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Hyperbaric oxygen therapy in children with post-concussion syndrome improves cognitive and behavioral function: a randomized controlled trial

Hadanny, Amir, Catalogna, Merav, Yaniv, Slava, Stolar, Orit, Rothstein, Lynn, Shabi, Adi, Suzin, Gil, Sasson, Efrat, Lang, Erez, Finci, Shachar, Polak, Nir, Fishlev, Gregory, Harpaz, Ruth Tock, Adler, Moran, Goldman, Ron-El, Zemel, Yonatan, Bechor, Yair, Efrati, Shai·2022·Scientific Reports

Abstract

Persistent post-concussion syndrome (PPCS) is a common and significant morbidity among children following traumatic brain injury (TBI) and the evidence for effective PPCS treatments remains limited. Recent studies have shown the beneficial effects of hyperbaric oxygen therapy (HBOT) in PPCS adult patients. This randomized, sham-control, double blind trial evaluated the effect of hyperbaric oxygen therapy (HBOT) on children (age 8–15) suffering from PPCS from mild-moderate TBI events six months to 10 years prior. Twenty-five children were randomized to receive 60 daily sessions of HBOT (n = 15) or sham (n = 10) treatments. Following HBOT, there was a significant increase in cognitive function including the general cognitive score (d = 0.598, p = 0.01), memory (d = 0.480, p = 0.02), executive function (d = 0.739, p = 0.003), PPCS symptoms including emotional score (p = 0.04, d = – 0.676), behavioral symptoms including hyperactivity (d = 0.244, p = 0.03), global executive composite score (d = 0.528, p = 0.001), planning/organizing score (d = 1.09, p = 0.007). Clinical outcomes correlated with significant improvements in brain MRI microstructural changes in the insula, supramarginal, lingual, inferior frontal and fusiform gyri. The study suggests that HBOT improves both cognitive and behavioral function, PPCS symptoms, and quality of life in pediatric PPCS patients at the chronic stage, even years after injury. Additional data is needed to optimize the protocol and to characterize the children who can benefit the most.

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  1. Barlow, K. M. et al. Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury. Pediatrics 126(2), e374–e381 (2010). · DOI · Paper page
  2. Langlois, J. A., Rutland-Brown, W. & Thomas, K. E. The incidence of traumatic brain injury among children in the United States: Differences by race. J. Head Trauma Rehabil. 20(3), 229–238 (2005). · DOI · Paper page
  3. McKinlay, A. et al. Prevalence of traumatic brain injury among children, adolescents and young adults: Prospective evidence from a birth cohort. Brain Inj. 22(2), 175–181 (2008). · DOI · Paper page
  4. Zemek, R. L. & Yeates, K. O. Rates of persistent postconcussive symptoms. JAMA 317(13), 1375–1376 (2017). · DOI
  5. Ganesalingam, K. et al. Family burden and parental distress following mild traumatic brain injury in children and its relationship to post-concussive symptoms. J. Pediatr. Psychol. 33(6), 621–629 (2008). · DOI
  6. Novak, Z. et al. Association of persistent postconcussion symptoms with pediatric quality of life. JAMA Pediatr. 170(12), e162900 (2016). · DOI
  7. Fried, E. et al. Persistent post-concussive syndrome in children after mild traumatic brain injury is prevalent and vastly underdiagnosed. Sci. Rep. 12(1), 4364 (2022). · DOI · Paper page
  8. Leddy, J. J. et al. Early subthreshold aerobic exercise for sport-related concussion: A randomized clinical trial. JAMA Pediatr. 173(4), 319–325 (2019). · DOI · Paper page
  9. Leddy, J. J. et al. Early targeted heart rate aerobic exercise versus placebo stretching for sport-related concussion in adolescents: A randomised controlled trial. Lancet Child Adolesc. Health. 5(11), 792–799 (2021). · DOI
  10. Barlow, K. M. Postconcussion syndrome: A review. J. Child. Neurol. 31(1), 57–67 (2016). · DOI
  11. Schneider, K. J. et al. Cervicovestibular rehabilitation in sport-related concussion: A randomised controlled trial. Br. J. Sports Med. 48(17), 1294–1298 (2014). · DOI · Paper page
  12. Leddy, J. J. et al. Exercise treatment for postconcussion syndrome: a pilot study of changes in functional magnetic resonance imaging activation, physiology, and symptoms. J. Head Trauma Rehabil. 28(4), 241–249 (2013). · DOI
