Physiological, vestibulo-ocular and cervicogenic post-concussion disorders: An evidence-based classification system with directions for treatment

Brain Injury

Volumn 29, Issue 2, 2015, Pages 238-248

  Ellis, Michael J ^a   Leddy, John J ^b   Willer, Barry ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Concussion; Physiology; Post concussion syndrome; Treatment

Indexed keywords

AEROBIC EXERCISE; AMNESIA; ANTEROGRADE AMNESIA; ARTICLE; BRAIN CONCUSSION; BRAIN METABOLISM; CONFUSION; CONVALESCENCE; DISEASE CLASSIFICATION; DISORIENTATION; EVIDENCE BASED PRACTICE; FUNCTIONAL DISEASE; HUMAN; MANIPULATIVE MEDICINE; MEDICAL LITERATURE; MEDLINE; NEUROIMAGING; NEUROLOGIC EXAMINATION; NEUROLOGIC GAIT DISORDER; NONHUMAN; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PHYSICAL EXAMINATION; POSTCONCUSSION SYNDROME; PROPRIOCEPTION; RETROGRADE AMNESIA; SCHOOL HEALTH SERVICE; SCREENING; TRAUMATIC BRAIN INJURY; TREADMILL EXERCISE; TREADMILL TEST; CERVICAL SPINE; COMPLICATION; EVIDENCE BASED MEDICINE; EXERCISE TEST; NEUROPSYCHOLOGICAL TEST; POST-CONCUSSION SYNDROME; POSTTRAUMATIC HEADACHE; RISK FACTOR; VESTIBULAR DISEASES; VESTIBULOOCULAR REFLEX;

CERVICAL VERTEBRAE; EVIDENCE-BASED MEDICINE; EXERCISE TEST; HUMANS; NEUROPSYCHOLOGICAL TESTS; PHYSICAL EXAMINATION; POST-CONCUSSION SYNDROME; POST-TRAUMATIC HEADACHE; REFLEX, VESTIBULO-OCULAR; RISK FACTORS; VESTIBULAR DISEASES;

EID: 84921263611     PISSN: 02699052     EISSN: 1362301X     Source Type: Journal    
DOI: 10.3109/02699052.2014.965207     Document Type: Article

References (75)

1. Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: A brief overview. The Journal of Head Trauma Rehabilitation 2006;21:375-378.
2. Collins M, Lovell MR, Iverson GL, Ide T, Maroon J. Examining concussion rates and return to play in high school football players wearing newer helmet technology: A three-year prospective cohort study. Neurosurgery 2006;58:275-286; discussion 275-286.
3. Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccerrelated concussion. The American Journal of Sports Medicine 2009;37:1699-1704.
4. Iverson GL, Gaetz M, Lovell MR, Collins MW. Cumulative effects of concussion in amateur athletes. Brain Injury 2004;18:433-443.
5. Kutcher JS, Eckner JT. At-risk populations in sports-related concussion. Current Sports Medicine Reports 2010;9:16-20.
6. Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive and symptom predictors of recovery in high school athletes. Clinical Journal of Sport Medicine: Official Journal of the Canadian Academy of Sport Medicine 2009;19:216-221.
7. Leddy JJ, Kozlowski K, Donnelly JP, Pendergast DR, Epstein LH, Willer B. A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clinical Journal of Sport Medicine: Official Journal of the Canadian Academy of Sport Medicine 2010;20:21-27.
8. Sady MD, Vaughan CG, Gioia GA. School and the concussed youth: Recommendations for concussion education and management. Physical Medicine and Rehabilitation Clinics of North America 2011;22:701-719, ix.
9. Willer B, Leddy JJ. Management of concussion and post-concussion syndrome. Current Treatment Options in Neurology 2006;8:415-426.
10. McCrory P, Meeuwisse WH, Aubry M, Cantu B, Dvorak J, Echemendia RJ, Engebretsen L, Johnston K, Kutcher JS, Raftery M, et al. Consensus statement on concussion in sport: The 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine 2013;47:250-258.
11. Giza CC, Hovda DA. The Neurometabolic Cascade of Concussion. Journal of Athletic Training 2001;36:228-235.
12. Shrey DW, Griesbach GS, Giza CC. The pathophysiology of concussions in youth. Physical Medicine and Rehabilitation Clinics of North America 2011;22:577-602, vii.
13. Adelson PD, Clyde B, Kochanek PM, Wisniewski SR, Marion DW, Yonas H. Cerebrovascular response in infants and young children following severe traumatic brain injury: A preliminary report. Pediatric Neurosurgery 1997;26:200-207.
14. Adelson PD, Srinivas R, Chang Y, Bell M, Kochanek PM. Cerebrovascular response in children following severe traumatic brain injury. Child's Nervous System: ChNS: Official Journal of the International Society for Pediatric Neurosurgery 2011;27: 1465-1476.
15. McCrory P, Davis G, Makdissi M. Second impact syndrome or cerebral swelling after sporting head injury. Current Sports Medicine Reports 2012;11:21-23.
16. Halstead ME, Walter KD. American Academy of Pediatrics. Clinical report-sport-related concussion in children and adolescents. Pediatrics 2010;126:597-615.
17. Rihn JA, Anderson DT, Lamb K, Deluca PF, Bata A, Marchetto PA, Neves N, Vaccaro AR. Cervical spine injuries in American football. Sports medicine 2009;39:697-708.
18. Master CL, Gioia GA, Leddy JJ, Grady MF. Importance of 'return-to-learn' in pediatric and adolescent concussion. Pediatric Annals 2012;41:1-6.
19. Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics 2012;129:28-37.
20. King ML, Lichtman SW, Seliger G, Ehert FA, Steinberg JS. Heartrate variability in chronic traumatic brain injury. Brain Injury 1997;11:445-453.
21. Hanna-Pladdy B, Berry ZM, Bennett T, Phillips HL, Gouvier WD. Stress as a diagnostic challenge for postconcussive symptoms: Sequelae of mild traumatic brain injury or physiological stress response. The Clinical Neuropsychologist 2001;15:289-304.
22. Gall B, Parkhouse WS, Goodman D. Exercise following a sport induced concussion. British Journal of Sports Medicine 2004;38:773-777.
23. Baker JG, Freitas MS, Leddy JJ, Kozlowski KF, Willer BS. Return to full functioning after graded exercise assessment and progressive exercise treatment of postconcussion syndrome. Rehabilitation Research and Practice 2012;2012:705309.
24. Leddy JJ, Kozlowski K, Fung M, Pendergast DR, Willer B. Regulatory and autoregulatory physiological dysfunction as a primary characteristic of post concussion syndrome: Implications for treatment. NeuroRehabilitation 2007;22:199-205.
25. Leddy JJ, Sandhu H, Sodhi V, Baker JG, Willer B. Rehabilitation of Concussion and Post-concussion Syndrome. Sports Health 2012;4:147-154.
26. Carter JB, Banister EW, Blaber AP. Effect of endurance exercise on autonomic control of heart rate. Sports Medicine 2003;33:33-46.
