Pediatric sports-related concussion produces cerebral blood flow alterations

Pediatrics

Volumn 129, Issue 1, 2012, Pages 28-37

  Maugans, Todd A ^a,b   Farley, Chad ^b   Altaye, Mekibib ^a   Leach, James ^a   Cecil, Kim M ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Cerebral blood flow; Concussion; Magnetic resonance spectroscopy; MRI; Pediatrics

Indexed keywords

LACTIC ACID; N ACETYLASPARTIC ACID;

ADOLESCENT; ANGIOGRAPHY; ARTICLE; AXONAL INJURY; BRAIN CONCUSSION; CASE CONTROL STUDY; CEREBROVASCULAR ACCIDENT; CHILD; CLINICAL ARTICLE; CONFUSION; CONSCIOUSNESS DISORDER; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; HEADACHE; HUMAN; IMAGE ANALYSIS; LACTATE BLOOD LEVEL; MALE; METABOLIC DISORDER; NERVE INJURY; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHASE CONTRAST ANGIOGRAPHY; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTON NUCLEAR MAGNETIC RESONANCE; QUADRIPLEGIA; RESPONSE TIME; SCHOOL CHILD; SCORING SYSTEM; SPORT INJURY; SUSCEPTIBILITY WEIGHTED IMAGING; SYMPTOM; T1 WEIGHTED IMAGING; VOMITING;

ADOLESCENT; ATHLETIC INJURIES; BRAIN CONCUSSION; CEREBROVASCULAR CIRCULATION; CHILD; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MAGNETIC RESONANCE ANGIOGRAPHY; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROLOGIC EXAMINATION;

EID: 84855326131     PISSN: 00314005     EISSN: 10984275     Source Type: Journal    
DOI: 10.1542/peds.2011-2083     Document Type: Article

References (102)

