Abstract
Objective:
Children who suffer traumatic brain injury (TBI) are at high risk of morbidity and mortality. We hypothesized that in patients with TBI, the abusive head trauma (AHT) mechanism versus accidental TBI (aTBI), would be associated with higher frequency of new functional impairment between baseline and later follow-up.
Design:
Retrospective single center cohort study
Setting and Patients:
Children under 3 years of age admitted with TBI to the Pediatric Intensive Care Unit (PICU) at a Level 1 Trauma Center between 2014-2019.
Measurements:
Patient characteristics, TBI mechanism, and Functional Status Scale (FSS) scores at baseline, hospital discharge, short-term (median 10 [interquartile range 3, 12] months), and long-term (median 4 [3, 6] years) post-discharge were abstracted from the electronic health record. New impairment was defined as an increase in FSS >1 from baseline. Patients who died were assigned the highest score (30). Multivariable logistic regression was performed to determine the association between TBI mechanism with new impairment.
Main Result:
Over 6 years, there were 460 TBI children (170 AHT, 290 aTBI), of which 13 with AHT and 4 with aTBI died. Frequency of new impairment by follow-up interval, in AHT vs. aTBI patients, were as follows: hospital discharge (42/157 [27%] vs. 27/286 [9%], P<0.001), short-term (42/153 [27%] vs. 26/259 [10%], P<0.001), and long-term (32/114 [28%] vs. 18/178 [10%], P<0.001). Sensory, communication, and motor domains were worse in AHT patients at the short- and long-term timepoint. On multivariable analysis, AHT mechanism was associated with greater odds (OR [95% confidence interval]) of poor outcome (death and new impairment) at hospital discharge (4.4 [2.2, 8.9]), short-term (2.7 [1.5, 4.9]), and long-term timepoints (2.4 [1.2, 4.8]), P<0.05.
Conclusions
In under 3 years olds admitted to the PICU after TBI, the AHT mechanism – versus aTBI – is associated with greater odds of poor outcome in the follow-up period through to ~5 years post-discharge. New impairment occurred in multiple domains and only AHT patients further declined in FSS over time.
Keywords: Child abuse, Traumatic brain injury, Patient outcome assessment, Pediatric intensive care units, Long-term effect
Traumatic brain injury (TBI) is a major cause of morbidity and mortality in children and abusive head trauma (AHT) is a prominent mechanism of TBI 1. In the 2018/2019 United States Centers for Disease Control and Prevention (CDC) TBI Surveillance Report, the annual incidence of AHT in children under 1 year of age is 22.8 per 100,000, and TBI by any mechanism in children 0-4 years old is 3.1 per 100,000 1.
In the 2014-2017 Approaches and Decisions for Acute Pediatric TBI (ADAPT) trial, which enrolled cases of severe TBI from 8 countries, 135/1000 (13.5%) patients had experienced AHT 2. A 2023 systematic review, an Asian Network retrospective cohort (2014-2017), and a United States Pediatric Health Information Systems database study (2010-2017), together indicate that AHT is associated with poor outcomes, but there is wide variability in the follow-up assessments, as well as factors associated with outcomes 3-5. Furthermore, in two cohorts with AHT, under 1-year-olds (2010-2017) as well as under 3-year-olds (2000-2018) were at risk of survival with new sequelae such as epilepsy, cognitive, and physical functional impairment on later follow-up 6,7. In a follow-up study of TBI cases aged <31 months at the time of injury (2013-2015), longitudinal neuropsychological observations at the same timepoints over 3 years showed that patients who experience severe TBI, which had a large contribution from AHT, had impairments in all domains including: communication, gross motor, personal social, problem solving, and fine motor 8.
We have therefore sought to examine up to 5-year outcomes in our center’s most contemporary cohort (2014-2019) of under 3-year-olds admitted to the PICU with either AHT or aTBI. Our objective is to compare longitudinal outcomes and the associations with new functional impairment.
