1,126
Views
5
CrossRef citations to date
0
Altmetric
Research Article

Long-term effects of multiple concussions on prefrontal cortex oxygenation during repeated squat-stands in retired contact sport athletes

ORCID Icon, , , , , , & show all
Pages 931-938 | Received 27 Sep 2021, Accepted 01 Aug 2022, Published online: 15 Aug 2022

References

  • Daneshvar DH, Riley DO, Nowinski CJ, McKee AC, Stern RA, Cantu RC. Long Term Consequences: effects on Normal Development Profile after Concussion. Phys Med Rehabil Clin N Am. 2011 Nov;22(4):683–700. doi:10.1016/j.pmr.2011.08.009.
  • McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE, Santini VE, Lee H-S, Kubilus CA, Stern RA, et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol. 2009 Jul 1;68(7):709–35. 10.1097/NEN.0b013e3181a9d503.
  • Omalu BI, Hamilton RL, Kamboh MI, DeKosky ST, Bailes J. Chronic traumatic encephalopathy (CTE) in a National football league player: case report and emerging medicolegal practice questions. J Forensic Nurs. 2010;6(1):40–46.doi:10.1111/j.1939-3938.2009.01064.x.
  • Bendlin BB, Ries ML, Lazar M, Alexander AL, Dempsey RJ, Rowley HA, Sherman JE, Johnson SC, et al. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. NeuroImage. 2008 Aug 15;42(2):503–14. 10.1016/j.neuroimage.2008.04.254.
  • Goswami R, Dufort P, Tartaglia MC, Green RE, Crawley A, Tator CH, et al. Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions. Brain Struct Funct. 2016 May 1;221(4):1911–25. 10.1007/s00429-015-1012-0.
  • Koerte IK, Hufschmidt J, Muehlmann M, Tripodis Y, Stamm JM, Pasternak O, Giwerc MY, Coleman MJ, Baugh CM, Fritts NG, et al. Cavum Septi Pellucidi in symptomatic former professional football players. J Neurotrauma. 2015 Sep 28;33(4):346–53. 10.1089/neu.2015.3880.
  • Tremblay S, De Beaumont L, Henry LC, Boulanger Y, Evans AC, Bourgouin P, Poirier J, Theoret H, Lassonde M, et al. Sports concussions and aging: a neuroimaging investigation. Cereb Cortex. 2013 May 1;23(5):1159–66. 10.1093/cercor/bhs102.
  • Guskiewicz KM, Marshall SW, Bailes J, McCrea M, Cantu RC, Randolph C, Jordan BD, et al. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery. 2005 Oct 1;57(4):719–26. 10.1227/01.NEU.0000175725.75780.DD.
  • Iverson GL, Echemendia RJ, LaMarre AK, Brooks BL, Gaetz MB. Possible lingering effects of multiple past concussions [Internet]. Rehabilitation Research and Practice. 2012 [Accessed 2019 Mar 11]. Available from: https://www.hindawi.com/journals/rerp/2012/316575/abs/
  • Montenigro PH, Alosco ML, Martin BM, Daneshvar DH, Mez J, Chaisson CE, Nowinski CJ, Au R, McKee AC, Cantu RC, et al. Cumulative head impact exposure predicts later-life depression, apathy, executive dysfunction, and cognitive impairment in former high school and college football players. J Neurotrauma. 2016 Mar 30;34(2):328–40. 10.1089/neu.2016.4413.
  • Len TK, Neary JP. Cerebrovascular pathophysiology following mild traumatic brain injury. Clin Physiol Funct Imaging. 2010 Mar;31(2):85–93. doi:10.1111/j.1475-097X.2010.00990.x.
  • Len TK, Neary JP, Asmundson GJG, Candow DG, Goodman DG, Bjornson B, Bhambhani YN, et al. Serial monitoring of CO2 reactivity following sport concussion using hypocapnia and hypercapnia. Brain Inj. 2013;27(3):346–53.doi:10.3109/02699052.2012.743185.
