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Glucose metabolism in pediatric traumatic brain injury

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Abstract

Traumatic brain injury is the number one cause of death and disability among the pediatric population in the USA. The heterogeneity of the pediatric population is reflected by both the normal cerebral maturation and the age differences in the causes of TBI, which generate unique age-related pathophysiology responses and recovery profiles. This review will address the normal changes in cerebral glucose metabolism throughout developmental phases and how TBI alters glucose metabolism. Evidence has shown that TBI disrupts the biochemical processing of glucose to energy. This brings to question, “What is the optimal substrate to manage a pediatric TBI patient?” Issues related to glycemic control and alternative substrate metabolism are addressed specifically in regard to pediatric TBI. Research into pediatric glucose metabolism after TBI is limited, and understanding these age-related differences within the pediatric population have great potential to improve support for the injured younger brain.

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References

  1. Sports-Related Concussions in Youth. Washington, D.C.: National Academies Press; 2014.

  2. Giza CC, Mink RB, Madikians A (2007) Pediatric traumatic brain injury: not just little adults. Curr Opin Crit Care. 13(2):143–152

    Article  PubMed  Google Scholar 

  3. Pinto PS, Poretti A, Meoded A, Tekes A, Huisman TAGM (2012) The unique features of traumatic brain injury in children. Review of the characteristics of the pediatric skull and brain, mechanisms of trauma, patterns of injury, complications and their imaging findings--part 1. J Neuroimaging. 22(2):e1–e17

    Article  PubMed  Google Scholar 

  4. Prins ML (2008) Cerebral metabolic adaptation and ketone metabolism after brain injury. J Cereb Blood Flow Metab. 28(1):1–16

    Article  CAS  PubMed  Google Scholar 

  5. Vannucci SJ, Simpson IA (2003) Developmental switch in brain nutrient transporter expression in the rat. Am J Physiol Endocrinol Metab. 285(5):E1127–E1134

    Article  CAS  PubMed  Google Scholar 

  6. Maher F, Vannucci S, Takeda J, Simpson IA (1992) Expression of mouse-GLUT3 and human-GLUT3 glucose transporter proteins in brain. Biochem Biophys Res Commun. 182(2):703–711

    Article  CAS  PubMed  Google Scholar 

  7. Leong SF, Clark JB (1984) Regional enzyme development in rat brain. Enzymes associated with glucose utilization. Biochem J. 218(1):131–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Nehlig A, de Vasconcelos AP, Boyet S (1988) Quantitative autoradiographic measurement of local cerebral glucose utilization in freely moving rats during postnatal development. J Neurosci. 8(7):2321–2333

    CAS  PubMed  Google Scholar 

  9. Chugani HT (1998) A critical period of brain development: studies of cerebral glucose utilization with PET. Prev Med. 27(2):184–188

    Article  CAS  PubMed  Google Scholar 

  10. Chiron C, Raynaud C, Mazière B, Zilbovicius M, Laflamme L, Masure MC et al (1992) Changes in regional cerebral blood flow during brain maturation in children and adolescents. J Nucl Med. 33(5):696–703

    CAS  PubMed  Google Scholar 

  11. Van Bogaert P, Wikler D, Damhaut P, Szliwowski HB, Goldman S (1998) Regional changes in glucose metabolism during brain development from the age of 6 years. NeuroImage. 8(1):62–68

    Article  PubMed  Google Scholar 

  12. Kim I-J, Kim S-J, Kim Y-K (2009) Age- and sex-associated changes in cerebral glucose metabolism in normal healthy subjects: statistical parametric mapping analysis of F-18 fluorodeoxyglucose brain positron emission tomography. Acta Radiol. 50(10):1169–1174

    Article  PubMed  Google Scholar 

  13. Trotta N, Archambaud F, Goldman S, Baete K, Van Laere K, Wens V et al (2016) Functional integration changes in regional brain glucose metabolism from childhood to adulthood. Hum Brain Mapp. 37(8):3017–3030

