Postoperative magnetic resonance imaging may predict poor outcome in children with severe traumatic brain injuries who undergo cranial surgery

Cordell M. Baker Department of Neurosurgery, Division of Pediatric Neurosurgery, Primary Children’s Hospital, University of Utah, Salt Lake City, Utah

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Andrew Parker Cox Department of Neurosurgery, Division of Pediatric Neurosurgery, Primary Children’s Hospital, University of Utah, Salt Lake City, Utah

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Joshua C. Hunsaker Department of Neurosurgery, Division of Pediatric Neurosurgery, Primary Children’s Hospital, University of Utah, Salt Lake City, Utah

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Jonathan Scoville Department of Neurosurgery, Division of Pediatric Neurosurgery, Primary Children’s Hospital, University of Utah, Salt Lake City, Utah

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Robert J. Bollo Department of Neurosurgery, Division of Pediatric Neurosurgery, Primary Children’s Hospital, University of Utah, Salt Lake City, Utah

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OBJECTIVE

Multiple studies have evaluated the use of MRI for prognostication in pediatric patients with severe traumatic brain injury (TBI) and have found a correlation between diffuse axonal injury (DAI)–type lesions and outcome. However, there remains a limited understanding about the use of MRI for prognostication after severe TBI in children who have undergone cranial surgery.

METHODS

Children with severe TBI who underwent craniectomy or craniotomy at Primary Children’s Hospital in Salt Lake City, Utah, between 2010 and 2019 were identified retrospectively. Of these 92 patients, 43 underwent postoperative brain MRI within 4 months of surgery. Susceptibility-weighted imaging (SWI) and FLAIR sequences were used to designate areas of hemorrhagic and nonhemorrhagic cerebral lesions related to DAI. Patients were then stratified based on the location of the DAI as read by a neuroradiologist as superficial, deep, or brainstem. The location of the DAI and other variables associated with poor outcome, including Glasgow Coma Scale (GCS) score, pediatric trauma score, mechanism of injury, and time to surgery, were analyzed for correlation with poor outcome. Outcomes were reported using the King’s Outcome Scale for Childhood Head Injury (KOSCHI).

RESULTS

In the 43 children with severe TBI who underwent postoperative brain MRI, the median GCS score on arrival was 4. The most common cause of injury was falls (14 patients, 33%). The most common primary intracranial pathology was subdural hematoma in 26 patients (60%), followed by epidural hematoma in 9 (21%). Fifteen patients (35%) had cerebral herniation and 31 (72%) had evidence of contusion. Variables associated with poor outcome included cerebral herniation (r = 0.338, p = 0.027) and location of DAI (r = 0.319, p = 0.037). In a separate analysis, brainstem DAI was shown to predict poor outcome, whereas location (no, superficial, or deep DAI) did not. Logistic regression showed that brainstem DAI (OR 22.3, p = 0.020) had a higher odds ratio than cerebral herniation (OR 10.5, p = 0.044) for poor outcome. Thirty-six children (84%) had a satisfactory outcome at last follow-up; 3 (7%) children died.

CONCLUSIONS

The majority of children in this series who presented with a severe TBI and underwent craniectomy or craniotomy made a satisfactory recovery. In patients in whom there is a concern for poor outcome, the location of DAI-type lesions with SWI and FLAIR may assist in prognostication. The authors’ results revealed that DAI-type lesions in the brainstem and evidence of cerebral herniation may indicate a poorer prognosis; however, more studies with larger cohorts are needed to make definitive conclusions.

ABBREVIATIONS

DAI = diffuse axonal injury; GCS = Glasgow Coma Scale; KOSCHI = King’s Outcome Scale for Childhood Head Injury; SWI = susceptibility-weighted imaging; TBI = traumatic brain injury.

OBJECTIVE

Multiple studies have evaluated the use of MRI for prognostication in pediatric patients with severe traumatic brain injury (TBI) and have found a correlation between diffuse axonal injury (DAI)–type lesions and outcome. However, there remains a limited understanding about the use of MRI for prognostication after severe TBI in children who have undergone cranial surgery.

METHODS

Children with severe TBI who underwent craniectomy or craniotomy at Primary Children’s Hospital in Salt Lake City, Utah, between 2010 and 2019 were identified retrospectively. Of these 92 patients, 43 underwent postoperative brain MRI within 4 months of surgery. Susceptibility-weighted imaging (SWI) and FLAIR sequences were used to designate areas of hemorrhagic and nonhemorrhagic cerebral lesions related to DAI. Patients were then stratified based on the location of the DAI as read by a neuroradiologist as superficial, deep, or brainstem. The location of the DAI and other variables associated with poor outcome, including Glasgow Coma Scale (GCS) score, pediatric trauma score, mechanism of injury, and time to surgery, were analyzed for correlation with poor outcome. Outcomes were reported using the King’s Outcome Scale for Childhood Head Injury (KOSCHI).

RESULTS

In the 43 children with severe TBI who underwent postoperative brain MRI, the median GCS score on arrival was 4. The most common cause of injury was falls (14 patients, 33%). The most common primary intracranial pathology was subdural hematoma in 26 patients (60%), followed by epidural hematoma in 9 (21%). Fifteen patients (35%) had cerebral herniation and 31 (72%) had evidence of contusion. Variables associated with poor outcome included cerebral herniation (r = 0.338, p = 0.027) and location of DAI (r = 0.319, p = 0.037). In a separate analysis, brainstem DAI was shown to predict poor outcome, whereas location (no, superficial, or deep DAI) did not. Logistic regression showed that brainstem DAI (OR 22.3, p = 0.020) had a higher odds ratio than cerebral herniation (OR 10.5, p = 0.044) for poor outcome. Thirty-six children (84%) had a satisfactory outcome at last follow-up; 3 (7%) children died.

CONCLUSIONS

The majority of children in this series who presented with a severe TBI and underwent craniectomy or craniotomy made a satisfactory recovery. In patients in whom there is a concern for poor outcome, the location of DAI-type lesions with SWI and FLAIR may assist in prognostication. The authors’ results revealed that DAI-type lesions in the brainstem and evidence of cerebral herniation may indicate a poorer prognosis; however, more studies with larger cohorts are needed to make definitive conclusions.

In Brief

In a large cohort of children with severe traumatic brain injury undergoing emergency hemicraniectomy, researchers identified diffuse axonal injury in the diencephalon and brainstem as powerful predictors of poor outcome.

Traumatic brain injury (TBI) is the leading cause of death and long-term disability among children worldwide.1 Every year in the United States, there are an estimated 630,000 emergency department visits for children with TBI and 6000 deaths.2,3 Not uncommonly, children with severe TBI will undergo cerebral surgery with or without evacuation of hematoma to alleviate intracranial pressure. Although many children who undergo these operations make a satisfactory recovery, it can be difficult to predict which patients will have a poor prognosis.

Many studies have explored the use of imaging modalities to predict outcomes in children with TBI. The Rotterdam CT score, a prognostic classification system based on CT scans in adults with TBI, has also been validated to predict mortality in the pediatric population in those with moderate or severe TBI.4 Despite the utility of CT for initial evaluation, the modality underestimates the extent of diffuse axonal injury (DAI) and parenchymal injury, which are more accurate predictors of outcomes and better seen on MRI. More recently, MRI has been used to predict outcomes in children with TBI.3 Multiple studies have suggested that the location of DAI-type lesions on MRI may be used for prognostication.57 This has also been confirmed in pediatric studies, which revealed that nonhemorrhagic lesions in the brainstem were predictive of poor outcome.8 However, the utility of MRI in children who have TBI and undergo cranial surgery is unclear because this unique population has different intracranial pathologies and treatment courses.

No study to date has evaluated MRI for prognostication in children who have undergone either craniectomy or craniotomy after severe TBI. The establishment of an accurate outcome predictor in these patients is necessary to guide appropriate clinical management and accurately counsel family members on prognosis and expectations when these injuries occur. The aim of this study was to evaluate the utility of postoperative MRI in children who present with severe TBI and undergo cerebral surgery. We hope that this study will provide further guidance on the use of MRI as a prognostication tool in these patients.

Methods

Study Population

Patient data were collected retrospectively at our level 1 pediatric trauma center with approval of the University of Utah IRB. Data were collected from the years 2010 to 2019. Eligible patients were 17 years of age and younger, sustained a trauma with a severe TBI designated as a Glasgow Coma Scale (GCS) score of 8 or less, underwent surgery within 48 hours of presentation, and underwent postoperative MRI of the brain within 4 months. Presenting GCS and pediatric trauma scores were taken from the medical records of the initial encounter.

Outcome of Interest

The outcome of interest was poor outcome as measured by the King’s Outcome Scale for Childhood Head Injury (KOSCHI),9,10 which has been used previously to assess outcomes after TBI in children.11 The KOSCHI is a 5-point ordinal scale that grades patients as 1 (death), 2 (vegetative state), 3 (severe disability involving some purposeful movement but highly dependent), 4 (moderate disability but mostly independent), and 5 (good without effect on functioning or no detectable sequelae). Children with a KOSCHI score of 1–3 were designated as having a poor outcome. The KOSCHI scores were taken from chart review of either neurosurgery or pediatric physical medicine and rehabilitation notes from the patient’s last clinical follow-up. This scale was chosen because it is specifically for children, has the advantage of being easily applied retrospectively, and provides long- and short-term functional outcome information.

All patients in the study had a postoperative brain MRI. Images were read by an attending pediatric neuroradiologist. Definitive diagnosis of DAI is made on postmortem pathological study;12 however, in living patients, a combination of clinical and imaging assessments is typically used to confirm diagnosis. The presence of small hemorrhagic lesions on susceptibility-weighted imaging (SWI) and nonhemorrhagic lesions on FLAIR sequences was used to make the diagnosis of DAI-type lesions.5,6,13,14 The location of lesions was classified into three zones that have been shown to be correlated with outcomes: a superficial zone, a deep zone, and the brainstem (Table 1).8

TABLE 1.

Categorized location of DAI-type lesions

ZoneDescription
SuperficialFrontal, parietal, temporal, & occipital cortical gray & subcortical white matter
DeepCorpus callosum, internal & external capsule, basal ganglia, & thalamus
BrainstemMidbrain, pons, & medulla

Informed by Smitherman et al., 2016.8

The degree of midline shift and presence of cerebral herniation were taken from preoperative CT scans of the head. Contusions were identified on head CT and brain MRI. Imaging characteristics were identified by a radiologist.

Statistical Analysis

Descriptive statistics were generated for patient and imaging characteristics and operative details. Univariate analysis with two-tailed Spearman’s rank-order correlation was conducted to assess association between variables thought to be associated with poor outcome. Fisher’s exact test was used to compare locations of cerebral DAI with poor outcome. Variables found to be associated with poor outcome were further analyzed by logistical regression; p < 0.05 was considered significant.

Literature Search

To identify relevant academic articles, PubMed and Google Scholar were searched with the following terms used alone or in combination: traumatic brain injury, pediatric, diffuse axonal injury, magnetic resonance imaging, outcomes, imaging, children, fluid-attenuated inversion recovery, susceptibility-weighted imaging, surgery, cerebral, hemicraniectomy, and hemicraniotomy.

Results

A total of 92 pediatric patients (median age 8 years, 26 [60%] males) who had a severe TBI and underwent either craniotomy or craniectomy were identified. Of these patients, 43 (47%) underwent postoperative brain MRI performed within 4 months of their injury (Table 2). The median day on which imaging was performed was day 5. The median GCS score was 4, and 49% of patients had a GCS score of 3 on arrival. Of the 29 children with documented field GCS scores, 26 (90%) had a GCS score of less than or equal to 8. The most common mechanisms of injury were fall in 14 patients (33%), abuse in 11 (26%), and recreational in 9 (21%). Subdural hematoma was the most common primary intracranial hemorrhage in 26 patients (60%); 9 (21%) patients had an epidural hematoma, and 7 (16%) patients had an intraparenchymal hemorrhage or contusion. The median midline shift was 7 mm; 15 (35%) patients had evidence of cerebral herniation on imaging and 31 (72%) had cerebral contusions. The median time from injury to start of surgery was 7 hours 59 minutes, and the median time from arrival to start of surgery was 1 hour 9 minutes. Seventy-eight percent of children had a surgery start time within 2 hours of arrival. The median KOSCHI score was 5. Thirty-six patients (84%) had a satisfactory outcome at the last known follow-up with a KOSCHI score of 4 or 5. Three patients (7%) died.

TABLE 2.

Descriptive characteristics of 43 patients

Variable Value
Median age (range) 8 yrs (6 mos–17 yrs)
Sex
 Male26 (60)
 Female17 (40)
Admission GCS score
 Median4
 321 (49)
 48 (19)
 51 (2)
 63 (7)
 74 (9)
 86 (14)
Field GCS score29 (67)
 13–15 (mild)1 (3)
 9–12 (moderate)2 (7)
 ≤8 (severe)26 (90)
Mechanism of injury
 Fall14 (33)
 MVC5 (12)
 Pedestrian vs car 3 (7)
 Abuse11 (26)
 Recreational 9 (21)
 GSW1 (2)
Pediatric trauma score
 9–12 (minor trauma)1 (2)
 6–8 (potentially life threatening)19 (44)
 0–5 (life threatening)23 (53)
Imaging
 Primary hemorrhage type
  SDH26 (60)
  EDH9 (21)
  IPH/contusion7 (16)
  tSAH1 (2)
 Median midline shift (range) 7 mm (0–18 mm)
 Cerebral herniation15 (35)
 Cerebral contusion31 (72)
Hemicraniectomy side
 Rt19 (44)
 Lt20 (47)
 Bifrontal 4 (9)
Median time to surgery from injury7 hrs 59 mins
Median time to surgery from arrival 1 hr 9 mins 30 sec
Median KOSCHI score5
 1–3 (poor outcome) 7 (16)
 4 or 5 (satisfactory outcome)36 (84)
Median last known follow-up 22 mos

EDH = epidural hematoma; GSW = gunshot wound; IPH = intraparenchymal hemorrhage; MVC = motor vehicle collision; SDH = subdural hematoma; tSAH = traumatic subarachnoid hemorrhage.

Values are reported as number of patients (%) unless otherwise indicated.

Univariate analysis of possible predictors of poor outcome included admission GCS score, pediatric trauma score, presence of cerebral herniation, mechanism of injury (including abusive vs nonabusive injuries), location of DAI, presence of cerebral contusion, and time to surgery. These predictors were selected a priori based on previous research suggesting that they may indicate the potential for poor outcome. Of these, two variables were moderately correlated with poor outcome: presence of cerebral herniation (correlation coefficient = 0.338, p = 0.027) and location of DAI (correlation coefficient = 0.319, p = 0.037) (Table 3). Abusive injuries were not predictive of poor outcome in this study.

TABLE 3.

Univariate analysis of possible predictors of poor outcome

Variable Correlation Coefficientp Value
Admit GCS score−0.0140.931
Pediatric trauma score−0.0880.576
Presence of herniation0.3380.027*
Mechanism of injury0.0210.894
Abusive injury vs nonabusive injuries 0.347
Location of DAI0.3190.037*
Contusion−0.2870.062
Time to surgery0.2410.185

Statistically significant (p < 0.05).

Fisher’s exact test, no correlation coefficient.

Further analysis of the location of DAI as a predictor of poor outcome showed that only brainstem DAI was significantly associated with poor outcome (p = 0.024) (Table 4). Logistic regression analysis of cerebral herniation and brainstem DAI showed that brainstem DAI had a higher OR of 22.3 (95% CI 1.62–306, p = 0.020), whereas cerebral herniation had an OR of 10.5 (95% CI 1.06–104, p = 0.044) (Table 5). Two of the 3 children who died had brainstem DAI, and 1 child had DAI in deep locations.

TABLE 4.

Location of DAI as predictor of poor outcome

Location of DAINo. of Patients (%)p Value
No DAI15 (35)0.624
Superficial9 (21)0.543
Deep14 (33)0.590
Brainstem5 (12)0.024*

Statistically significant (p < 0.05).

TABLE 5.

Binary logistic regression analysis of factors predictive of poor outcome

Variable OR95% CIp Value
Herniation 10.51.06–1040.044*
Brainstem DAI22.31.62–3060.020*

Statistically significant (p < 0.05).

Discussion

These results reveal that the use of postoperative MRI in children with severe TBI who have undergone either craniotomy or craniectomy may assist in predicting which patients will have a poor outcome. They are consistent with results of a prior study that showed that MRI signal abnormality in the brainstem predicted a poor outcome.8 Development of outcome predictors in these patients is necessary to ensure accurate family counseling and to appropriately guide postoperative management.

Many studies have examined the utility of MRI in prognostication in TBI,6,7,15,16 and several have looked specifically at the pediatric population.3,8,14 The presence of hemorrhage on SWI after pediatric head injury has been negatively correlated with intellectual and neuropsychological scores.14 A study assessing FLAIR signal in predicting outcome after pediatric TBI revealed that total FLAIR lesion volume and presence of FLAIR lesions in the brainstem were predictors of functional outcome.8 As in our study, the researchers divided the brain into three zones—superficial, deep, and brainstem—and our study confirmed their finding that the presence of lesions in the brainstem was the only predictor of poor outcome. Lesions in the superficial or deep areas were not associated with poor outcome.

Although these other pediatric TBI studies give us insight into the outcomes of patients in this treatment series, patients who present with pathology necessitating surgical intervention are unique. They typically have a mass-occupying lesion and increased intracranial pressure. The surgery itself may also impact their recovery.

Our results indicate that postoperative MRI in this population may be especially important for prognostication. However, in our initial patient identification, we found that many children (53%) who presented with severe TBI and underwent surgery never received a postoperative brain MRI. This may have occurred if the initial GCS score recorded on arrival was falsely low (e.g., patients received sedatives in transport or emergency responders had a low threshold to intubate). These patients would have been taken to the operating room urgently if a compressive hemorrhagic lesion was found on arrival and their GCS score might have improved significantly postoperatively, negating the need for MRI. In this series, we attempted to control for falsely low GCS scores by also documenting the field GCS score as documented by emergency medical services. Of those documented with field GCS scores, 90% were a GCS score of 8 or less. Another possibility is that there are wide practice variations in the providers who care for these children. Ferrazzano et al.3 surveyed 27 institutions about their use of MRI. They reported that 40% of sites in the US indicated that they obtain MRI studies in > 95% of children with severe TBI; however, international sites performed MRI less frequently. Most sites (60%) obtained an MRI within the first 7 days; the remainder of the scans were distributed throughout a 30-day postinjury period. Only 37% of the sites had a standardized MRI protocol for severe TBI.

Multiple studies have revealed the superiority of MRI to CT in assessing DAI.17,18 In our series, preoperative CT imaging demonstrated no brainstem DAI or hemorrhagic lesions that were consistent with DAI. For children with DAI in deep locations (corpus callosum, internal and external capsule, basal ganglia, and thalamus), only 5 of the 14 CT images revealed DAI or DAI-type lesions in deep locations.

Overall, the majority of pediatric patients with TBI who undergo surgery for evacuation of a hemorrhagic cerebral lesion have satisfactory outcomes.1921 Those who undergo craniectomy for decompression without evacuation of a space-occupying lesion tend to have a worse prognosis.11 One of 43 patients in this study did not have an obvious mass lesion but did have traumatic subarachnoid hemorrhage and a depressed skull fracture. Although studies suggest that a low GCS score on presentation is associated with poorer outcomes,19,21 no previous study has specifically evaluated outcomes of pediatric patients who present with severe TBI and undergo either craniectomy or craniotomy. Because of the paucity of these data, it can be difficult to counsel family members on prognosis and expectations.

