Abstract
Exposure to explosive blasts places one at risk for traumatic brain injury, especially for special weapons and tactics (SWAT) and military personnel, who may be repeatedly exposed to blasts. In the current study, the effectiveness of a jugular vein compression collar to prevent alterations in resting-state electrocortical activity following a single-SWAT breacher training session was investigated. SWAT team personnel were randomly assigned to wear a compression collar during breacher training and resting state electroencephalography (EEG) was measured within 2 days prior to and two after breacher training. It was hypothesized that significant changes in brain dynamics—indicative of possible underlying neurodegenerative processes—would follow blast exposure for those who did not wear the collar, with ameliorated changes for the collar-wearing group. Using recurrence quantification analysis (RQA) it was found that participants who did not wear the collar displayed longer periods of laminar electrocortical behavior (as indexed by RQA’s vertical max line measure) after breacher training. It is proposed that the blast wave exposure for the no-collar group may have reduced the number of pathways, via axonal disruption—for electrical transmission—resulting in the EEG signals becoming trapped in laminar states for longer periods of time. Longer laminar states have been associated with other electrocortical pathologies, such as seizure, and may be important for understanding head trauma and recovery.
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Notes
Each SWAT group consisted of a mix of tactical, precision rifle, K-9, medical, explosive and command personnel.
References
Bai Y, Xia X, Li X (2017) A review of resting-state electroencephalography analysis in disorders of consciousness. Front Neurol 8:471
Barkhoudarian G, Hovda DA, Giza CC (2011) The molecular pathophysiology of concussive brain injury. Clin Sports Med 30:33–48
Bassingthwaighte JB, Liebovitch LS, West BJ (1994) Intraorgan flow heterogeneities. Fractal physiology. Springer, Berlin, pp 236–262
Bayly P, Cohen T, Leister E, Ajo D, Leuthardt E, Genin G (2005) Deformation of the human brain induced by mild acceleration. J Neurotrauma 22:845–856
Becker K, Schneider G, Eder M, Ranft A, Kochs EF, Zieglgänsberger W, Dodt H-U (2010) Anaesthesia monitoring by recurrence quantification analysis of EEG data. PLoS One 5:e8876
Benson BW, Hamilton GM, Meeuwisse WH, McCrory P, Dvorak J (2009) Is protective equipment useful in preventing concussion? A systematic review of the literature. Br J Sports Med 43:i56–i67
Blumbergs PC, Jones NR, North JB (1989) Diffuse axonal injury in head trauma. J Neurol Neurosurg Psychiatry 52:838–841
Buzsaki G (2006) Rhythms of the brain. Oxford University Press, Oxford
Carr W, Polejaeva E, Grome A, Crandall B, LaValle C, Eonta SE, Young LA (2015) Relation of repeated low-level blast exposure with symptomology similar to concussion. J Head Trauma Rehabil 30:47–55
Carr W et al (2016) Repeated low-level blast exposure: a descriptive human subjects study. Mil Med 181:28–39
Carrubba S, Minagar A, Chesson AL, Frilot C, Marino AA (2012) Increased determinism in brain electrical activity occurs in association with multiple sclerosis. Neurol Res 34:286–290
Center TDaVBI (2018a) DoD numbers for traumatic brain injury worldwide—totals: 2000–2017
Center TDaVBI (2018b) DoD numbers for traumatic brain injury worldwide—totals: 2017 (Q1–Q4)
Chandler CDW (2006) Blast-related ear injury in current US military operations role of audiology on the interdisciplinary team. ASHA Leader 11:8–29
Chen YC, Huang W (2011) Non-impact, blast-induced mild TBI and PTSD: concepts and caveats. Brain Inj 25:641–650
Chen XH, Johnson VE, Uryu K, Trojanowski JQ, Smith DH (2009a) A lack of amyloid β plaques despite persistent accumulation of amyloid β in axons of long-term survivors of traumatic brain injury. Brain Pathol 19:214–223
Chen YC, Smith DH, Meaney DF (2009b) In-vitro approaches for studying blast-induced traumatic brain injury. J Neurotrauma 26:861–876