1. Halstead ME, Walter KD; Council on Sports Medicine and Fitness. American Academy of Pediatrics. Clinical report - sport-related concussion in children and adolescents. Pediatrics. 2010;126(3):597-615
2. Cohen JS, Gioia G, Atabaki S, Teach SJ. Sports-related concussions in pediatrics. Curr Opin Pediatr. 2009;21(3):288-293
3. Guskiewicz KM, Valovich McLeod TC. Pediatric sports-related concussion. PM R. 2011;3(4):353-364
4. Lincoln AE, Caswell SV, Almquist JL, Dunn RE, Norris JB, Hinton RY. Trends in concussion incidence in high school sports: a prospective 11-year study. Am J Sports Med. 2011;39(5):958-963
5. Meehan WP, III, Mannix R. Pediatric concussions in United States emergency departments in the years 2002 to 2006. J Pediatr. 2010;157(6):889-893
6. Schatz P, Moser RS. Current issues in pediatric sports concussion. Clin Neuropsychol. 2011;Aug25(6):1042-1057
7. Wiebe DJ, Comstock RD, Nance ML. Concussion research: a public health priority. Inj Prev. 2011;17(1):69-70
8. Johnson EW, Kegel NE, Collins MW. Neuropsychological assessment of sport-related concussion. Clin Sports Med. 2011;30(1):73-88, viii-ix [viii-ix.]
9. Lau BC, Collins MW, Lovell MR. Sensitivity and specificity of subacute computerized neurocognitive testing and symptom evaluation in predicting outcomes after sportsrelated concussion. Am J Sports Med. 2011;39(6):1209-1216
10. Lovell MR, Iverson GL, Collins MW, et al. Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol. 2006;13(3):166-174 (Pubitemid 44917660)
11. McClincy MP, Lovell MR, Pardini J, Collins MW, Spore MK. Recovery from sports concussion in high school and collegiate athletes. Brain Inj. 2006;20(1):33-39 (Pubitemid 43135748)
12. Schatz P, Pardini JE, Lovell MR, Collins MW, Podell K. Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes. Arch Clin Neuropsychol. 2006;21(1):91-99 (Pubitemid 41802930)
13. Thomas DG, Collins MW, Saladino RA, Frank V, Raab J, Zuckerbraun NS. Identifying neurocognitive deficits in adolescents following concussion. Acad Emerg Med 2011;18(3):246-254
14. Van Kampen DA, Lovell MR, Pardini JE, Collins MW, Fu FH. The "value added" of neurocognitive testing after sports-related concussion. Am J Sports Med. 2006;34(10):1630-1635 (Pubitemid 44385857)
15. Ayr LK, Yeates KO, Taylor HG, Browne M. Dimensions of postconcussive symptoms in children with mild traumatic brain injuries. J Int Neuropsychol Soc. 2009;15(1):19-30
16. Broglio SP, Macciocchi SN, Ferrara MS. Neurocognitive performance of concussed athletes when symptom free. J Athl Train. 2007;42(4):504-508 (Pubitemid 351377898)
17. Moser RS, Iverson GL, Echemendia RJ, Lovell MR, Schatz P, Webbe FM, et al Neuropsychological evaluation in the diagnosis and management of sports-related concussion. Arch Clin Neuropsychol. 2007;22(8):909-916 (Pubitemid 350102026)
18. Solomon GS, Ott SD, Lovell MR. Long-term neurocognitive dysfunction in sports: what is the evidence? Clin Sports Med. 2011;30(1):165-177, x-xi [x-xi.]
19. Taylor HG, Dietrich A, Nuss K, et al. Postconcussive symptoms in children with mild traumatic brain injury. Neuropsychology. 2010;24(2):148-159
20. Cubon VA, Putukian M, Boyer C, Dettwiler A. A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J Neurotrauma. 2011;28(2):189-201
21. Lange RT, Iverson GL, Brubacher JR, Madler B, Heran MK. Diffusion tensor imaging findings are not strongly associated with postconcussional disorder 2 months following mild traumatic brain injury. [published online ahead of print June 2, 2011] J Head Trauma Rehabil. 2011.
22. Niogi SN, Mukherjee P. Diffusion tensor imaging of mild traumatic brain injury. J Head Trauma Rehabil. 2010;25(4):241-255
23. Niogi SN, Mukherjee P, Ghajar J, et al. Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am J Neuroradiol. 2008;29(5):967-973 (Pubitemid 351684976)
24. Schrader H, Mickeviciene D, Gleizniene R, et al. Magnetic resonance imaging after most common form of concussion. BMC Med Imaging. 2009;9:11
25. Mayer AR, Ling J, Mannell MV, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology. 2010;74(8):643-650
26. Giza CC, Hovda DA. The Neurometabolic Cascade of Concussion. J Athl Train. 2001;36(3):228-235 (Pubitemid 33685230)
27. Vagnozzi R, Signoretti S, Cristofori L, Alessandrini F, Floris R, Isgro E, et al Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain. 2010;133(11):3232-3242
28. Vagnozzi R, Signoretti S, Tavazzi B, Floris R, Ludovici A, Marziali S, et al. Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes-part III. Neurosurgery. 2008;62(6):1286-1295; discussion 1295-1296
