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Zone 1 REBOA in a combat DCBI swine model does not worsen brain injury

      Abstract

      Background

      Zone 1 resuscitative endovascular balloon occlusion of the aorta has been recommended for refractory shock after a dismounted complex blast injury for the austere combat scenario. While resuscitative endovascular balloon occlusion of the aorta should enhance coronary perfusion, there is a potential risk of secondary brain injury due to loss of cerebral autoregulation. We developed a combat casualty relevant dismounted complex blast injury swine model to evaluate the effects of resuscitative endovascular balloon occlusion of the aorta zone I on intracranial pressure and cerebral edema. We hypothesized that zone 1 aortic occlusion with resuscitative endovascular balloon occlusion of the aorta would increase mean arterial pressure transmitted in excessive intracranial pressure, thereby worsening brain injury.

      Methods

      50 kg male Yorkshire swine were subjected to a combination dismounted complex blast injury model consisting of blast traumatic brain injury (50 psi, ARA Mobile Shock Laboratory), tissue injury (bilateral femur fractures), and hemorrhagic shock (controlled bleeding to a base deficit goal of 10 mEq/L). During the shock phase, pigs were randomized to no aortic occlusion (n = 8) or to 30 minutes of zone 1 resuscitative endovascular balloon occlusion of the aorta (zone 1 aortic occlusion group, n = 6). After shock, pigs in both groups received a modified Tactical Combat Casualty Care–based resuscitation and were monitored for an additional 240 minutes until euthanasia/death for a total of 6 hours. Intracranial pressure was monitored throughout, and brains were harvested for water content. Linear mixed models for repeated measures were used to compare mean arterial pressure and intracranial pressure between zone 1 aortic occlusion and no aortic occlusion groups.

      Results

      After dismounted complex blast injury, the zone 1 group had a significantly higher mean arterial pressure during hemorrhagic shock compared to the control group (41.2 mm Hg vs 16.7 mm Hg, P = .002). During balloon occlusion, intracranial pressure was not significantly elevated in the zone 1 aortic occlusion group vs control, but intracranial pressure was significantly lower in the zone 1 group at the end of the observation period. In addition, the zone 1 aortic occlusion group did not have increased brain water content (zone 1 aortic occlusion: 3.95 ± 0.1g vs no aortic occlusion: 3.95 ± 0.3 g, P = .87). Troponin levels significantly increased in the no aortic occlusion group but did not in the zone 1 aortic occlusion group.

      Conclusion

      Zone 1 aortic occlusion using resuscitative endovascular balloon occlusion of the aorta in a large animal dismounted complex blast injury model improved proximal mean arterial pressure while not significantly increasing intracranial pressure during balloon inflation. Observation up to 240 minutes postresuscitation did not show clinical signs of worsening brain injury or cardiac injury. These data suggest that in a dismounted complex blast injury swine model, resuscitative endovascular balloon occlusion of the aorta in zone 1 may provide neuro- and cardioprotection in the setting of blast traumatic brain injury. However, longer monitoring periods may be needed to confirm that the neuroprotection is lasting.
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      References