MATERIALS AND METHODS
The University of Pittsburgh Institutional Review Board (IRB) approved this retrospective observational cohort study with waiver of informed consent in August 2021 (STUDY21060042, “Patterns of and risk factors for multi-organ dysfunction in abusive head trauma compared to accidental traumatic brain injury”). Procedures were followed in accordance with the ethical standards of the IRB and with the Helsinki Declaration of 1975.
Patients aged under 3-years-old who were admitted to the UPMC Children’s Hospital PICU with TBI between 2014-2019 were eligible for cohort inclusion. Children with penetrating trauma were excluded. Children were classified as having AHT if the Child Protection Team determined the TBI was “highly concerning” or “diagnostic” for AHT. Other children were classified as aTBI.
Data Collection
Variables collected from the electronic health record (EHR) included patient demographics, TBI details, brain computed tomography (CT) or magnetic resonance imaging (MRI) results, and organ supports. Glasgow Coma Scale (GCS) score and Injury Severity Score (ISS) on presentation to our hospital were obtained. GCS scores between 15-13 are mild, 12-9 moderate, and 8 and below severe 9. An ISS score of below 9 is considered mild, while 16-24 is severe, and above 25 is profound injury 10.
Longitudinal assessment of function was evaluated using the details of the Functional Status Scale (FSS) recorded from information in the EHR 11,12. For example, we used the clinical documentation of neurologic examination and developmental history by specialists such as therapists (i.e., physical therapy, occupational therapy, speech therapy), rehabilitation medicine, neurology, neurosurgery, primary care, and other clinicians (in order of priority) to generate the FSS at specific timepoints 13,14. FSS subdomains include mental, sensory, communication, motor, feeding, and respiratory function. Information about each domain was abstracted at the following timepoints in a patient’s trajectory: pre-injury, hospital discharge, short-term (closest to 1 year after discharge), and long-term (closest to 5 years after discharge). These timepoints were chosen to be sensitive to changes in development.
Child Opportunity Index (COI) data were obtained by using patient Zone Improvement Plan (ZIP) codes (see www.diversitydatakids.org). The COI is a metric derived from 29 educational, societal, environmental, economic and health variables available by U.S. ZIP code 15. COI data are normalized for standard distribution (20% per quintile) into five quintiles of opportunity (i.e., Very High, High, Moderate, Low, or Very Low). We trichotomized data into High (Very High, High), Moderate (Moderate), and Low (Very Low, Low) groups for analysis because of the small numbers in some quintiles. Pennsylvania state COI data were used in this analysis as 418/460 (91%) of the cohort reside in the state.
Outcomes and Statistical Analysis
The primary outcome was new impairment, defined as an increase in FSS > 1 between baseline and post hospital discharge time points. Patients who died were excluded in impairment comparisons.
Nonparametric tests (Wilcoxon rank sum test, Pearson’s chi-squared test, and Fisher’s exact test) were used to compare characteristics between AHT and aTBI groups. A multivariable logistic regression was conducted to analyze the association between TBI mechanism and new impairment status.
In a univariate regression, the following variables were assessed for association with poor outcome at each timepoint: TBI mechanism (AHT), age in months, ISS at admission, state COI levels, Race, and presence of subdural hemorrhage on initial head CT. Poor outcome was defined as death or new impairment at discharge and new impairment at short term and long term timepoint. These variables were chosen since they have been shown to impact outcomes; then, via backwards stepwise regression for p values < 0.05, the variables included in the multivariable logistic regression were TBI mechanism (AHT vs aTBI), age in months, ISS at admission, and state COI levels. There were no concerns for collinearity.
All statistical analyses were performed by using RStudio version 2022.12.0+353 (Rstudio, Boston, MA) and R version 4.2.2 (R Foundation For Statistical Computing, Vienna, Austria) with the following packages: gtsummary, lubridate, ggplot2, and tidyverse. Missing data were not imputed. Statistical significance was defined as p <0.05, with no correction for multiple comparisons.