  • Giza CC, Hovda DA. The new neurometabolic cascade of concussion. Neurosurgery. 2014 Oct;75:S24–33. doi:10.1227/NEU.0000000000000505.
  • Bishop S, Dech R, Baker T, Butz M, Aravinthan K, Neary JP. Parasympathetic baroreflexes and heart rate variability during acute stage of sport concussion recovery. Brain Inj. 2017;31(2):247–59.doi:10.1080/02699052.2016.1226385.
  • Smirl JD, Wright AD, Bouilane K, Bryk K, van DP. A history of multiple concussions does not alter the transcranial Doppler-based assessment of the neurovascular coupling response. Br J Sports Med. 2017 Jun 1;51(11):A23–A23. 10.1136/bjsports-2016-097270.59.
  • Smirl JD, Wright AD, Grewal HS, Jakovac M, Bryk K, van DP. Heart rate variability reductions following a season of sub-concussive head hits are related to the magnitude of impacts experienced. Br J Sports Med. 2017 Jun 1;51(11):A30–A30. 10.1136/bjsports-2016-097270.76.
  • Wright AD, Smirl JD, Bryk K, van Donkelaar P. A prospective transcranial doppler ultrasound-based evaluation of the acute and cumulative effects of sport-related concussion on neurovascular coupling response dynamics. J Neurotrauma. 2017 Aug 4;34(22):3097–106. 10.1089/neu.2017.5020.
  • Bishop SA, Neary JP. Assessing prefrontal cortex oxygenation after sport concussion with near-infrared spectroscopy. Clin Physiol Funct Imaging. 2018;38(4):573–85.doi:10.1111/cpf.12447.
  • Mutch WAC, Ellis MJ, Ryner LN, McDonald PJ, Morissette MP, Pries P, Essig M, Mikulis DJ, Duffin J, Fisher JA, et al. Patient-Specific alterations in CO2 cerebrovascular responsiveness in acute and sub-acute sports-related concussion. Front Neurol Internet]. 2018 [cited 2018 Jul 30];9. Available from.;. https://www.frontiersin.org/articles/10.3389/fneur.2018.00023/full
  • Willer BS, Tiso MR, Haider MN, Hinds AL, Baker JG, Miecznikowski JC, Leddy JJ, et al. Evaluation of executive function and mental health in retired contact sport athletes. J Head Trauma Rehabil. 2018 Oct;33(5):E9–15. doi:10.1097/HTR.0000000000000423.
  • Golding EM, Robertson CS, Bryan RM. The consequences of traumatic brain injury on cerebral blood flow and autoregulation: a review. Clin Exp Hypertens N Y N. 1993;21(4):299–332. 1999 May. doi:10.3109/10641969909068668.
  • Bailey DM, Jones DW, Sinnott A, Brugniaux JV, New KJ, Hodson D, Marley C, Smirl J, Ogoh S, Ainslie P, et al. Impaired cerebral haemodynamic function associated with chronic traumatic brain injury in professional boxers. Clin Sci. 2013 Feb 1;124(3):177–89. 10.1042/CS20120259.
  • Smirl JD, Hoffman K, Tzeng Y-C, Hansen A, Ainslie PN. Methodological comparison of active- and passive-driven oscillations in blood pressure; implications for the assessment of cerebral pressure-flow relationships. J Appl Physiol Bethesda Md. 1985 2015 Sep 1;119(5):487–501.
  • Singh J, Teckchandani TA, Quarrie DM, Neary JP. Cerebral hemodynamic effects of 30-minute supine rest and postural changes at normoxia and hypoxia using near infrared spectroscopy. In: Biophotonics in Exercise Science, Sports Medicine, Health Monitoring Technologies, and Wearables [Internet]. International Society for Optics and Photonics, San Francisco, California, United States; 2020 [cited 2021 Sep 7]. p. 112370C. Available from: https://www.spiedigitallibrary.org/conference-proceedings-of-spie/11237/112370C/Cerebral-hemodynamic-effects-of-30-minute-supine-rest-and-postural/10.1117/12.2544509.short
  • Ferrari M, Quaresima V. A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. NeuroImage. 2012 Nov 1;63(2):921–35. 10.1016/j.neuroimage.2012.03.049.