    Article  PubMed  Google Scholar 

  14. Shan ZY, Leiker AJ, Onar-Thomas A, Li Y, Feng T, Reddick WE et al (2014) Cerebral glucose metabolism on positron emission tomography of children. Hum Brain Mapp. 35(5):2297–2309

    Article  PubMed  Google Scholar 

  15. Nehlig A (1989) Pereira de Vasconcelos A, Boyet S. Postnatal changes in local cerebral blood flow measured by the quantitative autoradiographic [14C]iodoantipyrine technique in freely moving rats. J Cereb Blood Flow Metab. 9(5):579–588

    Article  CAS  PubMed  Google Scholar 

  16. Yoshizawa H, Gazes Y, Stern Y, Miyata Y, Uchiyama S (2014) Characterizing the normative profile of 18F-FDG PET brain imaging: sex difference, aging effect, and cognitive reserve. Psychiatry Res. 221(1):78–85

    Article  PubMed  Google Scholar 

  17. Baxter LR, Mazziotta JC, Phelps ME, Selin CE, Guze BH, Fairbanks L (1987) Cerebral glucose metabolic rates in normal human females versus normal males. Psychiatry Res. 21(3):237–245

    Article  PubMed  Google Scholar 

  18. Nehlig A, Porrino LJ, Crane AM, Sokoloff L (1985) Local cerebral glucose utilization in normal female rats: variations during the estrous cycle and comparison with males. J Cereb Blood Flow Metab. 5(3):393–400

    Article  CAS  PubMed  Google Scholar 

  19. Satterthwaite TD, Shinohara RT, Wolf DH, Hopson RD, Elliott MA, Vandekar SN et al (2014) Impact of puberty on the evolution of cerebral perfusion during adolescence. Proc Natl Acad Sci U S A. 111(23):8643–8648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Rodriguez G, Warkentin S, Risberg J, Rosadini G (1988) Sex differences in regional cerebral blood flow. J Cereb Blood Flow Metab. 8(6):783–789

    Article  CAS  PubMed  Google Scholar 

  21. Liu W, Lou X, Ma L. Use of 3D pseudo-continuous arterial spin labeling to characterize sex and age differences in cerebral blood flow. Neuroradiology. 2016.

  22. Yoshino A, Hovda D, Kawamata T, Katayama Y, Becker D (1991) Dynamic changes in local cerebral glucose utilization following cerebral concussion in rats: evidence of a hyper- and subsequent hypometabolic state. Br Res. 561:106–119

    Article  CAS  Google Scholar 

  23. Bergsneider M, Hovda DA, Shalmon E, Kelly DF, Vespa PM, Martin NA et al (1997) Cerebral hyperglycolysis following severe traumatic brain injury in humans: a positron emission tomography study. J Neurosurg. 86(2):241–251

    Article  CAS  PubMed  Google Scholar 

  24. Katayama Y, Becker DP, Tamura T, Hovda DA (1990) Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg. 73(6):889–900

    Article  CAS  PubMed  Google Scholar 

  25. Kawamata T, Katayama Y, Hovda DA, Yoshino A, Becker DP (1992) Administration of excitatory amino acid antagonists via microdialysis attenuates the increase in glucose utilization seen following concussive brain injury. J Cereb Blood Flow Metab. 12(1):12–24

    Article  CAS  PubMed  Google Scholar 

  26. Osteen CL, Moore AH, Prins ML, Hovda DA (2001) Age-dependency of 45calcium accumulation following lateral fluid percussion: acute and delayed patterns. J Neurotrauma. 18(2):141–162

    Article  CAS  PubMed  Google Scholar 

  27. Bergsneider M, Hovda DA, McArthur DL, Etchepare M, Huang SC, Sehati N et al (2001) Metabolic recovery following human traumatic brain injury based on FDG-PET: time course and relationship to neurological disability. The Journal of head trauma rehabilitation. 16(2):135–148