Limitations

A limitation of this study is the small sample size due to the rarity of patients who undergo surgery after severe TBI and receive a postoperative MRI. Even current studies evaluating MRI for severe TBI in children that included nonoperative patients have had a similar number of or fewer patients.8,14 Another issue of debate is the appropriate MRI sequence to accurately delineate DAI-type lesions. We chose to base our evaluation of DAI-type lesions on the pediatric neuroradiologist interpretations of the study using multiple sequences. We believe this to be the most real-world and applicable way a provider would use these data to counsel family members.

Conclusions

The majority of children in this series who presented with a severe TBI and underwent craniectomy or craniotomy made a satisfactory recovery. In patients in whom there is a concern of poor outcome, the location of DAI-type lesions on SWI and FLAIR may assist in prognostication. Our results revealed that DAI-type lesions in the brainstem and evidence of cerebral herniation may indicate a poorer prognosis; however, more studies with larger cohorts are needed to draw definitive conclusions.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Bollo, Baker, Scoville. Acquisition of data: Baker, Cox, Hunsaker. Analysis and interpretation of data: Baker, Hunsaker. Drafting the article: Baker. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Bollo. Statistical analysis: Baker, Scoville. Study supervision: Bollo.

References

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Illustration from Pettersson et al. (pp 467–475).
  • 1

    Ballestero MFM, Furlanetti LL, Augusto LP, Chaves PHC, Santos MV, de Oliveira RS. Decompressive craniectomy for severe traumatic brain injury in children: analysis of long-term neuropsychological impairment and review of the literature. Childs Nerv Syst. 2019;35(9):15071515.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Faul LM, Wald CV. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002–2006. Centers for Disease Control and Prevention,. National Center for Injury Prevention and Control;2010.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Ferrazzano PA, Rosario BL, Wisniewski SR, et al. Use of magnetic resonance imaging in severe pediatric traumatic brain injury: assessment of current practice. J Neurosurg Pediatr. 2019;23(4):471479.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Liesemer K, Riva-Cambrin J, Bennett KS, et al. Use of Rotterdam CT scores for mortality risk stratification in children with traumatic brain injury. Pediatr Crit Care Med. 2014;15(6):554562.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Marquez de la Plata C, Ardelean A, Koovakkattu D, et al. Magnetic resonance imaging of diffuse axonal injury: quantitative assessment of white matter lesion volume. J Neurotrauma. 2007;24(4):591598.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Chastain CA, Oyoyo UE, Zipperman M, et al. Predicting outcomes of traumatic brain injury by imaging modality and injury distribution. J Neurotrauma. 2009;26(8):11831196.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Paterakis K, Karantanas AH, Komnos A, Volikas Z. Outcome of patients with diffuse axonal injury: the significance and prognostic value of MRI in the acute phase. J Trauma. 2000;49(6):10711075.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Smitherman E, Hernandez A, Stavinoha PL, et al. Predicting outcome after pediatric traumatic brain injury by early magnetic resonance imaging lesion location and volume. J Neurotrauma. 2016;33(1):3548.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Crouchman M, Rossiter L, Colaco T, Forsyth R. A practical outcome scale for paediatric head injury. Arch Dis Child. 2001;84(2):120124.

  • 10

    Calvert S, Miller HE, Curran A, et al. The King’s Outcome Scale for Childhood Head Injury and injury severity and outcome measures in children with traumatic brain injury. Dev Med Child Neurol. 2008;50(6):426431.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Kan P, Amini A, Hansen K, et al. Outcomes after decompressive craniectomy for severe traumatic brain injury in children. J Neurosurg. 2006;105(5)(suppl):337342.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Jang SH. Diagnostic problems in diffuse axonal injury. Diagnostics (Basel). 2020;10(2):117.

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