  • Fabiani M, Low KA, Tan C-H, Zimmerman B, Fletcher MA, Schneider‐Garces N, Maclin EL, Chiarelli AM, Sutton BP, Gratton G, et al. Taking the pulse of aging: mapping pulse pressure and elasticity in cerebral arteries with optical methods. Psychophysiology. 2014;51(11):1072–88.doi:10.1111/psyp.12288.
  • Tan CH, Low KA, Kong T, Fletcher MA, Zimmerman B, Maclin EL, et al. Mapping cerebral pulse pressure and arterial compliance over the adult lifespan with optical imaging. PLoS ONE Internet]. 2017 Feb 24 [cited 2020 Feb 12];12(2). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5325189/
  • Forcione M, Colonnese C, Belli A. Cerebral hemodynamic influences in task-related functional magnetic resonance imaging and near-infrared spectroscopy in acute sport-related concussion: a review. J Imaging. 2018 Apr;4(4):59. doi:10.3390/jimaging4040059.
  • Hocke LM, Duszynski CC, Debert CT, Dleikan D, Dunn JF. Reduced functional connectivity in adults with persistent post-concussion symptoms: a functional near-infrared spectroscopy study. J Neurotrauma. 2018 Jan 26;35(11):1224–32. 10.1089/neu.2017.5365.
  • Urban KJ, Barlow KM, Jimenez JJ, Goodyear BG, Dunn JF. Functional near-infrared spectroscopy reveals reduced interhemispheric cortical communication after pediatric concussion. J Neurotrauma. 2014 Nov 11;32(11):833–40. 10.1089/neu.2014.3577.
  • Karamzadeh N, Amyot F, Kenney K, Anderson A, Chowdhry F, Dashtestani H, Wassermann EM, Chernomordik V, Boccara C, Wegman E, et al. A machine learning approach to identify functional biomarkers in human prefrontal cortex for individuals with traumatic brain injury using functional near-infrared spectroscopy. Brain Behav. 2016;6(11):e00541.doi:10.1002/brb3.541.
  • Leddy J, Hinds A, Sirica D, Willer B. The role of controlled exercise in concussion management. Pm&r. 2016 Mar 1;8(3, Supplement):S91–100. 10.1016/j.pmrj.2015.10.017.
  • Highton D, Ghosh A, Tachtsidis I, Panovska-Griffiths J, Elwell CE, Smith M. Monitoring cerebral autoregulation after brain injury: multimodal assessment of cerebral slow-wave oscillations using near-infrared spectroscopy. Anesth Analg. 2015 Jul;121(1):198–205. doi:10.1213/ANE.0000000000000790.
  • Sharma A, Hind K, Hume P, Singh J, Neary JP. Neurovascular coupling by functional near infra-red spectroscopy and sport-related concussion in retired rugby players: the UK rugby health project. Front Hum Neurosci Internet]. 2020 [cited 2020 Mar 5];14. Available from.;. https://www.frontiersin.org/articles/10.3389/fnhum.2020.00042/full
  • McCrory P, Meeuwisse W, Dvorak J, Aubry M, Bailes J, Broglio S, et al. Consensus statement on concussion in sport-the 5(th) international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017 Apr 26; doi:10.1136/bjsports-2017-097699
  • Kennedy DO, Haskell CF. Cerebral blood flow and behavioural effects of caffeine in habitual and non-habitual consumers of caffeine: a near infrared spectroscopy study. Biol Psychol. 2011 Mar 1;86(3):298–306. 10.1016/j.biopsycho.2010.12.010.
  • Neary JP, Singh J, Bishop SA, Dech RT, Butz MJA, Len TK. An evidence-based objective study protocol for evaluating cardiovascular and cerebrovascular indices following concussion: the neary protocol. Methods Protoc. 2019 Mar;2(1):23.