DeKosky ST, Ikonomovic MD, Gandy S (2010) Traumatic brain injury—football, warfare, and long-term effects New England. J Med 363:1293–1296
Delius M (2002) Twenty years of shock wave research at the Institute for Surgical Research. Eur Surg Res 34:30–36
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21
Dennis EL et al (2015) Callosal function in pediatric traumatic brain injury linked to disrupted white matter integrity. J Neurosci 35:10202–10211
Drake A, Meyer KS, Cessante LM, Cheung CR, Cullen MA, McDonald EC, Holland MC (2010) Routine TBI screening following combat deployments. Neurorehabilitation 26:183–189
Eckmann J-P, Kamphorst SO, Ruelle D (1987) Recurrence plots of dynamical systems. EPL (Europhys Lett) 4:973
Elder GA, Stone JR, Ahlers ST (2014) Effects of low-level blast exposure on the nervous system: is there really a controversy? Front Neurol. https://doi.org/10.3389/fneur.2014.00269
Freeman WJ (1994) Role of chaotic dynamics in neural plasticity. Progress Brain Res 102:319–333
Galarneau MR, Woodruff SI, Dye JL, Mohrle CR, Wade AL (2008) Traumatic brain injury during Operation Iraqi Freedom: findings from the United States Navy–Marine Corps Combat Trauma Registry
Goeller J, Wardlaw A, Treichler D, O’Bruba J, Weiss G (2012) Investigation of cavitation as a possible damage mechanism in blast-induced traumatic brain injury. J Neurotrauma 29:1970–1981
Gultekin S, Smith TW (1994) Diffuse axonal injury in craniocerebral trauma. A comparative histologic and immunohistochemical study. Arch Pathol Lab Med 118:168–171
Gurau O, Bosl WJ, Newton CR (2017) How useful is electroencephalography in the diagnosis of autism spectrum disorders and the delineation of subtypes: a systematic review. Front Psychiatry 8:121
Han K et al (2014) Disrupted modular organization of resting-state cortical functional connectivity in US military personnel following concussive ‘mild’blast-related traumatic brain injury. Neuroimage 84:76–96
Hayward EP (2008) Planning beyond tactics: towards a military application of the philosophy of design in the formulation of strategy. Army Command and General Staff Coll fort Leavenworth KS School of Advanced Military Studies
Heltemes KJ, Holbrook TL, MacGregor AJ, Galarneau MR (2012) Blast-related mild traumatic brain injury is associated with a decline in self-rated health amongst US military personnel. Injury 43:1990–1995
Hicks RR, Fertig SJ, Desrocher RE, Koroshetz WJ, Pancrazio JJ (2010) Neurological effects of blast injury. J Trauma 68:1257–1263. https://doi.org/10.1097/TA.0b013e3181d8956d
Johnson VE, Stewart W, Smith DH (2013) Axonal pathology in traumatic brain injury. Exp Neurol 246:35–43
Kaplan D, Glass L (1995) Time-series analysis. Understanding nonlinear dynamics. Springer, Berlin, pp 278–358
Kelso J (1995) Dynamic patterns: the self-organization of brain and behavior. MIT Press, Cambridge
Kennel MB, Brown R, Abarbanel HD (1992) Determining embedding dimension for phase-space reconstruction using a geometrical construction. Phys Rev A 45:3403
Kiefer A, Myer GD (2015) Training the antifragile athlete: a preliminary analysis of neuromuscular training effects on muscle activation dynamics nonlinear dynamics. Psychol Life Sci 19:489–510
Kleim JA, Jones TA (2008) Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res 51:S225–S239
Kolb B (1999) Synaptic plasticity and the organization of behaviour after early and late brain injury. Can J Exp Psychol 53:62
Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM (2007) White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 130:2508–2519
Littlefield PD, Pinto RL, Burrows HL, Brungart DS (2016) The vestibular effects of repeated low-level blasts. J Neurotrauma 33:71–81
Liu J, Kou Z, Tian Y (2014) Diffuse axonal injury after traumatic cerebral microbleeds: an evaluation of imaging techniques. Neural Regener Res 9:1222–1230. https://doi.org/10.4103/1673-5374.135330
Mac Donald CL et al (2011) Detection of blast-related traumatic brain injury in US military personnel. N Engl J Med 364:2091–2100
