Int J Sports Med 2018; 39(09): 682-687
DOI: 10.1055/s-0044-101454
Behavioural Sciences
© Georg Thieme Verlag KG Stuttgart · New York

A History of Concussion Does Not Lead to an Increase in Ocular Near Point of Convergence

Paul van Donkelaar
1   University of British Columbia, Health and Exercise Sciences, Kelowna, Canada
,
Jill Dierijck
1   University of British Columbia, Health and Exercise Sciences, Kelowna, Canada
,
Alexander Wright
2   University of British Columbia, MD/PhD Program, Kelowna, Canada
,
Jonathan Smirl
1   University of British Columbia, Health and Exercise Sciences, Kelowna, Canada
› Author Affiliations
Further Information

Publication History



accepted 11 January 2018

Publication Date:
21 June 2018 (online)

Abstract

Ocular near point of convergence (NPC) has been shown to be sensitive to the effects of concussion and subconcussive impacts. To determine if NPC is also sensitive to a previous history of concussion, male contact-sport athletes either with (n=26) or without (n=16) a history of at least one previous concussion had their NPC assessed. The results showed that participants with a history of concussion displayed NPC values (9.4±1.6 cm) indistinguishable from those with no history of concussion (8.4±2.1 cm, t-test, p=0.09). This was the case regardless of whether 1, 2, or 3 or more concussions had occurred and despite the fact participants with concussion (mean time since last concussion: 1136 days) suffered from an increased number and severity of symptoms as assessed with the SCAT 3 (3.6±2.2 vs. 2.13±1.89 symptoms, 6.1±4.1 vs. 3.19±2.99 severity, t-test, p<0.05). Taken together, these results imply that NPC may not be a suitable tool to assess the potential long-term effects of one or more concussions over a longer time frame. Future research using larger sample sizes is warranted to evaluate the potential dose-response relationship between number of prior concussions and NPC.