27. 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. American Journal of Physical Medicine & Rehabilitation/Association of Academic Physiatrists 1998;77:490-493.
28. Griesbach GS, Gomez-Pinilla F, Hovda DA. The upregulation of plasticity-related proteins following TBI is disrupted with acute voluntary exercise. Brain Research 2004;1016:154-162.
29. Griesbach GS, Hovda DA, Molteni R, Wu A, Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: Brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience 2004;125:129-139.
30. Leddy JJ, Baker JG, Kozlowski K, Bisson L, Willer B. Reliability of a graded exercise test for assessing recovery from concussion. Clinical Journal of Sport Medicine: Official Journal of the Canadian Academy of Sport Medicine 2011;21:89-94.
31. Leddy JJ, Willer B. Use of graded exercise testing in concussion and return-to-activity management. Current Sports Medicine Reports 2013;12:370-376.
32. Armstrong B, McNair P, Taylor D. Head and neck position sense. Sports Medicine 2008;38:101-117.
33. Ernst A, Basta D, Seidl RO, Todt I, Scherer H, Clarke A. Management of posttraumatic vertigo. Otolaryngology-Head and Neck Surgery: Official Journal of American Academy of Otolaryngology-Head and Neck Surgery 2005;132:554-558.
34. Kapoor N, Ciuffreda KJ. Vision disturbances following traumatic brain injury. Current Treatment Options in Neurology 2002;4:271-280.
35. Kapoor N, Ciuffreda KJ, Han Y. Oculomotor rehabilitation in acquired brain injury: A case series. Archives of Physical Medicine and Rehabilitation 2004;85:1667-1678.
36. Cripps A, Livingston SC. The value of balance-assessment measurements in identifying and monitoring acute postural instability among concussed athletes. Journal of Sport Rehabilitation 2013;22:67-71.
37. Hillier SL, Hollohan V. Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. The Cochrane Database of Systematic Reviews 2007 Oct 17;(4):CD005397, 1-45.
38. Hillier SL, McDonnell M. Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. The Cochrane Database of Systematic Reviews 2011 Feb 16;(2):CD005397, 1-75.
39. Alsalaheen BA, Mucha A, Morris LO, Whitney SL, Furman JM, Camiolo-Reddy CE, Collins MW, Lovell MR, Sparto PJ. Vestibular rehabilitation for dizziness and balance disorders after concussion. Journal of Neurologic Physical Therapy: JNPT 2010;34:87-93.
40. Gottshall KR, Hoffer ME. Tracking recovery of vestibular function in individuals with blast-induced head trauma using vestibular-visual- cognitive interaction tests. Journal of Neurologic Physical Therapy: JNPT 2010;34:94-97.
41. Balaban CD, Hoffer ME, Gottshall KR. Top-down approach to vestibular compensation: Translational lessons from vestibular rehabilitation. Brain Research 2012;1482:101-111.
42. Whitney SL, Sparto PJ. Principles of vestibular physical therapy rehabilitation. NeuroRehabilitation 2011;29:157-166.
43. Whitney SL, Rossi MM. Efficacy of vestibular rehabilitation. Otolaryngologic Clinics of North America 2000;33:659-672.
44. Bhattacharyya N, Baugh RF, Orvidas L, Barrs D, Bronston LJ, Cass S, Chalian AA, Desmond AL, Earll JM, Fife TD, et al. Clinical practice guideline: Benign paroxysmal positional vertigo. Otolaryngology-Head and Neck Surgery: Official Journal of American Academy of Otolaryngology-Head and Neck Surgery 2008;139(Suppl 5):S47-S81.
45. Ciuffreda KJ, Rutner D, Kapoor N, Suchoff IB, Craig S, Han ME. Vision therapy for oculomotor dysfunctions in acquired brain injury: a retrospective analysis. Optometry 2008;79:18-22.
46. Han Y, Ciuffreda KJ, Kapoor N. Reading-related oculomotor testing and training protocols for acquired brain injury in humans. Brain research. Brain Research Protocols 2004;14:1-12.
47. Kristjansson E, Treleaven J. Sensorimotor function and dizziness in neck pain: Implications for assessment and management. The Journal of Orthopaedic and Sports Physical Therapy 2009;39:364-377.
48. Peterson BW, Goldberg J, Bilotto G, Fuller JH. Cervicocollic reflex: Its dynamic properties and interaction with vestibular reflexes. Journal of Neurophysiology 1985;54:90-109.
49. Wilson VJ, Yamagata Y, Yates BJ, Schor RH, Nonaka S. Response of vestibular neurons to head rotations in vertical planes. III. Response of vestibulocollic neurons to vestibular and neck stimulation. Journal of Neurophysiology 1990;64:1695-1703.
50. Jurgens R, Mergner T. Interaction between cervico-ocular and vestibulo-ocular reflexes in normal adults. Experimental brain research. Experimentelle Hirnforschung. Experimentation Cerebrale 1989;77:381-390.