Marwan N, Wessel N, Meyerfeldt U, Schirdewan A, Kurths J (2002) Recurrence-plot-based measures of complexity and their application to heart-rate-variability data. Phys Rev E 66:026702
Marwan N, Romano CM, Thiel M, Kurths J (2007) Recurrence plots for the analysis of complex systems. Phys Rep 438:237–329. https://doi.org/10.1016/j.physrep.2006.11.001
Myer GD et al (2016a) The effects of external jugular compression applied during head impact exposure on longitudinal changes in brain neuroanatomical and neurophysiological biomarkers: a preliminary investigation. Front Neurol 7:74
Myer GD et al (2016b) Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med bjsports-2016:096134
Nakagawa A et al (2011) Mechanisms of primary blast-induced traumatic brain injury: insights from shock-wave research. J Neurotrauma 28:1101–1119
Nicolaou N, Georgiou J (2014) The study of EEG dynamics during anesthesia with cross-recurrence rate. Cureus 6:8
Niogi SN et al (2008) 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. Am J Neuroradiol 29:967–973
Okie S (2005) Traumatic brain injury in the war zone. N Engl J Med 352:2043–2047
Oni MB et al (2010) Diffusion tensor imaging analysis of frontal lobes in pediatric traumatic brain injury. J Child Neurol 25:976–984. https://doi.org/10.1177/0883073809356034
Przekwas A, Somayaji MR, Gupta RK (2016) Synaptic mechanisms of blast-induced brain injury. Front Neurol 7:2
Rapp PE et al (2015) Traumatic brain injury detection using electrophysiological methods. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2015.00011
Reid MW et al (2014) A multisite study of the relationships between blast exposures and symptom reporting in a post-deployment active duty military population with mild traumatic brain injury. J Neurotrauma 31:1899–1906
Rizzi M, Frigerio F, Iori V (2016a) The early phases of epileptogenesis induced by status epilepticus are characterized by persistent dynamical regime of intermittency type. In: Webber CL Jr, Ioana C, Marwan N (eds) Recurrence plots and their quantifications: expanding horizons. Springer, Berlin. https://doi.org/10.1007/978-3-319-29922-8
Rizzi M, Weissberg I, Milikovsky DZ, Friedman A (2016b) Following a potential epileptogenic insult, prolonged high rates of nonlinear dynamical regimes of intermittency type is the hallmark of epileptogenesis. Sci Rep 6:31129
Rodríguez-Millán M, Tan LB, Tse KM, Lee HP, Miguélez MH (2017) Effect of full helmet systems on human head responses under blast loading. Mater Des 117:58–71. https://doi.org/10.1016/j.matdes.2016.12.081
Romano MC, Thiel M, Kurths J, Kiss IZ, Hudson J (2005) Detection of synchronization for non-phase-coherent and non-stationary data. EPL (Europhys Lett) 71:466
Rosenfeld JV, McFarlane AC, Bragge P, Armonda RA, Grimes JB, Ling GS (2013) Blast-related traumatic brain injury. Lancet Neurol 12:882–893
Roulston MS (1999) Estimating the errors on measured entropy and mutual information. Phys D 125:285–294
Schinkel S, Marwan N, Kurths J (2007) Order patterns recurrence plots in the analysis of ERP data. Cogn Neurodyn 1:317–325
Schinkel S, Marwan N, Kurths J (2009) Brain signal analysis based on recurrences. J Physiol Paris 103:315–323
Smith DW, Bailes JE, Fisher JA, Robles J, Turner RC, Mills JD (2011) Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. Neurosurgery 70:740–746
Song I-H, Lee D-S, Kim SI (2004) Recurrence quantification analysis of sleep electroencephalogram in sleep apnea syndrome in humans. Neurosci Lett 366:148–153
Sporns O (2011) The human connectome: a complex network. Ann NY Acad Sci 1224:109–125
Stam CJ (2005) Nonlinear dynamical analysis of EEG and MEG: review of an emerging field. Clin Neurophysiol 116:2266–2301
Stergiou N, Decker LM (2011) Human movement variability, nonlinear dynamics, and pathology: is there a connection? Hum Mov Sci 30:869–888
Stergiou N, Harbourne RT, Cavanaugh JT (2006) Optimal movement variability: a new theoretical perspective for neurologic physical therapy. J Neurol Phys Ther 30:120–129
Takens F (1981) Detecting strange attractors in turbulence. Lect Notes Math 898:366–381
