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Utility of Early Magnetic Resonance Imaging to Enhance Outcome Prediction in Critically Ill Children with Severe Traumatic Brain Injury

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Abstract

Background

Many children with severe traumatic brain injury (TBI) receive magnetic resonance imaging (MRI) during hospitalization. There are insufficient data on how different patterns of injury on early MRI inform outcomes.

Methods

Children (3–17 years) admitted in 2010–2021 for severe TBI (Glasgow Coma Scale [GCS] score < 9) were identified using our site’s trauma registry. We used multivariable modeling to determine whether the hemorrhagic diffuse axonal injury (DAI) grade and the number of regions with restricted diffusion (subcortical white matter, corpus callosum, deep gray matter, and brainstem) on MRI obtained within 7 days of injury were independently associated with time to follow commands and with Functional Independence Measure for Children (WeeFIM) scores at the time of discharge from inpatient rehabilitation. We controlled for the clinical variables age, preadmission cardiopulmonary resuscitation, pupil reactivity, motor GCS score, and fever (> 38 °C) in the first 12 h.

Results

Of 260 patients, 136 (52%) underwent MRI within 7 days of injury at a median of 3 days (interquartile range [IQR] 2–4). Patients with early MRI were a median age of 11 years (IQR 7–14), 8 (6%) patients received cardiopulmonary resuscitation, 19 (14%) patients had bilateral unreactive pupils, the median motor GCS score was 1 (IQR 1–4), and 82 (60%) patients had fever. Grade 3 DAI was present in 46 (34%) patients, and restricted diffusion was noted in the corpus callosum in 75 (55%) patients, deep gray matter in 29 (21%) patients, subcortical white matter in 23 (17%) patients, and the brainstem in 20 (15%) patients. After controlling for clinical variables, an increased number of regions with restricted diffusion, but not hemorrhagic DAI grade, was independently associated with longer time to follow commands (hazard ratio 0.68, 95% confidence interval 0.53–0.89) and worse WeeFIM scores (estimate β − 4.67, 95% confidence interval − 8.33 to − 1.01).

Conclusions

Regional restricted diffusion on early MRI is independently associated with short-term outcomes in children with severe TBI. Multicenter cohort studies are needed to validate these findings and elucidate the association of early MRI features with long-term outcomes in children with severe TBI.

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References

  1. Coronado VG, Xu L, Basavaraju SV, et al. Surveillance for traumatic brain injury-related deaths—United States, 1997–2007. MMWR Surveill Summ. 2011;60(5):1–32.

    PubMed  Google Scholar 

  2. Faul M, Coronado V. Epidemiology of traumatic brain injury. Handb Clin Neurol. 2015;127:3–13. https://doi.org/10.1016/B978-0-444-52892-6.00001-5.

    Article  PubMed  Google Scholar 

  3. Aitken ME, McCarthy ML, Slomine BS, et al. Family burden after traumatic brain injury in children. Pediatrics. 2009;123(1):199–206. https://doi.org/10.1542/peds.2008-0607.

    Article  PubMed  Google Scholar 

  4. Kirschen MP, Walter JK. Ethical issues in neuroprognostication after severe pediatric brain injury. Semin Pediatr Neurol. 2015;22(3):187–95. https://doi.org/10.1016/j.spen.2015.05.004.

    Article  PubMed  Google Scholar 

  5. Suskauer SJ, Huisman TA. Neuroimaging in pediatric traumatic brain injury: current and future predictors of functional outcome. Dev Disabil Res Rev. 2009;15(2):117–23. https://doi.org/10.1002/ddrr.62.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kochanek PM, Tasker RC, Carney N, et al. Guidelines for the management of pediatric severe traumatic brain injury, third edition: update of the brain trauma foundation guidelines. Pediatr Crit Care Med. 2019;20(3S Supp1 1):S1–82. https://doi.org/10.1097/PCC.0000000000001735.

    Article  PubMed  Google Scholar 

  7. 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):471–9. https://doi.org/10.3171/2018.10.PEDS18374.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Babikian T, Freier MC, Tong KA, et al. Susceptibility weighted imaging: neuropsychologic outcome and pediatric head injury. Pediatr Neurol. 2005;33(3):184–94. https://doi.org/10.1016/j.pediatrneurol.2005.03.015.