RESULTS
We identified a cohort of 464 patients meeting inclusion criteria. Four patients were excluded for penetrating trauma, leaving 460 patients for analysis (Table 1). A total of 290/460 (63%) had aTBI and 170/460 (37%) had AHT. Children with aTBI were older than children with AHT (median 6 [IQR 2, 23] vs. 4 [2, 9] months, P = 0.017). A greater proportion of aTBI patients lived in ZIP codes with high (more advantaged) COI than children with AHT (38/170 [22%]) vs. 91/290 [31%], P = 0.038).
Table 1:
Patient Characteristics by TBI Etiology
| Characteristic | Overall, N = 4601 |
AHT, N = 1701 |
aTBI, N = 2901 |
|---|---|---|---|
| Age median (IQR) months | 5 (2, 16) | 4 (2, 9) | 6 (2, 23) |
| Male sex, n (%) | 282 (61%) | 99 (58%) | 183 (63%) |
| Race, n (%) | |||
| White | 335 (73%) | 123 (72%) | 212 (73%) |
| Black | 63 (14%) | 25 (15%) | 38 (13%) |
| Other | 62 (13%) | 22 (13%) | 40 (14%) |
| State Child Opportunity Index by category, n (%) | |||
| Low | 210 (46%) | 86 (51%) | 124 (43%) |
| Moderate | 121 (26%) | 46 (27%) | 75 (26%) |
| High | 129 (28%) | 38 (22%) | 91 (31%) |
| Previously Healthy, n (%) | 370 (80%) | 130 (76%) | 240 (83%) |
| GCS Severity by category, n (%) | |||
| Mild | 378 (82%) | 134 (79%) | 244 (84%) |
| Moderate | 18 (14%) | 5 (3%) | 13 (5%) |
| Severe | 64 (14%) | 31 (18%) | 33 (11%) |
| Admission ISS, median (IQR) | 13 (9, 18) | 17 (10, 26) | 10 (8, 17) |
| Mechanical Ventilation, n (%) | 93 (20%) | 48 (28%) | 45 (16%) |
| Ventilation Days, median (IQR) | 3 (1, 8) | 5 (3, 10) | 1 (1, 4) |
| Seizure, n (%) | 73 (16%) | 48 (28%) | 25 (8.6%) |
Trauma and Hospitalization details
In general, on univariate analysis of data in Table 1, diagnosis with AHT rather than aTBI, was associated with severe GCS (31/170 [18%] vs. 33/290 [11%], P = 0.040) and worse ISS (17 [10, 26] vs. 10 [8, 17], P < 0.001) at presentation. Also, during initial hospitalization, patients with AHT, rather than aTBI, were more frequently mechanically ventilated (48/170 [28%] vs. 45/290 [16%], P = 0.001) and a greater proportion had seizures (48/170 [28%] vs 25/290 [9%], P < 0.001). In the subset of children requiring mechanical ventilation, an AHT diagnosis versus aTBI diagnosis was associated with longer duration of support (5 [3, 10] vs. 1 [1, 4] days, P < 0.001).
Further univariate comparisons between the AHT and aTBI patients revealed the following associations with hospitalization characteristics. On brain imaging, a diagnosis of AHT was associated with a greater proportion having cerebral edema (39/170 [23%] vs 14/290 [5%], P < 0.001) and subdural hemorrhage (142/170 [84%] vs. 130/290 [45%], P < 0.001). Furthermore, a greater proportion of AHT patients had neurosurgical interventions performed, including: invasive intracranial pressure (ICP) monitoring (16/170 [9%] vs. 7/290 [2%], P < 0.001), extraventricular drain placement (EVD) (20/170 [12%] vs. 8/290 [3%], P < 0.001), and craniectomy (6/170 [4%] vs. 1/290, P < 0.001).
Patient Outcomes
Table 2 summarizes the outcomes by patient grouping as AHT and aTBI. Of note, 13/170 (8%) AHT and 4/290 (1%) aTBI children died during initial hospitalization. In the survivors, we failed to identify an association between diagnosis of AHT, in comparison with aTBI, and the referral for inpatient rehabilitation services after discharge from hospital (14/157 [9%] vs. (11/284 [4%], P = 0.11).