Thomasson N, Hoeppner TJ, Webber CL, Zbilut JP (2001) Recurrence quantification in epileptic EEGs. Phys Lett A 279:94–101
Timothy LT, Krishna BM, Nair U (2017) Classification of mild cognitive impairment EEG using combined recurrence and cross recurrence quantification analysis. Int J Psychophysiol 120:86–95
Turner RC, Naser ZJ, Bailes JE, Smith DW, Fisher JA, Rosen CL (2012) Effect of slosh mitigation on histologic markers of traumatic brain injury. J Neurosurg 117:1110–1118
Vakhtin AA, Calhoun VD, Jung RE, Prestopnik JL, Taylor PA, Ford CC (2013) Changes in intrinsic functional brain networks following blast-induced mild traumatic brain injury. Brain Inj 27:1304–1310
Warden D (2006) Military TBI during the Iraq and Afghanistan wars. J Head Trauma Rehabil 21:398–402
Webber CL Jr, Zbilut JP (1994) Dynamical assessment of physiological systems and states using recurrence plot strategies. J Appl Physiol 76:965–973
Webber CL Jr, Zbilut JP (2005) Recurrence quantification analysis of nonlinear dynamical systems. Tutor Contemp Nonlinear Methods Behav Sci 2005:26–94
Wozniak JR et al (2007) Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) study. Arch Clin Neuropsychol 22:555–568
Yuan W et al (2017) Neck collar with mild jugular vein compression ameliorates brain activation changes during a working memory task after a season of high school football. J Neurotrauma 34:2432
Yuan W et al (2018) White matter alterations over the course of two consecutive high-school football seasons and the effect of a jugular compression collar: a preliminary longitudinal diffusion tensor imaging study. Hum Brain Mapp 39:491–508
Zaepffel M, Trachel R, Kilavik BE, Brochier T (2013) Modulations of EEG beta power during planning and execution of grasping movements. PLoS One 8:e60060
Zbilut JP, Webber CL Jr (1992) Embeddings and delays as derived from quantification of recurrence plots. Phys Lett A 171:199–203
Zhang W, Worrell G, He B (2008) Recurrence based deterministic trends in EEG records of epilepsy patients. In: Information technology and applications in biomedicine, ITAB 2008. International conference on (2008) IEEE, pp 391–394
Acknowledgements
The authors would like to thank Hamilton County Police Association SWAT. We appreciate their patience with the testing scheduling, follow-ups, and equipment additions. Their enthusiastic support made this study possible. We would like to thank Chief David Schaefer-SWAT Commander, Sheriff Jim Neil-Hamilton County Sheriff and Chief Charles R. Lindsey-HCPA president for their help in obtaining approval for the study and for Interim SWAT Commander Tim Chin for helping to coordinate the entire study protocol. Special acknowledgement goes to SWAT Medical Directors, Dustin J. Calhoun, MD and Edward Otten, MD and Hamilton County Medical Director Lakshmi Kode Sammarco, MD. Without their time, commitment, and passion for the health and well-being of their team members, this study would not have been possible. We also thank Chief Jim Puthoff-Liaison to HCPA who supported and presented the research ideas to the SWAT that allowed for the initial discussions to medical directors. We would also like to thank James P. Bailey, Evans Demolition/Excavation Division who helped secure the bank for explosive breach training. We also thank the Bomb Explosive Ordnance Disposal Technicians Brad Justice and Steve Luensman who coordinated the explosive training and helped to ensure the safety of both SWAT members and the research team. The authors acknowledge funding support from Q30 Sports Innovations, LLC.
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Bonnette, S., Diekfuss, J.A., Kiefer, A.W. et al. A jugular vein compression collar prevents alterations of endogenous electrocortical dynamics following blast exposure during special weapons and tactical (SWAT) breacher training. Exp Brain Res 236, 2691–2701 (2018). https://doi.org/10.1007/s00221-018-5328-x
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DOI: https://doi.org/10.1007/s00221-018-5328-x