    Article  PubMed  Google Scholar 

  9. Babikian T, Tong KA, Galloway NR, Freier-Randall MC, Obenaus A, Ashwal S. Diffusion-weighted imaging predicts cognition in pediatric brain injury. Pediatr Neurol. 2009;41(6):406–12. https://doi.org/10.1016/j.pediatrneurol.2009.06.002.

    Article  PubMed  Google Scholar 

  10. Galloway NR, Tong KA, Ashwal S, Oyoyo U, Obenaus A. Diffusion-weighted imaging improves outcome prediction in pediatric traumatic brain injury. J Neurotrauma. 2008;25(10):1153–62. https://doi.org/10.1089/neu.2007.0494.

    Article  PubMed  Google Scholar 

  11. 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):35–48. https://doi.org/10.1089/neu.2014.3801.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Janas AM, Qin F, Hamilton S, et al. Diffuse axonal injury grade on early MRI is associated with worse outcome in children with moderate-severe traumatic brain injury. Neurocrit Care. 2022;36(2):492–503. https://doi.org/10.1007/s12028-021-01336-8.

    Article  PubMed  Google Scholar 

  13. Liu AY, Maldjian JA, Bagley LJ, Sinson GP, Grossman RI. Traumatic brain injury: diffusion-weighted MR imaging findings. AJNR Am J Neuroradiol. 1999;20(9):1636–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Katayama Y, Becker DP, Tamura T, Hovda DA. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg. 1990;73(6):889–900. https://doi.org/10.3171/jns.1990.73.6.0889.

    Article  CAS  PubMed  Google Scholar 

  15. Katayama Y, Becker DP, Tamura T, Ikezaki K. Early cellular swelling in experimental traumatic brain injury: a phenomenon mediated by excitatory amino acids. Acta Neurochir Suppl (Wien). 1990;51:271–3. https://doi.org/10.1007/978-3-7091-9115-6_92.

    Article  CAS  PubMed  Google Scholar 

  16. Hovda DA, Becker DP, Katayama Y. Secondary injury and acidosis. J Neurotrauma. 1992;9(Suppl 1):S47-60.

    PubMed  Google Scholar 

  17. Barzó P, Marmarou A, Fatouros P, Corwin F, Dunbar J. Magnetic resonance imaging-monitored acute blood-brain barrier changes in experimental traumatic brain injury. J Neurosurg. 1996;85(6):1113–21. https://doi.org/10.3171/jns.1996.85.6.1113.

    Article  PubMed  Google Scholar 

  18. Ewing-Cobbs L, Prasad M, Kramer L, et al. Acute neuroradiologic findings in young children with inflicted or noninflicted traumatic brain injury. Childs Nerv Syst 2000;16(1):25–33; discussion 34. https://doi.org/10.1007/s003810050006.

  19. Gentry LR. Imaging of closed head injury. Radiology. 1994;191(1):1–17. https://doi.org/10.1148/radiology.191.1.8134551.

    Article  CAS  PubMed  Google Scholar 

  20. Ahmad I. “T2 shine through effect” of vasogenic oedema on DWI. J Coll Physicians Surg Pak. 2013;23(4):311.

    PubMed  Google Scholar 

  21. Hammoud DA, Wasserman BA. Diffuse axonal injuries: pathophysiology and imaging. Neuroimaging Clin N Am. 2002;12(2):205–16. https://doi.org/10.1016/s1052-5149(02)00011-4.

    Article  PubMed  Google Scholar 

  22. Msall ME, DiGaudio K, Rogers BT, et al. The Functional Independence Measure for Children (WeeFIM). Conceptual basis and pilot use in children with developmental disabilities. Clin Pediatr (Phila). 1994;33(7):421–30. https://doi.org/10.1177/000992289403300708.

    Article  CAS  PubMed  Google Scholar 

  23. Msall ME, Tremont MR. Measuring functional status in children with genetic impairments. Am J Med Genet. 1999;89(2):62–74. https://doi.org/10.1002/(sici)1096-8628(19990625)89:2%3c62::aid-ajmg3%3e3.0.co;2-t.

    Article  CAS  PubMed  Google Scholar 

  24. Ziviani J, Ottenbacher KJ, Shephard K, Foreman S, Astbury W, Ireland P. Concurrent validity of the Functional Independence Measure for Children (WeeFIM) and the pediatric evaluation of disabilities inventory in children with developmental disabilities and acquired brain injuries. Phys Occup Ther Pediatr. 2001;21(2–3):91–101.

    CAS  PubMed  Google Scholar 

  25. Msall ME, DiGaudio K, Duffy LC, LaForest S, Braun S, Granger CV. WeeFIM. Normative sample of an instrument for tracking functional independence in children. Clin Pediatr (Phila). 1994;33(7):431–8. https://doi.org/10.1177/000992289403300709.

    Article  CAS  PubMed  Google Scholar 

  26. Calkins CM, Bensard DD, Partrick DA, Karrer FM. A critical analysis of outcome for children sustaining cardiac arrest after blunt trauma. J Pediatr Surg. 2002;37(2):180–4. https://doi.org/10.1053/jpsu.2002.30251.

    Article  PubMed  Google Scholar 

  27. Hazinski MF, Chahine AA, Holcomb GW 3rd, Morris JA Jr. Outcome of cardiovascular collapse in pediatric blunt trauma. Ann Emerg Med. 1994;23(6):1229–35. https://doi.org/10.1016/s0196-0644(94)70346-9.

    Article  CAS  PubMed  Google Scholar 

  28. Hickey RW, Cohen DM, Strausbaugh S, Dietrich AM. Pediatric patients requiring CPR in the prehospital setting. Ann Emerg Med. 1995;25(4):495–501. https://doi.org/10.1016/s0196-0644(95)70265-2.

    Article  CAS  PubMed  Google Scholar 

  29. Martin SK, Shatney CH, Sherck JP, et al. Blunt trauma patients with prehospital pulseless electrical activity (PEA): poor ending assured. J Trauma 2002;53(5):876–80; discussion 880–1. https://doi.org/10.1097/00005373-200211000-00011.

  30. Natale JE, Joseph JG, Helfaer MA, Shaffner DH. Early hyperthermia after traumatic brain injury in children: risk factors, influence on length of stay, and effect on short-term neurologic status. Crit Care Med. 2000;28(7):2608–15. https://doi.org/10.1097/00003246-200007000-00071.

    Article  CAS  PubMed  Google Scholar 

  31. Perron AD, Sing RF, Branas CC, Huynh T. Predicting survival in pediatric trauma patients receiving cardiopulmonary resuscitation in the prehospital setting. Prehosp Emerg Care. 2001;5(1):6–9. https://doi.org/10.1080/10903120190940245.

    Article  CAS  PubMed  Google Scholar 

  32. Suz P, Vavilala MS, Souter M, Muangman S, Lam AM. Clinical features of fever associated with poor outcome in severe pediatric traumatic brain injury. J Neurosurg Anesthesiol. 2006;18(1):5–10. https://doi.org/10.1097/01.ana.0000189079.26212.37.

    Article  PubMed  Google Scholar 

  33. Zwingmann J, Mehlhorn AT, Hammer T, Bayer J, Südkamp NP, Strohm PC. Survival and neurologic outcome after traumatic out-of-hospital cardiopulmonary arrest in a pediatric and adult population: a systematic review. Crit Care. 2012;16(4):R117. https://doi.org/10.1186/cc11410.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Mikkonen ED, Skrifvars MB, Reinikainen M, et al. Validation of prognostic models in intensive care unit-treated pediatric traumatic brain injury patients. J Neurosurg Pediatr. 2019. https://doi.org/10.3171/2019.4.Peds1983.

    Article  PubMed  Google Scholar 

  35. Bao L, Chen D, Ding L, Ling W, Xu F. Fever burden is an independent predictor for prognosis of traumatic brain injury. PLoS ONE. 2014;9(3): e90956. https://doi.org/10.1371/journal.pone.0090956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Li J, Jiang JY. Chinese Head Trauma Data Bank: effect of hyperthermia on the outcome of acute head trauma patients. J Neurotrauma. 2012;29(1):96–100. https://doi.org/10.1089/neu.2011.1753.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Heagerty PJ, Lumley T, Pepe MS. Time-dependent ROC curves for censored survival data and a diagnostic marker. Biometrics. 2000;56(2):337–44. https://doi.org/10.1111/j.0006-341x.2000.00337.x.