29. Henry LC, Tremblay S, Boulanger Y, Ellemberg D, Lassonde M. Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J Neurotrauma. 2010;27(1):65-76
30. McCrory P, Meeuwisse W, Johnston K, et al. Consensus statement on concussion in sport - the Third International Conference on Concussion in Sport held in Zurich, November 2008. Phys Sportsmed. 2009;37(2):141-159
31. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B. 1996;111(3):209-219 (Pubitemid 126758682)
32. Cecil KM, Hills EC, Sandel ME, et al. Proton magnetic resonance spectroscopy for detection of axonal injury in the splenium of the corpus callosum of brain-injured patients. J Neurosurg. 1998;88(5):795-801 (Pubitemid 28215141)
33. Makoroff KL, Cecil KM, Care M, Ball WS Jr, Elevated lactate as an early marker of brain injury in inflicted traumatic brain injury. Pediatr Radiol. 2005;35(7):668-676 (Pubitemid 40909156)
34. Sinson G, Bagley LJ, Cecil KM, et al. Magnetization transfer imaging and proton MR spectroscopy in the evaluation of axonal injury: correlation with clinical outcome after traumatic brain injury. AJNR Am J Neuroradiol. 2001;22(1):143-151 (Pubitemid 32105367)
35. Walz NC, Cecil KM, Wade SL, Michaud LJ. Late proton magnetic resonance spectroscopy following traumatic brain injury during early childhood: relationship with neurobehavioral outcomes. J Neurotrauma. 2008;25(2):94-103 (Pubitemid 351252577)
36. Cecil KM, DelBello MP, Morey R, Strakowski SM. Frontal lobe differences in bipolar disorder as determined by proton MR spectroscopy. Bipolar Disord. 2002;4(6):357-365 (Pubitemid 36041465)
37. Cecil KM, Lenkinski RE, Gur RE, Gur RC. Proton magnetic resonance spectroscopy in the frontal and temporal lobes of neuroleptic naive patients with schizophrenia. Neuropsychopharmacology. 1999;20(2):131-140 (Pubitemid 29010372)
38. Patel NC, Cecil KM, Strakowski SM, Adler CM, DelBello MP. Neurochemical alterations in adolescent bipolar depression: a proton magnetic resonance spectroscopy pilot study of the prefrontal cortex. J Child Adolesc Psychopharmacol. 2008;18(6):623-627
39. Patel NC, DelBello MP, Cecil KM, Stanford KE, Adler CM, Strakowski SM. Temporal change in N-acetyl-aspartate concentrations in adolescents with bipolar depression treated with lithium. J Child Adolesc Psychopharmacol. 2008;18(2):132-139 (Pubitemid 351591441)
40. Meehan WP, III, d'Hemecourt P, Comstock RD. High school concussions in the 2008-2009 academic year: mechanism, symptoms, and management. Am J Sports Med. 2010;38(12):2405-2409
41. Barlow KM, Crawford S, Stevenson A, Sandhu SS, Belanger F, Dewey D. Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury. Pediatrics. 2010;126(2):e374-e381
42. Broglio SP, Eckner JT, Surma T, Kutcher JS. Post-concussion cognitive declines and symptomatology are not related to concussion biomechanics in high school football players. [published online ahead of print August 29, 2011] J Neurotrauma. 2011.
43. Broglio SP, Sosnoff JJ, Ferrara MS. The relationship of athlete-reported concussion symptoms and objective measures of neurocognitive function and postural control. Clin J Sport Med. 2009;19(5):377-382
44. McCrory P. Sports concussion and the risk of chronic neurological impairment. Clin J Sport Med. 2011;21(1):6-12
45. Ponsford J, Cameron P, Fitzgerald M, Grant M, Mikocka-Walus A. Long-term outcomes after uncomplicated mild traumatic brain injury: a comparison with trauma controls. J Neurotrauma. 2011;28(6):937-946
46. Valovich McLeod TC, Register-Mihalik JK. Clinical outcomes assessment for the management of sport-related concussion. J Sport Rehabil. 2011;20(1):46-60
47. Yeates KO. Mild traumatic brain injury and postconcussive symptoms in children and adolescents. J Int Neuropsychol Soc. 2010;16(6):953-960
48. Covassin T, Elbin RJ, III, Stiller-Ostrowski JL, Kontos AP. Immediate post-concussion assessment and cognitive testing (ImPACT) practices of sports medicine professionals. J Athl Train. 2009;44(6):639-644
49. Iverson GL, Lovell MR, Collins MW. Validity of ImPACT for measuring processing speed following sports-related concussion. J Clin Exp Neuropsychol. 2005;27(6):683-689 (Pubitemid 41663404)
50. Maerlender A, Flashman L, Kessler A, et al. Examination of the construct validity of ImPACT™ computerized test, traditional, and experimental neuropsychological meaures. Clin Neuropsychol. 2010;24(8):1309-1325
51. Covassin T, Elbin RJ, Nakayama Y. Tracking neurocognitive performance following concussion in high school athletes. Phys Sportsmed. 2010;38(4):87-93
52. Ellemberg D, Henry LC, Macciocchi SN, Guskiewicz KM, Broglio SP. Advances in sport concussion assessment: from behavioral to brain imaging measures. J Neurotrauma. 2009;26(12):2365-2382
53. Field M, Collins MW, Lovell MR, Maroon J. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr. 2003;142(5):546-553 (Pubitemid 36623566)
54. Frommer LJ, Gurka KK, Cross KM, Ingersoll CD, Comstock RD, Saliba SA. Sex differences in concussion symptoms of high school athletes. J Athl Train. 2011;46(1):76-84
55. Lee MA, Fine B. Adolescent concussions. Conn Med. 2010;74(3):149-156
56. Sabini RC, Reddy CC. Concussion management and treatment considerations in the adolescent population. Phys Sportsmed. 2010;38(1):139-146
57. Cantu RC. Chronic traumatic encephalopathy in the National Football League. Neurosurgery. 2007;61(2):223-225 (Pubitemid 47357282)
58. Gavett BE, Stern RA, McKee AC. Chronic traumatic encephalopathy: a potential late effect of sport-related concussive and subconcussive head trauma. Clin Sports Med. 2011;30(1):179-188, xi [xi.]
59. Omalu BI, Fitzsimmons RP, Hammers J, Bailes J. Chronic traumatic encephalopathy in a professional American wrestler. J Forensic Nurs. 2010;6(3):130-136
60. Watanabe T, Elovic E, Zafonte R. Chronic traumatic encephalopathy. PM R. 2010;2(7):671-675
61. Cecil KM. MR spectroscopy of metabolic disorders. Neuroimaging Clin N Am. 2006;16(1):87-116, viii
62. Cecil KM, DelBello MP, Sellars MC, Strakowski SM. Proton magnetic resonance spectroscopy of the frontal lobe and cerebellar vermis in children with a mood disorder and a familial risk for bipolar disorders. J Child Adolesc Psychopharmacol. 2003;13(4):545-555 (Pubitemid 38174244)
63. Cecil KM, Dietrich KN, Altaye M, et al. Proton magnetic resonance spectroscopy in adults with childhood lead exposure. Environ Health Perspect. 2011;119(3):403-408
64. Cecil KM, Kos RS. Magnetic resonance spectroscopy and metabolic imaging in white matter diseases and pediatric disorders. Top Magn Reson Imaging. 2006;17(4):275-293 (Pubitemid 46594177)
65. Cecil KM, Lenkinski RE. Proton MR spectroscopy in inflammatory and infectious brain disorders. Neuroimaging Clin N Am. 1998;8(4):863-880 (Pubitemid 28532522)
66. Cecil KM, Lenkinski RE, Meaney DF, McIntosh TK, Smith DH. High-field proton magnetic resonance spectroscopy of a swine model for axonal injury. J Neurochem. 1998;70(5):2038-2044 (Pubitemid 28207828)
67. Cecil KM, Lin A, Ross BD, Egelhoff JC. Methylsulfonylmethane observed by in vivo proton magnetic resonance spectroscopy in a 5-year-old child with developmental disorder: effects of dietary supplementation. J Comput Assist Tomogr. 2002;26(5):818-820 (Pubitemid 35423390)
68. Dinopoulos A, Cecil KM, Schapiro MB, et al. Brain MRI and proton MRS findings in infants and children with respiratory chain defects. Neuropediatrics. 2005;36(5):290-301 (Pubitemid 41501115)
69. Smith DH, Cecil KM, Meaney DF, et al. Magnetic resonance spectroscopy of diffuse brain trauma in the pig. J Neurotrauma. 1998;15(9):665-674 (Pubitemid 28429262)
70. Cernak I, Chang T, Ahmed FA, et al. Pathophysiological response to experimental diffuse brain trauma differs as a function of developmental age. Dev Neurosci. 2010;32(5-6):442-453
71. Botteri M, Bandera E, Minelli C, Latronico N. Cerebral blood flow thresholds for cerebral ischemia in traumatic brain injury. A systematic review. Crit Care Med. 2008;36(11):3089-3092
72. Bouma GJ, Muizelaar JP. Cerebral blood flow in severe clinical head injury. New Horiz. 1995;3(3):384-394
73. Della Corte F, Giordano A, Pennisi MA, Barelli A, Caricato A, Campioni P, et al. Quantitative cerebral blood flow and metabolism determination in the first 48 hours after severe head injury with a new dynamic SPECT device. Acta Neurochir (Wien). 1997;139(7):636-641; discussion 641-642
74. Ge Y, Patel MB, Chen Q, Grossman EJ, Zhang K, Miles L, et al Assessment of thalamic perfusion in patients with mild traumatic brain injury by true FISP arterial spin labelling MR imaging at 3T. Brain Inj. 2009;23(7):666-674
75. Hlatky R, Contant CF, Diaz-Marchan P, Valadka AB, Robertson CS. Significance of a reduced cerebral blood flow during the first 12 hours after traumatic brain injury. Neurocrit Care. 2004;1(1):69-83
76. Inoue Y, Shiozaki T, Tasaki O, et al. Changes in cerebral blood flow from the acute to the chronic phase of severe head injury. J Neurotrauma. 2005;22(12):1411-1418 (Pubitemid 43122356)
77. Isa R, Wan Adnan WA, Ghazali G, et al. Outcome of severe traumatic brain injury: comparison of three monitoring approaches. Neurosurg Focus. 2003;15(6):E1