  13. Gagnon, I., Galli, C., Friedman, D., Grilli, L. & Iverson, G. L. Active rehabilitation for children who are slow to recover following sport-related concussion. Brain Inj. 23(12), 956–964 (2009). · DOI
  14. Barlow, K. M. et al. Efficacy of melatonin in children with postconcussive symptoms: A randomized clinical trial. Pediatrics 145(4), 1 (2020). · DOI
  15. Hadanny, A. & Efrati, S. The hyperoxic-hypoxic paradox. Biomolecules 10(6), 1 (2020). · DOI · Paper page
  16. Efrati, S. & Ben-Jacob, E. Reflections on the neurotherapeutic effects of hyperbaric oxygen. Expert Rev. Neurother. 14(3), 233–236 (2014). · DOI
  17. Tal, S., Hadanny, A., Sasson, E., Suzin, G. & Efrati, S. Hyperbaric oxygen therapy can induce angiogenesis and regeneration of nerve fibers in traumatic brain injury patients. Front. Hum. Neurosci. 11, 508 (2017). · DOI · Paper page
  18. Boussi-Gross, R. et al. Hyperbaric oxygen therapy can improve post concussion syndrome years after mild traumatic brain injury—randomized prospective trial. PLoS ONE 8(11), e79995 (2013). · DOI · Paper page
  19. Hadanny, A., Abbott, S., Suzin, G., Bechor, Y. & Efrati, S. Effect of hyperbaric oxygen therapy on chronic neurocognitive deficits of post-traumatic brain injury patients: Retrospective analysis. BMJ Open 8(9), e023387 (2018). · DOI · Paper page
  20. Gottfried, I., Schottlender, N. & Ashery, U. Hyperbaric oxygen treatment-from mechanisms to cognitive improvement. Biomolecules 11(10), 1 (2021). · DOI
  21. Weaver, L. K. et al. Hyperbaric oxygen for post-concussive symptoms in United States military service members: A randomized clinical trial. Undersea Hyperb Med. 45(2), 129–156 (2018). · DOI
  22. Harch, P. G. et al. Hyperbaric oxygen therapy for mild traumatic brain injury persistent postconcussion syndrome: A randomized controlled trial. Med. Gas. Res. 10(1), 8–20 (2020). · DOI
  23. McAllister, T. W., Flashman, L. A., McDonald, B. C. & Saykin, A. J. Mechanisms of working memory dysfunction after mild and moderate TBI: Evidence from functional MRI and neurogenetics. J. Neurotrauma. 23(10), 1450–1467 (2006). · DOI · Paper page
  24. Kumar, S., Rao, S. L., Chandramouli, B. A. & Pillai, S. Reduced contribution of executive functions in impaired working memory performance in mild traumatic brain injury patients. Clin. Neurol. Neurosurg. 115(8), 1326–1332 (2013). · DOI
  25. Toledo, E. et al. The young brain and concussion: Imaging as a biomarker for diagnosis and prognosis. Neurosci. Biobehav. Rev. 36(6), 1510–1531 (2012). · DOI
  26. Muscara, F., Catroppa, C. & Anderson, V. The impact of injury severity on executive function 7–10 years following pediatric traumatic brain injury. Dev. Neuropsychol. 33(5), 623–636 (2008). · DOI
  27. Wilkinson, A. A. et al. Brain biomarkers and pre-injury cognition are associated with long-term cognitive outcome in children with traumatic brain injury. BMC Pediatr. 17(1), 173 (2017). · DOI
  28. Yeates, K. O. et al. Long-term attention problems in children with traumatic brain injury. J. Am. Acad. Child Adolesc. Psychiatry. 44(6), 574–584 (2005). · DOI
  29. Gerring, J. P. et al. Premorbid prevalence of ADHD and development of secondary ADHD after closed head injury. J. Am. Acad. Child. Adolesc. Psychiatry. 37(6), 647–654 (1998). · DOI
  30. Copay, A. G., Subach, B. R., Glassman, S. D., Polly, D. W. Jr. & Schuler, T. C. Understanding the minimum clinically important difference: A review of concepts and methods. Spine J. 7(5), 541–546 (2007). · DOI · Paper page
  31. Mortaheb, S. et al. Neurophysiological biomarkers of persistent post-concussive symptoms: A scoping review. Front. Neurol. 12, 687197 (2021). · DOI
  32. Killgore, W. D. S. et al. Gray matter volume and executive functioning correlate with time since injury following mild traumatic brain injury. Neurosci Lett. 612, 238–244 (2016). · DOI
  33. Smits, M. et al. Postconcussion syndrome after minor head injury: Brain activation of working memory and attention. Hum. Brain Mapp. 30(9), 2789–2803 (2009). · DOI
  34. hadanny A, Meir O, Bechor Y, Fishlev G, Bergan J, Efrati S,. The safety of hyperbaric oxygen treatment—retrospective analysis in 2334 patients. Undersea Hyperb. Med. 43(2), 113–122 (2016).