    Article  CAS  PubMed  Google Scholar 

  28. Andersen BJ, Marmarou A (1992) Post-traumatic selective stimulation of glycolysis. Brain Res. 585(1-2):184–189

    Article  CAS  PubMed  Google Scholar 

  29. Richards HK, Simac S, Piechnik S, Pickard JD (2001) Uncoupling of cerebral blood flow and metabolism after cerebral contusion in the rat. J Cereb Blood Flow Metab. 21(7):779–781

    Article  CAS  PubMed  Google Scholar 

  30. Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A (2004) Functional abnormalities in symptomatic concussed athletes: an fMRI study. NeuroImage. 22(1):68–82

    Article  PubMed  Google Scholar 

  31. O'Connell MT, Seal A, Nortje J, Al-Rawi PG, Coles JP, Fryer TD et al (2005) Glucose metabolism in traumatic brain injury: a combined microdialysis and [18F]-2-fluoro-2-deoxy-D-glucose-positron emission tomography (FDG-PET) study. Acta Neurochir Suppl. 95:165–168

    Article  PubMed  Google Scholar 

  32. Moore AH, Osteen CL, Chatziioannou AF, Hovda DA, Cherry SR (2000) Quantitative assessment of longitudinal metabolic changes in vivo after traumatic brain injury in the adult rat using FDG-microPET. J Cereb Blood Flow Metab. 20(10):1492–1501

    Article  CAS  PubMed  Google Scholar 

  33. Hovda DA, Villablanca JR, Chugani HT, Phelps ME (1996) Cerebral metabolism following neonatal or adult hemineodecortication in cats: I. Effects on glucose metabolism using [14C]2-deoxy-D-glucose autoradiography. J Cereb Blood Flow Metab. 16(1):134–146

    Article  CAS  PubMed  Google Scholar 

  34. Queen SA, Chen MJ, Feeney DM (1997) d-Amphetamine attenuates decreased cerebral glucose utilization after unilateral sensorimotor cortex contusion in rats. Brain Res. 777(1-2):42–50

    Article  CAS  PubMed  Google Scholar 

  35. Sutton RL, Hovda DA, Adelson PD, Benzel EC, Becker DP (1994) Metabolic changes following cortical contusion: relationships to edema and morphological changes. Acta Neurochir Suppl (Wien) 60:446–448

    CAS  Google Scholar 

  36. Prins ML, Hovda DA (2009) The effects of age and ketogenic diet on local cerebral metabolic rates of glucose after controlled cortical impact injury in rats. J Neurotrauma. 26(7):1083–1093

    Article  PubMed  PubMed Central  Google Scholar 

  37. Humayun MS, Presty SK, Lafrance ND, Holcomb HH, Loats H, Long DM et al (1989) Local cerebral glucose abnormalities in mild closed head injured patients with cognitive impairments. Nucl Med Commun. 10(5):335–344

    Article  CAS  PubMed  Google Scholar 

  38. Gross H, Kling A, Henry G, Herndon C, Lavretsky H (1996) Local cerebral glucose metabolism in patients with long-term behavioral and cognitive deficits following mild traumatic brain injury. J Neuropsychiatry Clin Neurosci. 8(3):324–334

    Article  CAS  PubMed  Google Scholar 

  39. Umile EM, Sandel ME, Alavi A, Terry CM, Plotkin RC (2002) Dynamic imaging in mild traumatic brain injury: support for the theory of medial temporal vulnerability. Archives of physical medicine and rehabilitation. 83(11):1506–1513

    Article  PubMed  Google Scholar 

  40. Thomas S, Prins ML, Samii M, Hovda DA (2000) Cerebral metabolic response to traumatic brain injury sustained early in development: a 2-deoxy-D-glucose autoradiographic study. J Neurotrauma. 17(8):649–665

    Article  CAS  PubMed  Google Scholar 

  41. Prins ML, Hovda DA (2001) Mapping cerebral glucose metabolism during spatial learning: interactions of development and traumatic brain injury. J Neurotrauma. 18(1):31–46

    Article  CAS  PubMed  Google Scholar 

  42. Prins ML, Alexander D, Giza CC, Hovda DA (2013) Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability. J Neurotrauma. 30(1):30–38

    Article  PubMed  PubMed Central  Google Scholar 

  43. Roberts MA, Manshadi FF, Bushnell DL, Hines ME (1995) Neurobehavioural dysfunction following mild traumatic brain injury in childhood: a case report with positive findings on positron emission tomography (PET). Brain Inj. 9(5):427–436

    Article  CAS  PubMed  Google Scholar 

  44. Worley G, Hoffman JM, Paine SS, Kalman SL, Claerhout SJ, Boyko OB et al (1995) 18-Fluorodeoxyglucose positron emission tomography in children and adolescents with traumatic brain injury. Dev Med Child Neurol. 37(3):213–220

    Article  CAS  PubMed  Google Scholar 

  45. Pappius HM (1995) Cortical hypometabolism in injured brain: new correlations with the noradrenergic and serotonergic systems and with behavioral deficits. Neurochem Res. 20(11):1311–1321

    Article  CAS  PubMed  Google Scholar 

  46. Martín A, Rojas S, Pareto D, Santalucia T, Millán O, Abasolo I et al (2009) Depressed glucose consumption at reperfusion following brain ischemia does not correlate with mitochondrial dysfunction and development of infarction: an in vivo positron emission tomography study. Curr Neurovasc Res. 6(2):82–88

    Article  PubMed  Google Scholar 

  47. Povlishock JT, Pettus EH (1996) Traumatically induced axonal damage: evidence for enduring changes in axolemmal permeability with associated cytoskeletal change. Acta Neurochir Suppl. 66:81–86

    CAS  PubMed  Google Scholar 

  48. Mac Donald CL, Dikranian K, Bayly P, Holtzman D, Brody D (2007) Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J Neurosci. 27(44):11869–11876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Campbell JN, Churn SB, Register D. Traumatic Brain Injury Causes an FK506-Sensitive Loss and an Overgrowth of Dendritic Spines in Rat Forebrain. J Neurotrauma. 2011.

  50. Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D et al (2010) A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology. 74(8):643–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Chu Z, Wilde EA, Hunter JV, McCauley SR, Bigler ED, Troyanskaya M et al (2010) Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR Am J Neuroradiol. 31(2):340–346

    Article  CAS  PubMed  Google Scholar 

  52. Okumura A, Yasokawa Y, Nakayama N, Miwa K, Shinoda J, Iwama T (2005) The clinical utility of MR diffusion tensor imaging and spatially normalized PET to evaluate traumatic brain injury patients with memory and cognitive impairments. No To Shinkei. 57(2):115–122

    PubMed  Google Scholar 

  53. Herholz K (2006) Cognitive dysfunction and emotional-behavioural changes in MS: the potential of positron emission tomography. J Neurol Sci. 245(1-2):9–13

    Article  PubMed  Google Scholar 

  54. Browne SE, Lin L, Mattsson A, Georgievska B, Isacson O (2001) Selective antibody-induced cholinergic cell and synapse loss produce sustained hippocampal and cortical hypometabolism with correlated cognitive deficits. Exp Neurol. 170(1):36–47

    Article  CAS  PubMed  Google Scholar 

  55. Vagnozzi R, Signoretti S, Tavazzi B, Floris R, Ludovici A, Marziali S et al (2008) Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes--part III. Neurosurgery 62(6):1286–1295 discussion1295–6

    PubMed  Google Scholar 

  56. Vagnozzi R, Signoretti S, Cristofori L, Alessandrini F, Floris R, Isgrò E et al (2010) Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain. 133(11):3232–3242

    Article  PubMed  Google Scholar 

  57. Vagnozzi R, Tavazzi B, Signoretti S, Amorini AM, Belli A, Cimatti M et al (2007) Temporal window of metabolic brain vulnerability to concussions: mitochondrial-related impairment--part I. Neurosurgery 61(2):379–388 discussion388–9

    Article  PubMed  Google Scholar 

  58. Tavazzi B, Vagnozzi R, Signoretti S, Amorini AM, Belli A, Cimatti M et al (2007) Temporal window of metabolic brain vulnerability to concussions: oxidative and nitrosative stresses--part II. Neurosurgery 61(2):390–395 discussion395–6

    Article  PubMed  Google Scholar 

  59. Prins ML, Hales A, Reger M, Giza CC, Hovda DA (2010) Repeat traumatic brain injury in the juvenile rat is associated with increased axonal injury and cognitive impairments. Dev Neurosci. 32(5-6):510–518

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Vagnozzi R, Tavazzi B, Signoretti S, Amorini AM, Belli A, Cimatti M et al (2007) Temporal window of metabolic brain vulnerability to concussions: mitochondrial-related impairment--part I. Neurosurgery 61(2):379–388 discussion388–9

    Article  PubMed  Google Scholar 

  61. Henry LC, Tremblay S, Boulanger Y, Ellemberg D, Lassonde M (2010) Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J Neurotrauma. 27(1):65–76

    Article  PubMed  Google Scholar 

  62. Cochran A, Scaife ER, Hansen KW, Downey EC (2003) Hyperglycemia and outcomes from pediatric traumatic brain injury. The Journal of Trauma: Injury, Infection, and Critical Care. 55(6):1035–1038

    Article  Google Scholar 

  63. Jeremitsky E, Omert LA, Dunham CM, Wilberger J, Rodriguez A (2005) The impact of hyperglycemia on patients with severe brain injury. The Journal of Trauma: Injury, Infection, and Critical Care. 58(1):47–50

    Article  CAS  Google Scholar 

  64. Salim A, Hadjizacharia P, Dubose J, Brown C, Inaba K, Chan LS et al (2009) Persistent hyperglycemia in severe traumatic brain injury: an independent predictor of outcome. Am Surg. 75(1):25–29

    PubMed  Google Scholar 

  65. van den Berghe G, Wouters P, Weekers F, Verwaest C, Bruyninckx F, Schetz M et al (2001) Intensive insulin therapy in critically ill patients. N Engl J Med. 345(19):1359–1367

    Article  PubMed  Google Scholar 

  66. Vespa P, Boonyaputthikul R, McArthur DL, Miller C, Etchepare M, Bergsneider M et al (2006) Intensive insulin therapy reduces microdialysis glucose values without altering glucose utilization or improving the lactate/pyruvate ratio after traumatic brain injury. Crit Care Med. 34(3):850–856

    Article  CAS  PubMed  Google Scholar 

  67. Buitrago Blanco MM, Prashant GN, Vespa PM (2016) Cerebral Metabolism and the Role of Glucose Control in Acute Traumatic Brain Injury. Neurosurg Clin N Am. 27(4):453–463

    Article  PubMed  Google Scholar 

  68. Melo JRT, Di Rocco F, Blanot S, Laurent-Vannier A, Reis RC, Baugnon T et al (2010) Acute hyperglycemia is a reliable outcome predictor in children with severe traumatic brain injury. Acta Neurochirurgica. 152(9):1559–1565

    Article  PubMed  Google Scholar 

  69. Smith RL, Lin JC, Adelson PD, Kochanek PM, Fink EL, Wisniewski SR et al (2012) Relationship between hyperglycemia and outcome in children with severe traumatic brain injury. Pediatr Crit Care Med. 13(1):85–91

    Article  PubMed  PubMed Central  Google Scholar 

  70. Forbes NC, Anders N (2013) Does tight glycemic control improve outcomes in pediatric patients undergoing surgery and/or those with critical illness? Int J Gen Med. 7:1–11

    Article  PubMed  PubMed Central  Google Scholar 

  71. Hirshberg E, Lacroix J, Sward K, Willson D, Morris AH (2008) Blood glucose control in critically ill adults and children: a survey on stated practice. Chest. 133(6):1328–1335

