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REBOA-Induced Ischemia-Reperfusion Injury

  • Jigarkumar A. Patel
  • Joseph M. WhiteEmail author
Chapter
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Part of the Hot Topics in Acute Care Surgery and Trauma book series (HTACST)

Abstract

Resuscitative endovascular balloon occlusion of the aorta (REBOA)-induced ischemia-reperfusion injury (IRI) represents a complex pathophysiologic process involving dysfunction of intracellular and extracellular components responsible for metabolic, thrombotic, and inflammatory signaling and cellular function. Mitigation strategies following repair and re-establishment of end-organ perfusion include surgical and pharmacologic considerations and adjuncts. Currently, there is a paucity of clinical data concerning the incidence and associated clinical ramifications of IRI following REBOA deployment. Given this limitation, this chapter aims to review IRI as a result of REBOA and discuss the current literature on REBOA-associated IRI mitigation strategies.

References

  1. 1.
    Morrison JJ. Noncompressible torso hemorrhage. Crit Care Clin. 2017;33(1):37–54.PubMedGoogle Scholar
  2. 2.
    Eastridge BJ, Mabry RL, Seguin P, Cantrell J, Tops T, Uribe P, Mallett O, Zubko T, Oetjen-Gerdes L, Rasmussen TE, Butler FK, Kotwal RS, Holcomb JB, Wade C, Champion H, Lawnick M, Moores L, Blackbourne LH. Death on the battlefield (2001-2011): implications for the future of combat casualty care. J Trauma Acute Care Surg. 2012;73(6 Suppl 5):S431–7.PubMedPubMedCentralGoogle Scholar
  3. 3.
    DeBakey ME, Simeone FA. Battle injuries of the arteries in World War II. Ann Surg. 1946;123:534–79.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Hughes CW. The primary repair of wounds of major arteries; an analysis of experience in Korea in 1953. Ann Surg. 1955;141:297–303.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Hughes CW. Acute vascular trauma in Korean War casualties; an analysis of 180 cases. Surg Gynecol Obstet. 1954;99:91–100.PubMedGoogle Scholar
  6. 6.
    Rich NM, Hughes CW. Vietnam vascular registry: a preliminary report. Surgery. 1969;65:218–26.PubMedGoogle Scholar
  7. 7.
    Rich NM, Baugh JH, