Cerebral blood flow during treadmill exercise is a marker of physiological postconcussion syndrome in female athletes

Journal of Head Trauma Rehabilitation

Volumn 31, Issue 3, 2016, Pages 215-224

  Clausen, Mary ^a   Pendergast, David R ^b   Willer, Barry ^b   Leddy, John ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Carbon dioxide sensitivity; Cerebral blood flow; Exercise; Postconcussion syndrome; Ventilation

Indexed keywords

ADULT; AEROBIC EXERCISE; ARTICLE; ATHLETE; BLOOD FLOW VELOCITY; BLOOD PRESSURE; BRAIN BLOOD FLOW; CARDIORESPIRATORY FITNESS; CLINICAL ARTICLE; CONCUSSION; CONTROLLED STUDY; DISEASE EXACERBATION; END TIDAL CARBON DIOXIDE TENSION; EXERCISE INTENSITY; EXERCISE TOLERANCE; EXPIRED AIR; FEMALE; HUMAN; KINESIOTHERAPY; LUNG GAS EXCHANGE; LUNG MINUTE VOLUME; POSTCONCUSSION SYNDROME; PROSPECTIVE STUDY; RETURN TO SPORT; TRANSCRANIAL DOPPLER ULTRASONOGRAPHY; TREADMILL EXERCISE; TREADMILL TEST; YOUNG ADULT; ADOLESCENT; BRAIN CIRCULATION; BRAIN INJURY; EXERCISE TEST; LUNG FUNCTION TEST; PATHOPHYSIOLOGY; SPORT INJURY;

ADOLESCENT; ATHLETES; ATHLETIC INJURIES; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; EXERCISE TEST; EXERCISE TOLERANCE; FEMALE; HUMANS; POST-CONCUSSION SYNDROME; PROSPECTIVE STUDIES; RESPIRATORY FUNCTION TESTS; YOUNG ADULT;

EID: 84969819982     PISSN: 08859701     EISSN: 1550509X     Source Type: Journal    
DOI: 10.1097/HTR.0000000000000145     Document Type: Article

References (72)

1. McCrory P, Meeuwisse W, Aubry M, et al. Consensus statement on concussion in sport - The 4th International Conference on Concussion in Sport held in Zurich, November 2012. Clin J Sport Med. 2013;23(2):89-117.
2. Leddy JJ, Sandhu H, Sodhi V, Baker JG, Willer B. Rehabilitation of concussion and postconcussion syndrome. Sports Health. 2012;4(2):147-154.
3. World Health Organization. International Statistical Classification of Diseases and Related Health Problems. 10th ed. Geneva, Switzerland: World Health Organization; 1992.
4. Harmon KG, Drezner JA, Gammons M, et al. American Medical Society for Sports Medicine position statement: concussion in sport. Br J Sports Med. 2013;47(1):15-26.
5. Leddy JJ, Kozlowski K, Donnelly JP, Pendergast DR, Epstein LH, Willer B. A preliminary study of subsymptom threshold exercise training for refractory postconcussion syndrome. Clin J Sport Med. 2010;20(1):21-27.
6. Leddy JJ, Kozlowski K, Fung M, Pendergast DR, Willer B. Regulatory and autoregulatory physiological dysfunction as a primary characteristic of postconcussion syndrome: implications for treatment. NeuroRehabilitation. 2007;22(3):199-205.
7. Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics. 2012;129(1):28-37.
8. McAllister TW, Saykin AJ, Flashman LA, et al. Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology. 1999;53(6):1300-1308.
9. Leddy JJ, Cox JL, Baker JG, et al. Exercise treatment for postcon-cussion syndrome: a pilot study of changes in functional magnetic resonance imaging activation, physiology, and symptoms. J Head Trauma Rehabil. 2013;28(4):241-249.
10. Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A. Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage. 2004;22(1):68-82.
11. Ogoh S, Dalsgaard MK, Yoshiga CC, et al. Dynamic cerebral autoregulation during exhaustive exercise in humans. Am J Physiol Heart Circ Physiol. 2005;288(3):H1461-H1467.
12. Querido JS, Sheel AW. Regulation of cerebral blood flow during exercise. Sports Med. 2007;37(9):765-782.
13. Gall B, Parkhouse WS, Goodman D. Exercise following a sport induced concussion. Br J Sports Med. 2004;38(6):773-777.
14. Hilz MJ, DeFina PA, Anders S, et al. Frequency analysis unveils cardiac autonomic dysfunction after mild traumatic brain injury. J Neurotrauma. 2011;28(9):1727-1738.
15. Gall B, Parkhouse W, Goodman D. Heart rate variability of recently concussed athletes at rest and exercise. Med Sci Sports Exerc. 2004;36(8):1269-1274.
16. King ML, Lichtman SW, Seliger G, Ehert FA, Steinberg JS. Heart-rate variability in chronic traumatic brain injury. Brain Inj. 1997;11(6):445-453.
17. DeWitt DS, Prough DS. Traumatic cerebral vascular injury: the effects of concussive brain injury on the cerebral vasculature. J Neurotrauma. 2003;20(9):795-825.
18. Kozlowski KF, Graham J, Leddy JJ, Devinney-Boymel L, Willer BS. Exercise intolerance in individuals with postconcussion syndrome. J Athl Train. 2013;48(5):627-635.
19. Imray CH, Walsh S, Clarke T, et al. Effects of breathing air containing 3% carbon dioxide, 35% oxygen or a mixture of 3% carbon dioxide/35% oxygen on cerebral and peripheral oxygenation at 150 m and 3459 m. Clin Sci (Lond). 2003;104(3):203-210.
20. Ogoh S, Ainslie PN. Regulatory mechanisms of cerebral blood flow during exercise: new concepts. Exerc Sport Sci Rev. 2009; 37(3):123-129.
21. Levy M, Koeppen B, Stanton B, eds. Berne and Levy Principles of Physiology. 4th ed. Philadelphia, PA: Elsevier Mosby; 2006.
22. 2 sensitivity in SCUBA divers. Undersea Hyperb Med. 2006;33(6): 447-453.
23. Polak P, Leddy JJ, Dwyer MG, Willer B, Zivadinov R. Diffusion tensor imaging alterations in patients with postconcussion syndrome undergoing exercise treatment: a pilot longitudinal study. J Head Trauma Rehabil. 2015;30(2):E32-E42.
24. Covassin T, Elbin RJ. The female athlete: the role of gender in the assessment and management of sport-related concussion. Clin Sports Med. 2011;30(1):125-131, x.
25. Leddy JJ, Baker JG, Kozlowski K, Bisson L, Willer B. Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med. 2011;21(2):89-94.
26. Miyamura M, Hiruta S, Sakurai S, Ishida K, Saito M. Effects of prolonged physical training on ventilatory response to hypercap-nia. Tohoku J Exp Med. 1988;156(Suppl.):125-135.
27. Miyamura M, Ishida K. Adaptive changes in hypercapnic venti-latory response during training and detraining. Eur J Appl Physiol Occup Physiol. 1990;60(5):353-359.
28. Lovell MR, Iverson GL, Collins MW, et al. Measurement of symptoms following sports-related concussion: reliability and normative data for the postconcussion scale. Appl Neuropsychol. 2006;13(3):166-174.
29. Leddy JJ, Willer B. Use of graded exercise testing in concussion and return-to-activity management. Curr Sports Med Rep. 2013;12(6):370-376.
30. Whaley M. ACSM's Guidelines for Exercise Testing and Prescription. 7th ed. Philadelphia, PA: Lippincott Williams and Wilkins; 2005.
31. 2 in the emergency department setting. Emerg Med J. 2004;21(5):557-559.
32. 2 relationships and ventilation during rebreathing. J Appl Physiol. 1967;23(1):53-70.
33. Serrador JM, Picot PA, Rutt BK, Shoemaker JK, Bondar RL. MRI measures of middle cerebral artery diameter in conscious humans during simulated orthostasis. Stroke. 2000;31(7):1672-1678.
34. Tarasow E, Abdulwahed Saleh Ali A, Lewszuk A, Walecki J. Measurements of the middle cerebral artery in digital subtraction angiography and MR angiography. Med Sci Monit. 2007;13 (Suppl. 1):65-72.
35. Ogoh S, Ainslie PN, Miyamoto T. Onset responses of ventilation and cerebral blood flow to hypercapnia in humans: rest and exercise. J Appl Physiol. 2009;106(3):880-886.
36. Brys M, Brown CM, Marthol H, Franta R, Hilz MJ. Dynamic cerebral autoregulation remains stable during physical challenge in healthy persons. Am J Physiol Heart Circ Physiol. 2003; 285(3):H1048-H1054.
37. Fisher JP, Ogoh S, Young CN, Raven PB, Fadel PJ. Regulation of middle cerebral artery blood velocity during dynamic exercise in humans: influence of aging. J Appl Physiol. 2008;105(1):266-273.
38. Hellstrom G, Fischer-Colbrie W, Wahlgren NG, Jogestrand T. Carotid artery blood flow and middle cerebral artery blood flow velocity during physical exercise. J Appl Physiol. 1996;81(1): 413-418.
39. Hellstrom G, Wahlgren NG. Physical exercise increases middle cerebral artery blood flow velocity. Neurosurg Rev. 1993;16(2): 151-156.
40. Ogoh S, Fadel PJ, Zhang R, et al. Middle cerebral artery flow velocity and pulse pressure during dynamic exercise in humans. Am J Physiol Heart Circ Physiol. 2005;288(4):H1526-H1531.
41. Jorgensen LG, Perko G, Secher NH. Regional cerebral artery mean flow velocity and blood flow during dynamic exercise in humans. J Appl Physiol. 1992;73(5):1825-1830.
42. Jorgensen LG, Perko M, Hanel B, Schroeder TV, Secher NH. Middle cerebral artery flow velocity and blood flow during exercise and muscle ischemia in humans. J Appl Physiol. 1992;72(3):1123-1132.
43. Moraine JJ, Lamotte M, Berre J, Niset G, Leduc A, Naeije R. Relationship of middle cerebral artery blood flow velocity to intensity during dynamic exercise in normal subjects. Eur J Appl Physiol Occup Physiol. 1993;67(1):35-38.
44. Thomas SN, Schroeder T, Secher NH, Mitchell JH. Cerebral blood flow during submaximal and maximal dynamic exercise in humans. J Appl Physiol. 1989;67(2):744-748.
45. ACSM's Guidelines for Exercise Testing and Prescription. 7th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2006.
46. McConnell AK, Semple ES. Ventilatory sensitivity to carbon dioxide: the influence of exercise and athleticism. Med Sci Sports Exerc. 1996;28(6):685-691.
47. Kelley MA, Laufe MD, Millman RP, Peterson DD. Ventilatory response to hypercapnia before and after athletic training. Respir Physiol. 1984;55(3):393-400.