 
  • References

  • 1 Agarwal M, Ulmer JL, Chandra T, Klein AP, Mark LP, Mohan S. Imaging correlates of neural control of ocular movements. Eur Radiol 2016; 26: 2193-2205
  • 2 Alvarez TL, Jaswal R, Gohel S, Biswal BB. Functional activity within the frontal eye fields, posterior parietal cortex, and cerebellar vermis significantly correlates to symmetrical vergence peak velocity: an ROI-based, fMRI study of vergence training. Front Integr Neurosci 2014; 8: 50
  • 3 Amen DG, Willeumier K, Omalu B, Newberg A, Raghavendra C, Raji CA. Perfusion neuroimaging abnormalities alone distinguish National Football League players from a healthy population. J Alzheimers Dis 2016; 53: 237-241
  • 4 Brennan JH, Mitra B, Synnot A, McKenzie J, Willmott C, McIntosh AS, Maller JJ, Rosenfeld JV. Accelerometers for the assessment of concussion in male athletes: A systematic review and meta-analysis. Sports Med 2017; 47: 469-478
  • 5 Brown JA, Dalecki M, Hughes C, Macpherson AK, Sergio LE. Cognitive-motor integration deficits in young adult athletes following concussion. BMC Sports Sci Med Rehabil 2015; 7: 25
  • 6 Capo-Aponte JE, Urosevich TG, Temme LA, Tarbett AK, Sanghera NK. Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Mil Med 2012; 177: 804-813
  • 7 Churchill N, Hutchison M, Richards D, Leung G, Graham S, Schweizer TA. Brain structure and function associated with a history of sport concussion: a multi-modal magnetic resonance imaging study. J Neurotrauma 2017; 34: 765-771
  • 8 Ciuffreda KJ, Han Y, Kapoor N, Ficarra AP. Oculomotor rehabilitation for reading in acquired brain injury. NeuroRehab 2006; 21: 9-21
  • 9 Collins MW, Grindel SH, Lovell MR, Dede DE, Moser DJ, Phalin BR, Nogle S, Wasik M, Cordry D, Daugherty KM, Sears SF, Nicolette G, Indelicato P, McKeag DB. Relationship between concussion and neuropsychological performance in college football players. JAMA 1999; 282: 964-970
  • 10 Coubard OA, Kapoula Z. Dorsolateral prefrontal cortex prevents short-latency saccade and vergence: A TMS study. Cereb Cortex 2006; 16: 425-436
  • 11 Davidson TW, Tremblay F. Evidence of alterations in transcallosal inhibition as a possible long-term consequence of concussion in sports: A transcranial magnetic stimulation study. Clin Neurophysiol 2016; 127: 3364-3375
  • 12 De Beaumont L, Lassonde M, Leclerc S, Théoret H. Long-term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery 2007; 61: 329-336
  • 13 De Beaumont L, Théoret H, Mongeon D, Messier J, Leclerc S, Tremblay S, Ellemberg D, Lassonde M. Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 2009; 132: 695-708
  • 14 De Beaumont L, Tremblay S, Henry LC, Poirier J, Lassonde M, Théoret H. Motor system alterations in retired former athletes: the role of aging and concussion history. BMC Neurol 2013; 13: 109
  • 15 Decq P, Gault N, Blandeau M, Kerdraon T, Berkal M, ElHelou A, Dusfour B, Peyrin JC. Long-term consequences of recurrent sports concussion. Acta Neurochir 2016; 158: 289-300
  • 16 Fogt N, Toole AJ, Rogers DL. A review of proximal inputs to the near response. Clin Exp Optom 2016; 99: 30-38
  • 17 Gamlin PD. Subcortical neural circuits for ocular accommodation and vergence in primates. Ophthalmic Physiol Opt 1999; 19: 81-89
  • 18 Gamlin PD, Yoon K. An area for vergence eye movement in primate frontal cortex. Nature 2000; 407: 1003-1007
  • 19 Gamlin PD, Zhang Y, Clendaniel RA, Mays LE. Behavior of identified Edinger-Westphal neurons during ocular accommodation. J Neurophysiol 1984; 72: 2368-2382
  • 20 Goswami R, Dufort P, Tartaglia MC, Green RE, Crawley A, Tator CH, Wennberg R, Mikulis DJ, Keightley M, Davis KD. Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions. Brain Struct Funct 2016; 221: 1911-1925
  • 21 Guskiewicz KM, Register-Mihalik J, McCrory P, McCrea M, Johnston K, Makdissi M, Dvorák J, Davis G, Meeuwisse W. Evidence-based approach to revising the SCAT2: Introducing the SCAT3. Br J Sports Med 2013; 47: 289-293
  • 22 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 Update. Int J Sports Med 2017; 38: 1126-1131
  • 23 Hart Jr J, Kraut MA, Womack KB, Strain J, Didehbani N, Bartz E, Conover H, Mansinghani S, Lu H, Cullum CM. Neuroimaging of cognitive dysfunction and depression in aging retired National Football League players: a cross-sectional study. JAMA Neurol 2013; 70: 326-335
  • 24 Heinmiller L, Gunton KB. A review of the current practice in diagnosis and management of visual complaints associated with concussion and postconcussion syndrome. Curr Opin Ophthalmol 2016; 27: 407-412
  • 25 Huber BR, Alosco ML, Stein TD, McKee AC. Potential long-term consequences of concussive and subconcussive injury. Phys Med Rehabil Clin N Am 2016; 27: 503-511
  • 26 Hume PA, Theadom A, Lewis GN, Quarrie KL, Brown SR, Hill R, Marshall SW. A comparison of cognitive function in former rugby union players compared with former non-contact-sport players and the impact of concussion history. Sports Med 2017; 47: 1209-1220
  • 27 Hung GK, Ciuffreda KJ, Semmlow JL. Static vergence and accommodation: population norms and orthoptics effects. Doc Ophthalmol 1986; 62: 165-179
  • 28 Johnson B, Hallett M, Slobounov S. Follow-up evaluation of oculomotor performance with fMRI in the subacute phase of concussion. Neurology 2015; 85: 1163-1166
  • 29 Johnson B, Zhang K, Hallett M, Slobounov S. Functional neuroimaging of acute oculomotor deficits in concussed athletes. Brain Imaging Behav 2015; 9: 564-573
  • 30 Johnson Zhang K, Gay M, Horovitz S, Hallett M, Sebastianelli W, Slobounov S. Alteration of brain default network in subacute phase of injury in concussed individuals: Resting-state fMRI study. Neuroimage 2012; 59: 511-518
  • 31 Kapoula Z, Yang Q, Coubard O, Daunys G, Orssaud C. Role of the posterior parietal cortex in the initiation of saccades and vergence: right/left functional asymmetry. Ann N Y Acad Sci 2005; 1039: 184-197
  • 32 Kawata K, Rubin LH, Lee JH, Sim T, Takahagi M, Szwanki V, Bellamy A, Darvish K, Assari S, Henderer JD, Tierney R, Langford D. Association of football subconcussive head impacts with ocular near point of convergence. JAMA Ophthalmol 2016; 134: 763-769
  • 33 Kawata K, Tierney R, Phillips J, Jeka JJ. Effect of repetitive sub-concussive head impacts on ocular near point of convergence. Int J Sports Med 2016; 37: 405-410
  • 34 List J, Ott S, Bukowski M, Lindenberg R, Flöel A. Cognitive function and brain structure after recurrent mild traumatic brain injuries in young-to-middle-aged adults. Front Hum Neurosci 2015; 9: 228
  • 35 Little CE, Emery C, Scott SH, Meeuwisse W, Palcios-Derflingher L, Dukelow SP. Do children and adolescent ice hockey players with and without a history of concussion differ in robotic testing of sensory, motor and cognitive function?. J Neuroeng Rehab 2016; 13: 89-107
  • 36 Manley GT, Gardner AJ, Schneider KJ, Guskiewicz KM, Bailes J, Cantu RC, Castellani RJ, Turner M, Jordan BD, Randolph C, Dvořák J, Hayden KA, Tator CH, McCrory P, Iverson GL. A systematic review of potential long-term effects of sport-related concussion. Br J Sports Med 2017; 51: 969-977
  • 37 Mannix R, Meehan 3rd WP, Pascual-Leone A. Sports-related concussions – media, science and policy. Nat Rev Neurol 2016; 12: 486-490
  • 38 Moser RS, Schatz P, Jordan BD. Prolonged effects of concussion in high school athletes. Neurosurg 2005; 57: 300-306
  • 39 Mucha A, Collins MW, Elbin RJ, Furman JM, Troutman-Enseki C, DeWolf RM, Marchetti G, Kontos AP. A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: Preliminary findings. Am J Sport Med 2014; 42: 2479-2486
  • 40 Multani N, Goswami R, Khodadadi M, Ebraheem A, Davis KD, Tator CH, Wennberg R, Mikulis DJ, Ezerins L, Tartaglia MC. The association between white-matter tract abnormalities, and neuropsychiatric and cognitive symptoms in retired professional football players with multiple concussions. J Neurol 2016; 263: 1332-1341
  • 41 Orr CA, Albaugh MD, Watts R, Garavan H, Andrews T, Nickerson JP, Gonyea J, Hipko S, Zweber C, Logan K, Hudziak JJ. Neuroimaging biomarkers of a history of concussion observed in asymptomatic young athletes. J Neurotrauma 2016; 33: 803-810
  • 42 Pearce AJ, Hoy K, Rogers MA, Corp DT, Maller JJ, Drury HG, Fitzgerald PB. The long-term effects of sports concussion on retired Australian football players: a study using transcranial magnetic stimulation. J Neurotrauma 2014; 31: 1139-1145
  • 43 Pearce KL, Sufrinko A, Lau BC, Henry L, Collins MW, Kontos AP. Near point of convergence after a sport-related concussion: Measurement reliability and relationship to neurocognitive impairment and symptoms. Am J Sports Med 2015; 43: 3055-3061
  • 44 Perry DC, Sturm VE, Peterson MJ, Pieper CF, Bullock T, Boeve BF, Miller BL, Guskiewicz KM, Berger MS, Kramer JH, Welsh-Bohmer KA. Association of traumatic brain injury with subsequent neurological and psychiatric disease: A meta-analysis. J Neurosurg 2016; 124: 511-526
  • 45 Poltavski DV, Biberdorf D. Screening for lifetime concussion in athletes: Importance of oculomotor measures. Brain Inj 2014; 28: 475-485
  • 46 Rambold HA, Neumann G, Helmchen A. Vergence deficits in pontine lesions. Neurology 2004; 62: 1850-1853
  • 47 Sander T, Sprenger A, Neumann G, Machner B, Gottschalk S, Rambold H, Helmchen C. Vergence deficits in patients with cerebellar lesions. Brain 2009; 132: 103-115
  • 48 Storey EP, Master SR, Lockyer JE, Podolak OE, Grady MF, Master CL. Near point of convergence after concussion in children. Optom Vis Sci 2017; 94: 96-100
  • 49 Strain J, Didehbani N, Cullum CM, Mansinghani S, Conover H, Kraut MA, Hart Jr. J, Womack KB. Depressive symptoms and white matter dysfunction in retired NFL players with concussion history. Neurology 2013; 81: 25-32
  • 50 Strain JF, Didehbani N, Spence J, Conover H, Bartz EK, Mansinghani S, Jeroudi MK, Rao NK, Fields LM, Kraut MA, Cullum CM, Hart Jr J, Womack KB. White matter changes and confrontation naming in retired aging National Football League athletes. J Neurotrauma 2017; 34: 372-379
  • 51 Strain JF, Womack KB, Didehbani N, Spence JS, Conover H, Hart Jr J, Kraut MA, Cullum CM. Imaging correlates of memory and concussion history in retired National Football League athletes. JAMA Neurol 2015; 72: 773-780
  • 52 Terry DP, Faraco CC, Smith D, Diddams MJ, Puente AN, Miller LS. Lack of long-term fMRI differences after multiple sports-related concussions. Brain Inj 2012; 26: 1684-1696
  • 53 Tremblay S, Henry LC, Bedetti C, Larson-Dupuis C, Gagnon JF, Evans AC, Théoret H, Lassonde M, De Beaumont L. Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain 2014; 137: 2997-3011
  • 54 Ventura RE, Balcer LJ, Galetta SL. The neuro-ophthalmology of head trauma. Lancet Neurol 2014; 13: 1006-1016
  • 55 Ventura RE, Balcer LJ, Galetta SL, Rucker JC. Ocular motor assessment in concussion: current status and future directions. J Neurol Sci 2016; 361: 79-86
  • 56 Ward MK, Bolding MS, Schultz KP, Gamlin PD. Mapping the macaque superior temporal sulcus: Functional delineation of vergence and version eye-movement-related activity. J Neurosci 2015; 35: 7428-7442
  • 57 Wright MJ, Woo E, Birath JB, Siders CA, Kelly DF, Wang C, Swerdloff R, Romero E, Kernan C, Cantu RC, Guskiewicz K. An index predictive of cognitive outcome in retired professional American Football players with a history of sports concussion. J Clin Exp Neuropsychol 2016; 38: 561-571
  • 58 Yang Q, Kapoula Z. Distinct control of initiation and metrics of memory-guided saccades and vergence by the FEF: a TMS study. PLoS One 2011; 6: e20322
  • 59 Yengo-Kahn AM, Hale AT, Zalneraitis BH, Zuckerman SL, Sills AK, Solomon GS. The sport concussion assessment tool: A systematic review. Neurosurg Focus 2016; 40: E6-E6
  • 60 Zhang H, Gamlin PD. Neurons in the posterior interposed nucleus of the cerebellum related to vergence and accommodation. I. Steady-state characteristics. J Neurophysiol 1998; 79: 1255-1269
  • 61 Zhang Y, Mays LE, Gamlin PD. Characteristics of near response cells projecting to the oculomotor nucleus. J Neurophysiol 1992; 67: 944-960