  35. Barlow, K. M. et al. Efficacy of melatonin for sleep disturbance in children with persistent post-concussion symptoms: secondary analysis of a randomized controlled trial. J. Neurotrauma. 38(8), 950–959 (2021). · DOI
  36. Tomfohr-Madsen, L. et al. A pilot randomized controlled trial of cognitive-behavioral therapy for insomnia in adolescents with persistent postconcussion symptoms. J. Head Trauma Rehabil. 35(2), E103–E112 (2020). · DOI
  37. Teel, E., Brossard-Racine, M., Corbin-Berrigan, L. A. & Gagnon, I. Perceptual cognitive training does not improve clinical outcomes at 4 and 12 weeks following concussion in children and adolescents: A randomized controlled trial. J. Head Trauma Rehabil. 36(2), E97–E107 (2021). · DOI · Paper page
  38. Quinn de Launay, K., Cheung, S. T., Riggs, L., Reed, N. & Beal, D. S. The effect of transcranial direct current stimulation on cognitive performance in youth with persistent cognitive symptoms following concussion: a controlled pilot study. Brain Inj. 36(1), 39–51 (2022). · DOI
  39. McCarty, C. A. et al. Collaborative care for adolescents with persistent postconcussive symptoms: A randomized trial. Pediatrics 138(4), 1 (2016). · DOI
  40. Cifu, D. X. et al. Effects of hyperbaric oxygen on eye tracking abnormalities in males after mild traumatic brain injury. J. Rehabil. Res. Dev. 51(7), 1047–1056 (2014). · DOI
  41. Cifu, D. X., Hart, B. B., West, S. L., Walker, W. & Carne, W. The effect of hyperbaric oxygen on persistent postconcussion symptoms. J. Head Trauma Rehabil. 29(1), 11–20 (2014). · DOI
  42. Miller, R. S. et al. Effects of hyperbaric oxygen on symptoms and quality of life among service members with persistent postconcussion symptoms: A randomized clinical trial. JAMA Intern. Med. 175(1), 43–52 (2015). · DOI
  43. Mu, J. et al. Delayed hyperbaric oxygen therapy induces cell proliferation through stabilization of cAMP responsive element binding protein in the rat model of MCAo-induced ischemic brain injury. Neurobiol. Dis. 51, 133–143 (2013). · DOI
  44. Yang, Y. J. et al. Hyperbaric oxygen induces endogenous neural stem cells to proliferate and differentiate in hypoxic-ischemic brain damage in neonatal rats. J. Undersea Hyperbaric Med. Soc. 35(2), 113–129 (2008).
  45. Chang, C. C. et al. Damage of white matter tract correlated with neuropsychological deficits in carbon monoxide intoxication after hyperbaric oxygen therapy. J. Neurotrauma 26(8), 1263–1270 (2009). · DOI
  46. Vilela, D. S., Lazarini, P. R. & Da Silva, C. F. Effects of hyperbaric oxygen therapy on facial nerve regeneration. Acta Otolaryngol. 128(9), 1048–1052 (2008). · doi:10.1080/00016480701827525
  47. Haapaniemi, T., Nylander, G., Kanje, M. & Dahlin, L. Hyperbaric oxygen treatment enhances regeneration of the rat sciatic nerve. Exp. Neurol. 149(2), 433–438 (1998). · doi:10.1006/exnr.1997.6745
  48. Bradshaw, P. O., Nelson, A. G., Fanton, J. W., Yates, T. & Kagan-Hallet, K. S. Effect of hyperbaric oxygenation on peripheral nerve regeneration in adult male rabbits. Undersea Hyperbaric Med. J. Undersea Hyperbaric Med. Soc. 23(2), 107–113 (1996).
  49. Mukoyama, M., Iida, M. & Sobue, I. Hyperbaric oxygen therapy for peripheral nerve damage induced in rabbits with clioquinol. Exp. Neurol. 47(3), 371–380 (1975). · doi:10.1016/0014-4886(75)90070-9
  50. Zhang, J. H., Lo, T., Mychaskiw, G. & Colohan, A. Mechanisms of hyperbaric oxygen and neuroprotection in stroke. Pathophysiology 12(1), 63–77 (2005). · DOI
  51. Calvert, J. W., Cahill, J. & Zhang, J. H. Hyperbaric oxygen and cerebral physiology. Neurol. Res. 29(2), 132–141 (2007). · DOI
  52. Chen, J. et al. Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ. Res. 92(6), 692–699 (2003). · DOI · Paper page
  53. Jiang, Q. et al. Investigation of neural progenitor cell induced angiogenesis after embolic stroke in rat using MRI. Neuroimage 28(3), 698–707 (2005). · DOI
  54. Tal, S. et al. Hyperbaric oxygen may induce angiogenesis in patients suffering from prolonged post-concussion syndrome due to traumatic brain injury. Restor. Neurol. Neurosci. 33(6), 943–951 (2015).