    Article  PubMed  Google Scholar 

  72. Bartnik BL, Sutton RL, Fukushima M, Harris NG, Hovda DA, Lee SM (2005) Upregulation of pentose phosphate pathway and preservation of tricarboxylic acid cycle flux after experimental brain injury. J Neurotrauma. 22(10):1052–1065

    Article  PubMed  Google Scholar 

  73. Jalloh I, Carpenter KLH, Grice P, Howe DJ, Mason A, Gallagher CN et al (2015) Glycolysis and the pentose phosphate pathway after human traumatic brain injury: microdialysis studies using 1,2-(13)C2 glucose. J Cereb Blood Flow Metab. 35(1):111–120

    Article  CAS  PubMed  Google Scholar 

  74. Prins ML. Cerebral ketone metabolism during development and injury. Epilepsy Res. 2011 18.

  75. Cosi C, Marien M (1998) Decreases in mouse brain NAD+ and ATP induced by 1-methyl-4-phenyl-1, 2,3,6- tetrahydropyridine (MPTP): prevention by the poly(ADP-ribose) polymerase inhibitor, benzamide. Brain Res. 809(1):58–67

    Article  CAS  PubMed  Google Scholar 

  76. Sheline C, Behrens M, Choi D (2000) Zinc-induced cortical neuronal death: contribution of energy failure attributable to loss of NAD+ and inhibition of glycolysis. J Neurosci. 20(9):3139–3146

    CAS  PubMed  Google Scholar 

  77. Lee SM, Wong MD, Samii A, Hovda DA (1999) Evidence for energy failure following irreversible traumatic brain injury. Ann N Y Acad Sci. 893:337–340

    Article  CAS  PubMed  Google Scholar 

  78. Deng-Bryant Y, Prins ML, Hovda DA, Harris NG (2011) Ketogenic diet prevents alterations in brain metabolism in young but not adult rats after traumatic brain injury. J Neurotrauma. 28(9):1813–1825

    Article  PubMed  PubMed Central  Google Scholar 

  79. Scafidi S, O'Brien J, Hopkins I, Robertson C, Fiskum G, McKenna M (2009) Delayed cerebral oxidative glucose metabolism after traumatic brain injury in young rats. J Neurochem. 109(Suppl 1):189–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Robertson CL, Saraswati M, Scafidi S, Fiskum G, Casey P, McKenna MC (2013) Cerebral glucose metabolism in an immature rat model of pediatric traumatic brain injury. J Neurotrauma. 30(24):2066–2072

    Article  PubMed  PubMed Central  Google Scholar 

  81. Prins ML, Fujima LS, Hovda DA (2005) Age-dependent reduction of cortical contusion volume by ketones after traumatic brain injury. J Neurosci Res. 82(3):413–420

    Article  CAS  PubMed  Google Scholar 

  82. Greco T, Hovda DA, Prins ML (2015) Adolescent TBI-induced hypopituitarism causes sexual dysfunction in adult male rats. Dev Neurobiol. 75(2):193–202

    Article  PubMed  Google Scholar 

  83. Hu Z-G, Wang H-D, Jin W, Yin H-X (2009) Ketogenic diet reduces cytochrome c release and cellular apoptosis following traumatic brain injury in juvenile rats. Ann Clin Lab Sci. 39(1):76–83

    CAS  PubMed  Google Scholar 

  84. Scafidi S, Racz J, Hazelton J, McKenna MC, Fiskum G (2010) Neuroprotection by acetyl-L-carnitine after traumatic injury to the immature rat brain. Dev Neurosci. 32(5-6):480–487

    CAS  PubMed  Google Scholar 

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The author thanks UCLA Brain Injury Research Center, Austin & Marilyn Andersson Foundation.

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Prins, M.L. Glucose metabolism in pediatric traumatic brain injury. Childs Nerv Syst 33, 1711–1718 (2017). https://doi.org/10.1007/s00381-017-3518-7

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