present with MHI.21 Several studies showed a low prevalence of confirming TBI using brain CT in this group of patients (4.8% – 8.4%).11,22, 23, 24, 25, 26 The results of our investigation were consistent with the most common MHI presentation, but a higher prevalence (16.0%) of ICH on brain CT was identified. The consensus is that patients with a GCS score <13 should undergo a screening brain CT.27 Our study results confirmed that there was a substantial GCS score difference between the groups with and without ICH (p < 0.001). Moreover, a multivariable logistic regression modeling analysis demonstrated that a GCS score < 13 is a risk factor for ICH (OR = 4.28, 95% CI: 1.87 – 9.78, p < 0.001). Our patients with ICH diagnosed by CT scan had a higher occurrence of palpable skull fracture and signs of basilar skull fracture on physical examination than those with normal CT scan. Similarly, previous research showed that basal skull fractures and skull fractures are substantially associated with ICH in pediatric MHI cases.18,28, 29, 30, 31
In our study, we further found that high blunt force mechanisms and motor vehicle accidents were the factors significantly associated with ICH. This may be due to the nature of the mechanism of the injury, which can lead to a high impact and cause ICH. This result is similar to that of an earlier study, where Osmond et al.12 found high blunt force mechanisms of injury and vehicle accidents to be strongly associated with brain injury in pediatric MHI.32
Interestingly, we discovered that vomiting ≥3 times is a significant predictor of ICH in pediatric TBI patients. Previous meta-analysis showed that isolated vomiting did not significantly predict ICH in pediatric MHI29,30, and Osmond et al.12 also showed that vomiting ≥ 2 times was not associated with brain injury. However, other studies have mentioned that a history of vomiting was a predictor for ICH.31,32
For the SDM group, the decision to perform brain CT is based on several factors. Clinical factors used to guide decision-making for the SDM group, according to PECARN, included multiple or isolated factors, worsening findings during observation, physician experience, parental preference, or aged <3 months. The results of our study demonstrated that the SDM group accounts for approximately 47.7% of all patients with MHI, which aligns with the previous studies by Pennell et al.14 and Kauffman et al.15.
In addition, only 15.0% of the patients in the SDM group presented with ICH, and 75.0% of these ICH cases were detected with multiple factors. A minority of cases (1.4%) in the MHI group required neurosurgical intervention. Furthermore, 1 case in the SDM group that required neurosurgical intervention had multiple factors, which may imply that in the SDM group, brain CT benefits patients with multiple factors. Therefore, the patients in the SDM group with isolated predictive factors could have avoided brain CT with appropriate parental counseling.
The strength of this study resides in the inclusion of all severities of head trauma in pediatric TBI, with a subgroup analysis only in the case of MHI. The findings support the previously mentioned important clinical predictors of ICH. Nevertheless, this study has several limitations. Only a small number of positive CT scans were identified in pediatric patients diagnosed with TBI. Because of a small number of patients under the age of 2 years, patients with moderate to severe head injuries, and those with penetrating injuries, these precluded us from drawing definitive conclusions about the associated risk factors in these patient groups. Furthermore, the nature of a retrospective review study makes it difficult to ensure that all desired data points are present on each patient chart, and some important data may have been missing. Lastly, we did not correlate injury progression with hospital stay, intubation status, and long-term outcomes.
In conclusion, we found an association between 6 predictive factors and ICH in cases of pediatric TBI, which included injury type (blunt high energy), injury event (motor vehicle accident), pediatric GCS score <13, palpable skull fracture, signs of basilar skull fracture, and vomiting ≥3 times. A pediatric GCS score <13, palpable skull fracture, and signs of basilar skull fracture were characteristics in the CTR group that indicated the need for brain CT. In the SDM group, injury type (blunt high energy), injury event (motor vehicle accident), and vomiting ≥3 times were statistically significant independent risk factors for traumatic ICH in pediatric TBI patients. This data may assist physicians decide which patients should undergo immediate brain CT, in cases indicative of ICH in children with a TBI in the emergency department.
Funding
Nil.
Ethical statement
The study protocol was approved by the Human Research Ethics Committee, REC.61-343-7-4, of Faculty of Medicine, Prince of Songkla University, Thailand.
Declaration of competing interest
The authors have indicated there is no potential conflict of interest to disclosure.
Author contributions
Pattama Tanaanantarak: conceptualized and designed the study (lead), data collection (equal), analyzed data (lead), reviewed and revised the manuscript (lead); Soraya Suntornsawat: drafted the initial manuscript (equal), collected data (equal), and performed the initial analysis (equal); Srila Samphao: reviewed and revised the manuscript (equal). All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
Footnotes
Peer review under responsibility of Chinese Medical Association.
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