48. Miyamoto T, Inagaki M, Takaki H, et al. Adaptation of the respiratory controller contributes to the attenuation of exercise hyperpnea in endurance-trained athletes. Eur J Appl Physiol. 2012;112(1):237-251.
49. Katayama K, Sato Y, Morotome Y, et al. Ventilatory chemosensi-tive adaptations to intermittent hypoxic exposure with endurance training and detraining. J Appl Physiol. 1999;86(6):1805-1811.
50. 2 reactivity testing without blood pressure monitoring? Stroke. 1999;30(2): 398-401.
51. 2 at 1 ATA. Undersea Biomed Res. 1980;7(1):17-26.
52. 2 in trained underwater swimmers. J Appl Physiol. 1957;10(2):203-206.
53. Lally DA, Zechman FW, Tracy RA. Ventilatory responses to exercise in divers and nondivers. Respir Physiol. 1974;20(2):117-129.
54. 2, brainstem chemoreceptors and breathing. Prog Neurobiol. 1999;59(4):299-331.
55. 2 stress testing: a pilot study in patients with concussion. PloS one. 2014;9(7):e102181.
56. Pott F, Ray CA, Olesen HL, Ide K, Secher NH. Middle cerebral artery blood velocity, arterial diameter and muscle sympathetic nerve activity during postexercise muscle ischaemia. Acta Physiol Scand. 1997;160(1):43-47.
57. Linkis P, Jorgensen LG, Olesen HL, Madsen PL, Lassen NA, Secher NH. Dynamic exercise enhances regional cerebral artery mean flow velocity. J Appl Physiol. 1995;78(1):12-16.
58. Pott F, Knudsen L, Nowak M, Nielsen HB, Hanel B, Secher NH. Middle cerebral artery blood velocity during rowing. Acta Physiol Scand. 1997;160(3):251-255.
59. Ide K, Pott F, Van Lieshout JJ, Secher NH. Middle cerebral artery blood velocity depends on cardiac output during exercise with a large muscle mass. Acta Physiol Scand. 1998;162(1): 13-20.
60. Giller CA, Giller AM, Cooper CR, Hatab MR. Evaluation of the cerebral hemodynamic response to rhythmic handgrip. J Appl Physiol. 2000;88(6):2205-2213.
61. Nybo L, Nielsen B. Middle cerebral artery blood velocity is reduced with hyperthermia during prolonged exercise in humans. J Physiol (Lond). 2001;534(Pt 1):279-286.
62. Imray CHE, Myers SD, Pattinson KTS, et al. Effect of exercise on cerebral perfusion in humans at high altitude. J Appl Physiol. 2005;99(2):699-706.
63. Querido JS, Rupert JL, McKenzie DC, Sheel AW. Effects of intermittent hypoxia on the cerebrovascular responses to sub-maximal exercise in humans. Eur J Appl Physiol. 2009;105(3): 403-409.
64. Ide K, Horn A, Secher NH. Cerebral metabolic response to sub-maximal exercise. J Appl Physiol. 1999;87(5):1604-1608.
65. Heckmann JG, Brown CM, Cheregi M, Hilz MJ, Neundörfer B. Delayed cerebrovascular autoregulatory response to ergome-ter exercise in normotensive elderly humans. Cerebrovasc Dis. 2003;16(4):423-429.
66. Doering TJ, Resch KL, Steuernagel B, Brix J, Schneider B, Fischer GC. Passive and active exercises increase cerebral blood flow velocity in young, healthy individuals. Am J Phys Med Rehabil. 1998;77(6):490-493.
67. Engelborghs K, Haseldonckx M, Van Reempts J, et al. Impaired autoregulation of cerebral blood flow in an experimental model of traumatic brain injury. J Neurotrauma. 2000;17(8): 667-677.
68. Ter Minassian A, Dube L, Guilleux AM, Wehrmann N, Ursino M, Beydon L. Changes in intracranial pressure and cerebral autoregu-lation in patients with severe traumatic brain injury. Crit Care Med. 2002;30(7):1616-1622.
69. Toledo E, Lebel A, Becerra L, et al. The young brain and concussion: imaging as a biomarker for diagnosis and prognosis. Neurosci Biobehav Rev. 2012;36(6):1510-1531.
70. Sviri GE, Aaslid R, Douville CM, Moore A, Newell DW. Time course for autoregulation recovery following severe traumatic brain injury. J Neurosurg. 2009;111(4):695-700.
71. Carter JB, Banister EW, Blaber AP. The effect of age and gender on heart rate variability after endurance training. Med Sci Sports Exerc. 2003;35(8):1333-1340.
72. Conder RL, Conder AA. Heart rate variability interventions for concussion and rehabilitation. Front Psychol. 2014;5: 1-7.