78. Schütt S, Horn P, Roth H, et al. Bedside monitoring of cerebral blood flow by transcranial thermo-dye-dilution technique in patients suffering from severe traumatic brain injury or subarachnoid hemorrhage. J Neurotrauma. 2001;18(6):595-605 (Pubitemid 32568177)
79. van Santbrink H, Schouten JW, Steyerberg EW, Avezaat CJ, Maas AI. Serial transcranial Doppler measurements in traumatic brain injury with special focus on the early posttraumatic period. Acta Neurochir (Wien). 2002;144(11):1141-1149 (Pubitemid 35352143)
80. Zweifel C, Czosnyka M, Lavinio A, et al. A comparison study of cerebral autoregulation assessed with transcranial Doppler and cortical laser Doppler flowmetry. Neurol Res. 2010;32(4):425-428
81. Zwienenberg M, Muizelaar JP. Cerebral perfusion and blood flow in neurotrauma. Neurol Res. 2001;23(2-3):167-174 (Pubitemid 32290901)
82. Adelson PD, Srinivas R, Chang Y, Bell M, Kochanek PM. Cerebrovascular response in children following severe traumatic brain injury. Child Nerv Syst. 2011;27(9):1465-1476
83. Figaji AA, Zwane E, Fieggen AG, et al. Pressure autoregulation, intracranial pressure, and brain tissue oxygenation in children with severe traumatic brain injury. J Neurosurg Pediatr. 2009;4(5):420-428
84. Sharples PM, Stuart AG, Matthews DS, Aynsley-Green A, Eyre JA. Cerebral blood flow and metabolism in children with severe head injury. Part 1: Relation to age, Glasgow coma score, outcome, intracranial pressure, and time after injury. J Neurol Neurosurg Psychiatry. 1995;58(2):145-152
85. Vavilala MS, Muangman S, Waitayawinyu P, et al. Neurointensive care; impaired cerebral autoregulation in infants and young children early after inflicted traumatic brain injury: a preliminary report. J Neurotrauma. 2007;24(1):87-96 (Pubitemid 46214414)
86. Schramm P, Klein KU, Pape M, et al. Serial measurement of static and dynamic cerebrovascular autoregulation after brain injury. J Neurosurg Anesthesiol. 2011;23(1):41-44
87. Len TK, Neary JP. Cerebrovascular pathophysiology following mild traumatic brain injury. Clin Physiol Funct Imaging. 2011;31(2):85-93
88. Gergont A, Król-Jawień W, Weryński P, Herman-Sucharska I, Zajac A, Gleń A. Results of cerebral angiography performed after neuroradiological indications in children with CNS diseases [in Polish]. Przegl Lek. 2007;64(11):937-941
89. Nowak A, Gergont A, Steczkowska M. Assessment of cerebral blood flow after visual stimulation in children with a migraine and chronic tension-type headache - preliminary reports [in Polish]. Przegl Lek. 2008;65(11):777-782
90. Roach ES, Stump DA. Regional cerebral blood flow in childhood headache. Headache. 1989;29(6):379-383 (Pubitemid 20381948)
91. Vavilala MS, Lee LA, Boddu K, et al. Cerebral autoregulation in pediatric traumatic brain injury. Pediatr Crit Care Med. 2004;5(3):257-263
92. Chen JK, Johnston KM, Collie A, McCrory P, Ptito A. A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurol Neurosurg Psychiatry. 2007;78(11):1231-1238 (Pubitemid 350057288)
93. Gosselin N, Saluja RS, Chen JK, Bottari C, Johnston K, Ptito A. Brain functions after sports-related concussion: insights from event-related potentials and functional MRI. Phys Sportsmed. 2010;38(3):27-37
94. Slobounov SM, Zhang K, Pennell D, Ray W, Johnson B, Sebastianelli W. Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study. Exp Brain Res. 2010;202(2):341-354
95. Biagi L, Abbruzzese A, Bianchi MC, Alsop DC, Del Guerra A, Tosetti M. Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling. J Magn Reson Imaging. 2007;25(4):696-702 (Pubitemid 46516719)
96. Nesmith JD. Sports concussion in the child and adolescent athlete. J Ark Med Soc. 2010;107(6):111-114
97. Tavazzi B, Vagnozzi R, Signoretti S, et al. Temporal window of metabolic brain vulnerability to concussions: oxidative and nitrosative stresses - part II. Neurosurgery. 2007;61(2):390-395
98. Vagnozzi R, Tavazzi B, Signoretti S, Amorini AM, Belli A, Cimatti M, et al Temporal window of metabolic brain vulnerability to concussions: mitochondrialrelated impairment-part I. Neurosurgery. 2007;61(2):379-388 (Pubitemid 47357346)
99. Buzzini SR, Guskiewicz KM. Sport-related concussion in the young athlete. Curr Opin Pediatr. 2006;18(4):376-382 (Pubitemid 44258993)
100. Wetjen NM, Pichelmann MA, Atkinson JL. Second impact syndrome: concussion and second injury brain complications. J Am Coll Surg. 2010;211(4):553-557
101. Saunders RL, Harbaugh RE. The second impact in catastrophic contact-sports head trauma. JAMA. 1984;252(4):538-539 (Pubitemid 14088112)
102. Meehan WP III. Medical therapies for concussion. Clin Sports Med. 2011;30(1):115-124, ix [ix.]