        • Kauvar D.S.
        • Wade C.E.
        The epidemiology and modern management of traumatic hemorrhage: US and international perspectives.
        Crit Care. 2005; 9: S1-S9
        • Rhee P.
        • Joseph B.
        • Pandit V.
        • et al.
        Increasing trauma deaths in the United States.
        Ann Surg. 2014; 260: 13-21
        • Morrison J.J.
        • Ross J.D.
        • Rasmussen T.E.
        • Midwinter M.J.
        • Jansen J.O.
        Resuscitative endovascular balloon occlusion of the aorta: a gap analysis of severely injured UK combat casualties.
        Shock. 2014; 41: 388-393
        • Cannon J.W.
        • Hofmann L.J.
        • Glasgow S.C.
        • et al.
        Dismounted complex blast injuries: a comprehensive review of the modern combat experience.
        J Am Coll Surg. 2016; 223: 652-664.e8
        • Eastridge B.J.
        • Mabry R.L.
        • Seguin P.
        • et al.
        Death on the battlefield (2001–2011): implications for the future of combat casualty care.
        J Trauma Acute Care Surg. 2012; 73: S431-S437
        • Eastridge B.J.
        • Holcomb J.B.
        • Shackelford S.
        Outcomes of traumatic hemorrhagic shock and the epidemiology of preventable death from injury.
        Transfusion. 2019; 59: 1423-1428
        • Stokes S.C.
        • Theodorou C.M.
        • Zakaluzny S.A.
        • DuBose J.J.
        • Russo R.M.
        Resuscitative endovascular balloon occlusion of the aorta in combat casualties: the past, present, and future.
        J Trauma Acute Care Surg. 2021; 91: S56-S64
        • Rafaels K.A.
        • Bass C.R.
        • Panzer M.B.
        • et al.
        Brain injury risk from primary blast.
        J Trauma Acute Care Surg. 2012; 73: 895-901
        • Uchino H.
        • Tamura N.
        • Echigoya R.
        • Ikegami T.
        • Fukuoka T.
        “REBOA”: is it really safe? A case with massive intracranial hemorrhage possibly due to endovascular balloon occlusion of the aorta (REBOA).
        Am J Case Rep. 2016; 17: 810-813
        • Johnson M.A.
        • Williams T.K.
        • Ferencz S.E.
        • et al.
        The effect of resuscitative endovascular balloon occlusion of the aorta, partial aortic occlusion and aggressive blood transfusion on traumatic brain injury in a swine multiple injuries model.
        J Trauma Acute Care Surg. 2017; 83: 61-70
        • Hoehn M.R.
        • Teeter W.A.
        • Morrison J.J.
        • et al.
        Aortic branch vessel flow during resuscitative endovascular balloon occlusion of the aorta.
        J Trauma Acute Care Surg. 2019; 86: 79-85
        • Fuller G.
        • Hasler R.M.
        • Mealing N.
        • et al.
        The association between admission systolic blood pressure and mortality in significant traumatic brain injury: a multi-centre cohort study.
        Injury. 2014; 45: 612-617
        • Butcher I.
        • Maas A.I.
        • Lu J.
        • et al.
        Prognostic value of admission blood pressure in traumatic brain injury: results from the IMPACT study.
        J Neurotrauma. 2007; 24: 294-302
        • Cralley A.L.
        • Moore E.E.
        • Kissau D.
        • et al.
        A combat casualty relevant dismounted complex blast injury model in swine.
        J Trauma Acute Care Surg. 2022; (Epub ahead of print. May 12.)https://doi.org/10.1097/TA.0000000000003674
        • Davis J.W.
        • Dirks R.C.
        • Kaups K.L.
        • Tran P.
        Base deficit is superior to lactate in trauma.
        Am J Surg. 2018; 215: 682-685
        • Elliott M.B.
        • Jallo J.J.
        • Tuma R.F.
        An investigation of cerebral edema and injury volume assessments for controlled cortical impact injury.
        J Neurosci Methods. 2008; 168: 320-324
        • Keep R.F.
        • Hua Y.
        • Xi G.
        Brain water content: a misunderstood measurement?.
        Transl Stroke Res. 2012; 3: 263-265
        • Hawryluk G.W.
        • Phan N.
        • Ferguson A.R.
        • et al.
        Brain tissue oxygen tension and its response to physiological manipulations: influence of distance from injury site in a swine model of traumatic brain injury.
        J Neurosurg. 2016; 125: 1217-1228
        • Northern D.M.
        • Manley J.D.
        • Lyon R.
        • et al.
        Recent advances in austere combat surgery: use of aortic balloon occlusion as well as blood challenges by special operations medical forces in recent combat operations.
        J Trauma Acute Care Surg. 2018; 85: S98-S103
        • Wolf S.J.
        • Bebarta V.S.
        • Bonnett C.J.
        • Pons P.T.
        • Cantrill S.V.
        Blast injuries.
        Lancet. 2009; 374: 405-415
        • Rafaels K.
        • Bass C.R.
        • Salzar R.S.
        • et al.
        Survival risk assessment for primary blast exposures to the head.
        J Neurotrauma. 2011; 28: 2319-2328
        • Griesdale D.E.
        • Ortenwall V.
        • Norena M.
        • et al.
        Adherence to guidelines for management of cerebral perfusion pressure and outcome in patients who have severe traumatic brain injury.
        J Crit Care. 2015; 30: 111-115
        • Young J.S.
        • Blow O.
        • Turrentine F.
        • Claridge J.A.
        • Schulman A.