    Article  CAS  PubMed  Google Scholar 

  38. Tong KA, Ashwal S, Holshouser BA, et al. Diffuse axonal injury in children: clinical correlation with hemorrhagic lesions. Ann Neurol. 2004;56(1):36–50. https://doi.org/10.1002/ana.20123.

    Article  PubMed  Google Scholar 

  39. Zheng WB, Liu GR, Li LP, Wu RH. Prediction of recovery from a post-traumatic coma state by diffusion-weighted imaging (DWI) in patients with diffuse axonal injury. Neuroradiology. 2007;49(3):271–9. https://doi.org/10.1007/s00234-006-0187-8.

    Article  CAS  PubMed  Google Scholar 

  40. Mohamadpour M, Whitney K, Bergold PJ. The importance of therapeutic time window in the treatment of traumatic brain injury. Front Neurosci. 2019;13:07. https://doi.org/10.3389/fnins.2019.00007.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Diaz-Arrastia R, Kochanek PM, Bergold P, et al. Pharmacotherapy of traumatic brain injury: state of the science and the road forward: report of the Department of Defense Neurotrauma Pharmacology Workgroup. J Neurotrauma. 2014;31(2):135–58. https://doi.org/10.1089/neu.2013.3019.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Molteni E, Ranzini MBM, Beretta E, Modat M, Strazzer S. Individualized prognostic prediction of the long-term functional trajectory in pediatric acquired brain injury. J Pers Med. 2021. https://doi.org/10.3390/jpm11070675.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Rubin ML, Yamal JM, Chan W, Robertson CS. Prognosis of six-month glasgow outcome scale in severe traumatic brain injury using hospital admission characteristics, injury severity characteristics, and physiological monitoring during the first day post-injury. J Neurotrauma. 2019;36(16):2417–22. https://doi.org/10.1089/neu.2018.6217.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Davis KC, Slomine BS, Salorio CF, Suskauer SJ. Time to follow commands and duration of posttraumatic amnesia predict GOS-E peds scores 1 to 2 years after TBI in children requiring inpatient rehabilitation. J Head Trauma Rehabil. 2016;31(2):E39-47. https://doi.org/10.1097/htr.0000000000000159.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Lundine JP, Koterba C, Shield C, Shi J, Hoskinson KR. Predicting outcomes 2 months and 1 year after inpatient rehabilitation for youth with TBI using duration of impaired consciousness and serial cognitive assessment. J Head Trauma Rehabil. 2023;38(2):E99-e108. https://doi.org/10.1097/htr.0000000000000784.

    Article  PubMed  Google Scholar 

  46. Austin CA, Slomine BS, Dematt EJ, Salorio CF, Suskauer SJ. Time to follow commands remains the most useful injury severity variable for predicting WeeFIM® scores 1 year after paediatric TBI. Brain Inj. 2013;27(9):1056–62. https://doi.org/10.3109/02699052.2013.794964.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Slomine BS, Suskauer SJ, Nicholson R, Giacino JT. Preliminary validation of the coma recovery scale for pediatrics in typically developing young children. Brain Inj. 2019;33(13–14):1640–5. https://doi.org/10.1080/02699052.2019.1658221.

    Article  PubMed  Google Scholar 

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Funding

Analytic support was provided by the University of Colorado Section of Pediatric Critical Care. Dr. Maddux received support from the Eunice Kennedy Shriver National Institutes of Health and Human Development (K23HD096018).

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Contributions

AMJ, KRM, and ABM designed the research; KRM performed the statistical analysis; AMJ, NVS, and JMW collected data; all authors contributed to the interpretation of the data; AMJ drafted the manuscript; all authors made critical revisions to the manuscript for intellectual content; AMJ had primary responsibility for the final content; and all authors read and approved the final manuscript.

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Correspondence to Anna M. Janas.

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The authors declare that they have no conflict of interest.

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The study was approved by the Colorado Multiple Institutional Review Board (protocol #22-1376) and was conducted in accordance with institutional guidelines. Consent was not required (retrospective study).

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Janas, A.M., Miller, K.R., Stence, N.V. et al. Utility of Early Magnetic Resonance Imaging to Enhance Outcome Prediction in Critically Ill Children with Severe Traumatic Brain Injury. Neurocrit Care (2023). https://doi.org/10.1007/s12028-023-01898-9

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