  • Wright AD, Smirl JD, Bryk K, Fraser S, Jakovac M, van Donkelaar P. Sport-Related concussion alters indices of dynamic cerebral autoregulation. Front Neurol. 2018;9:196.doi:10.3389/fneur.2018.00196.
  • Tzeng Y-C, Lucas SJE, Atkinson G, Willie CK, Ainslie PN. Fundamental relationships between arterial baroreflex sensitivity and dynamic cerebral autoregulation in humans. J Appl Physiol. 2010 Mar 11;108(5):1162–68. 10.1152/japplphysiol.01390.2009.
  • Kurowski BG, Hugentobler J, Quatman-Yates C, Taylor J, Gubanich PJ, Altaye M, et al. Aerobic exercise for adolescents with prolonged symptoms after mild traumatic brain injury: an exploratory randomized clinical trial. J Head Trauma Rehabil. 2017 Apr;32(2):79. doi:10.1097/HTR.0000000000000238.
  • Lang EW, Czosnyka M, Mehdorn HM. Tissue oxygen reactivity and cerebral autoregulation after severe traumatic brain injury. Crit Care Med. 2003 Jan;31(1):267–71. doi:10.1097/00003246-200301000-00042.
  • Pincus SM. Approximate entropy as a measure of system complexity. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2297–301. 10.1073/pnas.88.6.2297.
  • Zweifel C, Lavinio A, Steiner LA, Radolovich D, Smielewski P, Timofeev I, Hiler M, Balestreri M, Kirkpatrick PJ, Pickard JD, et al. Continuous monitoring of cerebrovascular pressure reactivity in patients with head injury. Neurosurg Focus. 2008 Oct;25(4):E2. doi:10.3171/FOC.2008.25.10.E2.
  • Moir ME, Balestrini CS, Abbott KC, Klassen SA, Fischer LK, Fraser DD, Shoemaker JK, et al. An investigation of dynamic cerebral autoregulation in adolescent concussion. Med Sci Sports Exerc. 2018;50(11):2192–99.doi:10.1249/MSS.0000000000001695.
  • Leenders KL, Perani D, Lammertsma AA, Heather JD, Buckingham P, Jones T, Healy MJR, Gibbs JM, WISE RJS, Hatazawa J, et al. CEREBRAL BLOOD FLOW, BLOOD VOLUME AND OXYGEN UTILIZATIONNORMAL VALUES AND EFFECT OF AGE. Brain. 1990 Feb 1;113(1):27–47. 10.1093/brain/113.1.27.
  • Wen SW, Wong CHY. Aging- and vascular-related pathologies. Microcirculation. 2019;26(2):e12463.doi:10.1111/micc.12463.
  • Huang -C-C, Sandroni P, Sletten DM, Weigand SD, Low PA. Effect of age on adrenergic and vagal baroreflex sensitivity in normal subjects. Muscle Nerve. 2007 Nov;36(5):637–42. doi:10.1002/mus.20853.
  • Fisher JP, Ahmed A, Ainslie PN, Bain AR, Wildfong KW, Morris L, et al.Effect of age on the cerebrovascular responses to the initiation of dynamic exercise. FASEB J. 2017 Apr 1;31(1_supplement):1020.6–1020.6.
  • Carey BJ, Eames PJ, Blake MJ, Panerai RB, Potter JF. Dynamic cerebral autoregulation is unaffected by aging. Stroke. 2000 Dec;31(12):2895–900. doi:10.1161/01.STR.31.12.2895.
  • Carey BJ, Panerai RB, Potter JF. Effect of aging on dynamic cerebral autoregulation during head-up tilt. Stroke. 2003 Aug;34(8):1871–75. doi:10.1161/01.STR.0000081981.99908.F3.
  • Yam AT, Lang EW, Lagopoulos J, Yip K, Griffith J, Mudaliar Y, et al. Cerebral autoregulation and ageing. J Clin Neurosci Off J Neurosurg Soc Australas. 2005 Aug;12(6):643–46.