        Is there an upper limit of intracranial pressure in patients with severe head injury if cerebral perfusion pressure is maintained?.
        Neurosurg Focus. 2003; 15: E2
      1. Brain Trauma Foundation, American Association of Neurological Surgeons, Congress of Neurological Surgeons, Joint Section on Neurotrauma and Critical Care, Carney NA. Guidelines for the management of severe traumatic brain injury. Methods.
        J Neurotrauma. 2007; 24: S3-S6
        • Carney N.
        • Totten A.M.
        • O’Reilly C.
        • et al.
        Guidelines for the management of severe traumatic brain injury (4th edition).
        Neurosurgery. 2017; 80: 6-15
        • Clifton G.L.
        • Miller E.R.
        • Choi S.C.
        • Levin H.S.
        Fluid thresholds and outcome from severe brain injury.
        Crit Care Med. 2002; 30: 739-745
        • Bratton S.L.
        • Chestnut R.M.
        • Ghajar J.
        • et al.
        Guidelines for the management of severe traumatic brain injury. I. Blood pressure and oxygenation.
        J Neurotrauma. 2007; 24: S7-S13
        • Zafar S.N.
        • Millham F.H.
        • Chang Y.
        • et al.
        Presenting blood pressure in traumatic brain injury: a bimodal distribution of death.
        J Trauma. 2011; 71: 1179-1184
        • Russo R.M.
        • Neff L.P.
        • Lamb C.M.
        • et al.
        Partial resuscitative endovascular balloon occlusion of the aorta in swine model of hemorrhagic shock.
        J Am Coll Surg. 2016; 223: 359-368
        • Toth P.
        • Szarka N.
        • Farkas E.
        • et al.
        Traumatic brain injury-induced autoregulatory dysfunction and spreading depression-related neurovascular uncoupling: pathomechanisms, perspectives, and therapeutic implications.
        Am J Physiol Heart Circ Physiol. 2016; 311 (H1118–H31)
        • Qasim Z.A.
        • Sikorski R.A.
        physiologic considerations in trauma patients undergoing resuscitative endovascular balloon occlusion of the aorta.
        Anesth Analg. 2017; 125: 891-894
        • Sellmann T.
        • Miersch D.
        • Kienbaum P.
        • et al.
        The impact of arterial hypertension on polytrauma and traumatic brain injury.
        Dtsch Arztebl Int. 2012; 109: 849-856
        • Williams A.M.
        • Bhatti U.F.
        • Dennahy I.S.
        • et al.
        Traumatic brain injury may worsen clinical outcomes after prolonged partial resuscitative endovascular balloon occlusion of the aorta in severe hemorrhagic shock model.
        J Trauma Acute Care Surg. 2019; 86: 415-423
        • Armonda R.A.
        • Bell R.S.
        • Vo A.H.
        • et al.
        Wartime traumatic cerebral vasospasm: recent review of combat casualties.
        Neurosurgery. 2006; 59 (discussion 25): 1215-1225
        • Ling G.
        • Bandak F.
        • Armonda R.
        • Grant G.
        • Ecklund J.
        Explosive blast neurotrauma.
        J Neurotrauma. 2009; 26: 815-825
        • Prima V.
        • Serebruany V.L.
        • Svetlov A.
        • Hayes R.L.
        • Svetlov S.I.
        Impact of moderate blast exposures on thrombin biomarkers assessed by calibrated automated thrombography in rats.
        J Neurotrauma. 2013; 30: 1881-1887
        • Kabu S.
        • Jaffer H.
        • Petro M.
        • et al.
        Blast-associated shock waves result in increased brain vascular leakage and elevated ROS levels in a rat model of traumatic brain injury.
        PLoS One. 2015; 10e0127971
        • Gama Sosa M.A.
        • De Gasperi R.
        • Janssen P.L.
        • et al.
        Selective vulnerability of the cerebral vasculature to blast injury in a rat model of mild traumatic brain injury.
        Acta Neuropathol Commun. 2014; 2: 67
        • Logsdon A.F.
        • Meabon J.S.
        • Cline M.M.
        • et al.
        Blast exposure elicits blood-brain barrier disruption and repair mediated by tight junction integrity and nitric oxide dependent processes.
        Sci Rep. 2018; 811344
        • Toklu H.Z.
        • Yang Z.
        • Oktay S.
        • et al.
        Overpressure blast injury-induced oxidative stress and neuroinflammation response in rat frontal cortex and cerebellum.
        Behav Brain Res. 2018; 340: 14-22
        • Bauman R.A.
        • Ling G.
        • Tong L.
        • et al.
        An introductory characterization of a combat-casualty-care relevant swine model of closed head injury resulting from exposure to explosive blast.
        J Neurotrauma. 2009; 26: 841-860
        • Saljo A.
        • Arrhen F.
        • Bolouri H.
        • Mayorga M.
        • Hamberger A.
        Neuropathology and pressure in the pig brain resulting from low-impulse noise exposure.
        J Neurotrauma. 2008; 25: 1397-1406
        • Balaban C.
        • Jackson R.L.
        • Liu J.
        • Gao W.
        • Hoffer M.E.
        Intracranial venous injury, thrombosis and repair as hallmarks of mild blast traumatic brain injury in rats: lessons from histological and immunohistochemical studies of decalcified sectioned heads and correlative microarray analysis.
        J Neurosci Methods. 2016; 272: 56-68
        • Stocchetti N.
        • Maas A.I.
        Traumatic intracranial hypertension.
        N Engl J Med. 2014; 371: 972