Table 2:
Outcomes by TBI Mechanism (N = 460)
| N | Overall, N = 4601 |
AHT, N = 1701 |
aTBI, N = 2901 |
p-value2 | |
|---|---|---|---|---|---|
| Total LOS, median (IQR) days | 460 | 3 (2, 5) | 4 (3, 10) | 2 (1, 3) | <0.001 |
| ICU LOS, median (IQR) days | 460 | 1 (1, 2) | 2 (1, 4) | 1 (1, 2) | <0.001 |
| New Impairment | |||||
| Hospital Discharge | 443 | 69 (16) | 42 (27) | 27 (9) | <0.001 |
| Short Term Impairment | 412 | 68 (17) | 42 (27) | 26 (10) | <0.001 |
| Long Term Impairment | 292 | 50 (17) | 32 (28) | 18 (10) | <0.001 |
| Disposition | 460 | <0.001 | |||
| Home with pre-TBI parent/guardian | 329 (72) | 61 (36) | 268 (92) | ||
| Home with Foster guardian | 87 (19) | 81 (48) | 6 (2) | ||
| Rehab | 26 (5) | 14 (8) | 12 (4) | ||
| Death | 17 (4) | 13 (8) | 4 (1) | ||
| Skilled Facility | 1 (0) | 1 (1) | 0 (0) |
Median (IQR); n (%)
Wilcoxon rank sum test; Pearson's Chi-squared test; Fisher's exact test
Further analysis of the survivors of TBI showed that a diagnosis of AHT versus aTBI was associated with a higher frequency of new impairment at hospital discharge (55/157 [35%] vs. 31/286 [11%], P < 0.001). Short-term follow up outcomes were available for 413/457 (90%) survivors at median 11.2 [IQR 5.7, 12.5] months for AHT vs 10.1 [IQR 2.1, 12.2] months for aTBI after hospital discharge (P = 0.02). The diagnosis of AHT, as opposed to aTBI, was associated with higher frequency of impairment at this time (42/153 [27%] vs. 26/259 [10%], P<0.001).
Regarding longer-term follow-up of survivors, data were available for 292/457 (64%) of patients at median 49 [IQR 32, 64] months for AHT vs 49 [IQR 37, 67] months for aTBI (P = 0.2). In the long-term, the diagnosis of AHT, rather than aTBI, was associated with more frequent presence of impairment (32/114 [28%] vs. 18/178 [10%], P<0.001).
Outcomes by admission GCS score severity category in survivors are shown in the Supplemental Digital Content ((SDC) Table S1). In both mild and severe GCS severity categories, AHT patients was associated with more impairment than aTBI at each timepoint but we failed to identify any difference in the moderate GCS category.
FSS trajectories were trichotomized into improvement, no change, or impairment from the prior timepoint (Figure 1). Of all survivors at hospital discharge, 69/443 (16%) had impairments. Out of these 69 patients, 43/69 (42%) improved at short term follow up; of these patients 26/43 (60%) had AHT and 17/43 (40%) had aTBI. There were 6 patients who continued to improve, 24 patients who kept their improvement, and 4 AHT patients had more impairment at long term follow up. Fourteen patients had no change at short term follow up and 6 of those continued to have no change, implying their deficits persisted, while 4 improved and 1 AHT patient had further deficit at long term. There were 8 AHT patients who had further impairment at short term and 2 who even had more deficits at long term. Three of those impaired patients improved at long term while 2 had no change. There were no aTBI patients with further impairment and only 2 who didn’t have any improvement from discharge. Patients who improved over each time point after discharge were of older age when compared with those who acquired more impairment after discharge (median 17 (IQR 5, 30)] vs. 3 [IQR 2, 4] months, P < 0.001).
Figure 1. Patient Flowsheet Mapping FSS Trajectories.
In the upper plot, the FSS trajectory flowsheet of AHT patients is shown across the three timepoints while the lower plot demonstrates the aTBI patient flowsheet. There are 3 outcomes at discharge: death, impairment (FSS decrease > 1), or no change in FSS. At the short term and long term timepoints, there are 3 outcomes: improvement (FSS increase > 1), no change in FSS, or impairment (FSS decrease > 1). Of the patients who had deficits at hospital discharge, the only patients who had further decline over time were in the AHT diagnostic group.