  • Cerqueira JJ, Almeida OFX, Sousa N. The stressed prefrontal cortex. Left? Right! Brain Behav Immun. 2008 Jul 1;22(5):630–38. 10.1016/j.bbi.2008.01.005.
  • Gur RC, Reivich M. Cognitive task effects on hemispheric blood flow in humans: evidence for individual differences in hemispheric activation. Brain Lang. 1980 Jan;9(1):78–92. doi:10.1016/0093-934X(80)90073-5.
  • Halsey JH, Blauenstein UW, Wilson EM, Wills EH. Regional cerebral blood flow comparison of right and left hand movement. Neurology. 1979 Jan;29(1):21–28. doi:10.1212/WNL.29.1.21.
  • Tempest GD, Eston RG, Parfitt G, Bruce A. Prefrontal cortex haemodynamics and affective responses during exercise: a multi-channel near infrared spectroscopy study. PLoS ONE. Internet]. 2014 May 1 [cited 2020 May 6];9(5). Available from ():e95924. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4006862/
  • Weisz J, Emri M, Fent J, Lengyel Z, Márián T, Horváth G, Bogner P, Trón L, Ádám G, et al. Right prefrontal activation produced by arterial baroreceptor stimulation: a PET study. Neuroreport. 2001 Oct 29;12(15):3233–38. 10.1097/00001756-200110290-00018.
  • Kamiyama Y, Fujita Y, Fuchigami T, Kamiyama H, Takahashi S, Sakatani K. Asymmetrical changes in cerebral blood oxygenation induced by an active standing test in children with postural tachycardia syndrome. Adv Exp Med Biol. 2014;812:271–78.
  • 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 Feb 1;28(2):189–201. 10.1089/neu.2010.1430.
  • Zhavoronkova L, Moraresku S, Boldyreva G, Sharova E, Kuptsova S, Smirnov A, et al. FMRI and EEG reactions to hand motor tasks in patients with mild traumatic brain injury: left-hemispheric sensitivity to trauma. J Behav Brain Sci. 2019 May 29;9(6):273–87. 10.4236/jbbs.2019.96020.
  • Desjardins M, Drisdelle BL, Lefebvre C, Gagnon J-F, Beaumont LD, Jolicoeur P. Interhemispheric differences in P1 and N1 amplitude in EEG and MEG differ across older individuals with a concussion compared with age-matched controls. Psychophysiology. 2021;58(3):e13751.doi:10.1111/psyp.13751.
  • Solomito MJ, Reuman H, Wang DH. Sex differences in concussion: a review of brain anatomy, function, and biomechanical response to impact. Brain Inj. 2019 Jan 28;33(2):105–10. 10.1080/02699052.2018.1542507.
  • Duncan A, Meek JH, Clemence M, Elwell CE, Tyszczuk L, Cope M, Delpy D, et al. Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. Phys Med Biol. 1995 Feb;40(2):295–304. doi:10.1088/0031-9155/40/2/007.
  • Kohl M, Nolte C, Heekeren HR, Horst S, Scholz U, Obrig H, Villringer A, et al. Determination of the wavelength dependence of the differential pathlength factor from near-infrared pulse signals. Phys Med Biol. 1998 Jun;43(6):1771–82. doi:10.1088/0031-9155/43/6/028.
  • Labrecque L, Smirl JD, Brassard P. Letter to the editor: on the need of considering cardiorespiratory fitness when examining the influence of sex on dynamic cerebral autoregulation. Am J Physiol-Heart Circ Physiol. 2019 May 1;316(5):H1229–H1229. 10.1152/ajpheart.00152.2019.
  • Smirl JD, Peacock D, Wright AD, Bouliane KJ, Dierijck J, Burma JS, Kennefick M, Wallace C, van Donkelaar P; Smirl JD, Peacock D, Wright AD, Bouliane KJ, Dierijck J, Burma JS, et al. An acute bout of soccer heading subtly alters neurovascular coupling metrics. Front Neurol. 2020;11:738.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.