  55. Espy, K. A. & Cwik, M. F. The development of a trial making test in young children: The TRAILS-P. Clin. Neuropsychol. 18(3), 411–422 (2004). · DOI
  56. Grizzle, R. Wechsler intelligence scale for children, Fourth Edition. In Encyclopedia of child behavior and development (eds Goldstein, S. & Naglieri, J. A.) 1553–1555 (Springer, US, 2011). · DOI
  57. Ritchie, D. & Nierenberg, B. Test of Memory and Learning. In Encyclopedia of child behavior and development (eds Goldstein, S. & Naglieri, J. A.) 1479–1480 (Springer, US, 2011). · doi:10.1007/978-0-387-79061-9_2894
  58. Markel-Fox, S. & Hooper, S. R. The Rey auditory-verbal learning test (RAVLT): Preliminary normative data for children ages 6 to 12. Arch. Clin. Neuropsychol. 7(4), 347 (1992). · doi:10.1093/arclin/7.4.347
  59. Tucha, L., Aschenbrenner, S., Koerts, J. & Lange, K. W. The five-point test: Reliability, validity and normative data for children and adults. PLoS ONE 7(9), e46080 (2012). · DOI
  60. Iverson, G. L. & Lange, R. T. Examination of “postconcussion-like” symptoms in a healthy sample. Appl. Neuropsychol. 10(3), 137–144 (2003). · DOI · Paper page
  61. Sady, M. D., Vaughan, C. G. & Gioia, G. A. Psychometric characteristics of the postconcussion symptom inventory in children and adolescents. Arch. Clin. Neuropsychol. 29(4), 348–363 (2014). · DOI · Paper page
  62. Levant, R. F., Wimer, D. J. & Williams, C. M. An evaluation of the Health Behavior Inventory-20 (HBI-20) and its relationships to masculinity and attitudes towards seeking psychological help among college men. Psychol. Men Masculin. 12(1), 26–41 (2011). · DOI · Paper page
  63. Desai, A. D. et al. Validity and responsiveness of the pediatric quality of life inventory (PedsQL) 4.0 generic core scales in the pediatric inpatient setting. JAMA Pediatr. 168(12), 1114–1121 (2014). · DOI
  64. Jayadevappa, R., Cook, R. & Chhatre, S. Minimal important difference to infer changes in health-related quality of life-a systematic review. J. Clin. Epidemiol. 89, 188–198 (2017). · DOI
  65. Conners, C., & Pitkanen, J. Rzepa SJEoCNNY, NY: Springer. Conners 3rd edition (conners 3; conners 2008). 675–678 (2011). · DOI
  66. Conners, C. K., Sitarenios, G., Parker, J. D. & Epstein, J. N. The revised Conners’ Parent Rating Scale (CPRS-R): Factor structure, reliability, and criterion validity. J. Abnorm. Child Psychol. 26(4), 257–268 (1998). · DOI · Paper page
  67. Mueller, F., Brozovich, R., & Johnson, C.B. Conners' rating scales-revised (CRS-R). 24(1–4), 83–97 (1999). · DOI
  68. Bell, D. R., Guskiewicz, K. M., Clark, M. A. & Padua, D. A. Systematic review of the balance error scoring system. Sports Health. 3(3), 287–295 (2011). · doi:10.1177/1941738111403122
  69. Tristán-Vega, A. & Aja-Fernández, S. DWI filtering using joint information for DTI and HARDI. Med. Image Anal. 14(2), 205–218 (2010). · DOI
  70. Dwolatzky, T. et al. Validity of a novel computerized cognitive battery for mild cognitive impairment. BMC Geriatr. 3(1), 4 (2003). · DOI · Paper page

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Metadata

Authors
Hadanny, A., Catalogna, M., Yaniv, S., Stolar, O., Rothstein, L., Shabi, A., Suzin, G., Sasson, E., Lang, E., Finci, S., Polak, N., Fishlev, G., Harpaz, R. T., Adler, M., Goldman, R.-E., Zemel, Y., Bechor, Y., & Efrati, S.
Venue
Scientific Reports
Published
2022-09-23
Volume
12
Issue
1
ISSN
2045-2322
Cited by
25
References
6
Language
en
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