Figure S1 (see SDC file) shows the FSS sub-domain results by grouping of mechanism of injury. Three domains (i.e., sensory, communication, and motor) showed a higher frequency of impairment, at each time point, when the diagnostic of AHT was compared with the diagnosis of aTBI. Impairment in communication increased over time while motor impairment improved. The feeding domain was significantly higher in AHT at discharge but not at the other timepoints. There was no significant difference between AHT and aTBI in mental status or respiratory domains at any timepoint.
To examine the magnitude of impairment seen between AHT and aTBI patients, Table S2 shows impairment in survivors with escalating definitions of FSS change from pre-injury. At every level of FSS change (≥1, ≥ 2, ≥ 3), AHT patients had significantly more impairment than aTBI patients. A change of FSS ≥ 3 would classify the patient as having a moderate or severe dysfunction while a change in 1 or 2 would also include mild dysfunction13. Over time, the proportion of AHT patients with moderate or severe dysfunction decreased while the proportion of aTBI patients stayed the same: discharge (22/157 [14%] vs 10/286 [4%], P < 0.001), short term (16/153 [10%] vs 10/259 [4%], P = 0.008), and long term (12/114 [11%] vs 3/178 [2%], P < 0.001).
Multivariable association of TBI mechanism with outcomes
In the multivariable model, using the composite poor outcome in all patients (see methods), the diagnosis of AHT was associated with greater odds (odds ratio [OR], 95% confidence interval [95%CI]) of poor outcome after adjustment for Race, presence of subdural hemorrhage on CT scan, age, COI, and ISS score at hospital discharge (4.4 [2.4-8.6]), short-term (2.7, [1.5-4.9]), and long-term (2.4, [1.2-4.8]) (Table S2, see SDC file).
DISCUSSION
In this retrospective study of TBI patients aged <3 years admitted to the PICU in our center, 2014-2019, we have identified important factors that help to inform differences between outcomes in AHT versus aTBI cases. Our primary finding was that the AHT survivors, as opposed to aTBI, were associated with greater odds of new impairment at hospital discharge, and at short- and long-term time points of follow-up. Second, these new impairments were more commonly in the domains of sensory, communication, and motor function. Third, we found that decline in function, between discharge and the long-term follow-up timepoint, was associated with the diagnosis of AHT and not aTBI.
Our study findings are consistent with old cohorts of patients with AHT showing an association with poor outcomes and functional impairment 3-8. Recent publication of a 2013-2015 pediatric cohort of mixed mechanisms of TBI, aged less than 31 months, found that while mild and moderate severity TBI patients had minimal impairment after injury, severe TBI patients had subsequent impairments in communication, problem solving, and personal social domains that failed to improve over of median 3 years after injury 8. Strikingly, in our more contemporary cohort from 2014-2019, with longer follow-up, we have found that the diagnosis of AHT, rather than aTBI, is associated with greater odds of new impairment 1- and 5-years after injury.
The possible explanations for associated worse outcomes in AHT patients, rather than aTBI patients, include – in theory – late presentation leading to delays in care and increased likelihood of deleterious secondary neurologic insult and injury 16,17. Another explanation may be the unique mechanism and time course of injury, which can include multiple episodes of acceleration and deceleration of the head producing neuronal shear injury 18-20.
Most concerning is the subcohort of 15/42 (36%) AHT patients who continue to worsen over time. The reasons for this functional decline are unclear and this is worrying for lack of rehabilitation support. However, AHT patients have greater health services utilization and also attend school, suggesting these patients aren’t disappearing from the healthcare system21,22. Additionally, published studies across multiple different countries, epochs, healthcare, and economic situations agree with these findings. At long term follow up, COI was associated with impairment, implying social determinants of health as a possible moderator of outcomes23. Medicaid insurance, family substance abuse, and intimate partner violence may impact outcome24,25. Further, arrested development, or “growing into deficits”, could possibly explain worsened impairment trajectories as missed developmental milestones not able to be assessed at a younger age are recognized at later ages. In a recent study of executive function trajectory in pediatric TBI, some children aged 2-5 years old, mainly with severe TBI, worsen after a “recovery plateau” 26. Lastly, there is very little research in specific rehabilitation methods for AHT, with some support of its utility to improve outcomes 22,27.