51. Heikkila H, Astrom PG. Cervicocephalic kinesthetic sensibility in patients with whiplash injury. Scandinavian Journal Of Rehabilitation Medicine 1996;28:133-138.
52. Wenngren BI, Toolanen G, Hildingsson C. Oculomotor dysfunction in rheumatoid patients with upper cervical dislocation. Acta Otolaryngologica 1998;118:609-612.
53. Le Pera D, Graven-Nielsen T, Valeriani M, Oliviero A, Di Lazzaro V, Tonali PA, Arendt-Nielsen L. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 2001;112:1633-1641.
54. Passatore M, Roatta S. Influence of sympathetic nervous system on sensorimotor function: Whiplash associated disorders (WAD) as a model. European Journal Of Applied Physiology 2006;98:423-449.
55. Biondi DM. Cervicogenic headache: Mechanisms, evaluation, and treatment strategies. Journal of the American Osteopathic Association 2000;100:S7-S14.
56. Treleaven J, Jull G, Sterling M. Dizziness and unsteadiness following whiplash injury: Characteristic features and relationship with cervical joint position error. Journal of Rehabilitation Medicine 2003;35:36-43.
57. Chaibi A, Russell MB. Manual therapies for cervicogenic headache: A systematic review. The Journal of Headache and Pain 2012;13:351-359.
58. Miller J, Gross A, D'Sylva J, Burnie SJ, Goldsmith CH, Graham N, Haines T, Bronfort G, Hoving JL. Manual therapy and exercise for neck pain: A systematic review. Manual Therapy 2010;15:334-354.
59. Revel M, Minguet M, Gregoy P, Vaillant J, Manuel JL. Changes in cervicocephalic kinesthesia after a proprioceptive rehabilitation program in patients with neck pain: A randomized controlled study. Archives of Physical Medicine and Rehabilitation 1994;75:895-899.
60. Treleaven J. A tailored sensorimotor approach for management of whiplash associated disorders. A single case study. Manual Therapy 2010;15:206-209.
61. Strakowski SM, Adler CM, Delbello MP. Is depression simply a nonspecific response to brain injury? Current Psychiatry Reports 2013;15:386-385.
62. Hamon M, Blier P. Monoamine neurocircuitry in depression and strategies for new treatments. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2013;45:54-63.
63. Kito S, Hasegawa T, Koga Y. Cerebral blood flow ratio of the dorsolateral prefrontal cortex to the ventromedial prefrontal cortex as a potential predictor of treatment response to transcranial magnetic stimulation in depression. Brain Stimulation 2012;5:547-553.
64. Koenigs M, Grafman J. The functional neuroanatomy of depression: Distinct roles for ventromedial and dorsolateral prefrontal cortex. Behavioural Brain Research 2009;201:239-243.
65. Seel RT, Kreutzer JS, Rosenthal M, Hammond FM, Corrigan JD, Black K. Depression after traumatic brain injury: A National Institute on Disability and Rehabilitation Research Model Systems multicenter investigation. Archives of Physical Medicine and Rehabilitation 2003;84:177-184.
66. West SL. Substance use among persons with traumatic brain injury: A review. NeuroRehabilitation 2011;29:1-8.
67. Grauwmeijer E, Heijenbrok-Kal MH, Haitsma IK, Ribbers GM. A prospective study on employment outcome 3 years after moderate to severe traumatic brain injury. Archives of Physical Medicine And Rehabilitation 2012;93:993-999.
68. Tyerman A, Booth J. Family interventions after traumatic brain injury: A service example. NeuroRehabilitation 2001;16:59-66.
69. Barker-Collo S, Starkey N, Theadom A. Treatment for depression following mild traumatic brain injury in adults: A meta-analysis. Brain Injury 2013;27:1124-1133.
70. Simpson G, Tate R. Suicidality in people surviving a traumatic brain injury: Prevalence, risk factors and implications for clinical management. Brain Injury 2007;21:1335-1351.
71. Fazel S, Lichtenstein P, Grann M, Langstrom N. Risk of violent crime in individuals with epilepsy and traumatic brain injury: A 35-year Swedish population study. PLoS Medicine 2011;8:e1001150.
72. Manzoni GC, Bonavita V, Bussone G, Cortelli P, Narbone MC, Cevoli S, D'Amico D, De Simone R, Torelli P. Chronic migraine classification: Current knowledge and future perspectives. The Journal of Headache and Pain 2011;12:585-592.
73. Lucas S, Hoffman JM, Bell KR, Dikmen S. A prospective study of prevalence and characterization of headache following mild traumatic brain injury. Cephalalgia 2014;34:93-102.
74. Mihalik JP, Stump JE, Collins MW, Lovell MR, Field M, Maroon JC. Posttraumatic migraine characteristics in athletes following sports-related concussion. Neurosurgery 2005;102:850-855.
75. Damen L, Bruijn JK, Verhagen AP, Berger MY, Passchier J, Koes BW. Symptomatic treatment of migraine in children: A systematic review of medication trials. Pediatrics 2005;116:e295-e302.