Consistent with a 2023 PROSPERO (International Prospectively Register of Systematic Reviews) registered systematic review, the clinical implications of our work show that the diagnosis of AHT in under 3-year-old patients requiring PICU admission are at risk of longitudinal functional impairment3. These patients are especially vulnerable and should undergo close long-term neurodevelopmental assessment and rehabilitation to optimize recovery. We have not been able to disentangle failure in follow-up from patient deterioration after discharge from PICU. Focused research is needed to support evidence-based guidelines for hospital-to-home based interventions that may impact outcomes for children seen after AHT or aTBI. The design of our study does not permit this evaluation and we could equally assume that our patients were receiving the appropriate interventions on follow-up, but the underlying pathology was such that it was irremediable.
Our retrospective study does have limitations. First, these data are from a single center cohort, albeit contemporary. Second, derivation of FSS scores by abstracting data from a variety of providers also may fail to present an accurate reflection of the patient’s status. However, there have been studies using this approach which have been considered reliable and accurate 13,14. Third, we did not have a validated definition of change in FSS that we could use to compare neuropsychological measures. In our study, detailed neuropsychological outcomes were not available. Fourth, loss to follow up was prominent at the long-term (~5 year) follow-up time point, which limited the confidence in the outcomes presented (i.e., missing data about late deaths or functional improvement). Fifth, there is heterogeneity in the severity of illness in our cohort for both AHT and aTBI. Sixth, the ISS and GCS score assignment may be less accurate in infants. Finally, we did not have detailed information about the imaging findings and seizure characteristic, both impacting outcomes, that could have helped us to better understand morbidities.
CONCLUSION
In children with TBI, aged under 3-years-old and requiring admission to the PICU for emergency care, there are significant associations between AHT (as opposed to aTBI) and greater odds of longitudinal functional impairment, particularly in the sensory, communication, and motor domains. Future research should explore mechanistic and causative relationships that contribute to worse outcomes in the AHT population.
Supplementary Material
INFORMATION BOXES.
Research In Context:
Abusive head trauma (AHT) is a common mechanism of traumatic brain injury (TBI) in children under 3 years of age requiring admission to the PICU.
Patients who suffer AHT are at increased risk of new impairment in multiple functional domains.
Our objective was to compare longitudinal functional outcomes between AHT and accidental TBI.
What this Study Means:
At hospital discharge after PICU admission, diagnosis of AHT rather than aTBI was associated with greater odds of functional impairment at the short-term and long-term follow-up timepoints.
The communication, sensory, and motor domains were most affected by impairment in both aTBI and AHT, but more associated with AHT.
Some TBI patients have worsening impairments over time and further studies are required to better understand mechanism and potential remediation.
Acknowledgements
The authors wish to acknowledge the Safar Center of Resuscitation at the University of Pittsburgh and the associated NIH training grant (5T32HD040686-22) under the direction of Dr. Patrick Kochanek and Dr. Robert Clark. The Benedum Trauma Center at UPMC Children’s Hospital of Pittsburgh was invaluable in their assistance with this project.
Financial Support:
NIH T32 (5T32HD040686-22) (CRM)
Copyright Form Disclosure:
Drs. McNamara, Kochanek, and Fink received support for article research from the National Institutes of Health (NIH). Dr. McNamara received funding from the NIH (5T32HD040686-22). Dr. Horvat’s institution received funding from the National Institute of Child Health and Human Development. Drs. Kochanek and Fink’s institution received funding from the NIH. Dr. Berger’s institution received funding for expert testimony. Dr. Fink’s institution received funding from the Neurocritical Care Society; they received funding from the American Board of Pediatrics. The remaining authors have disclosed that they do not have any potential conflicts of interest.
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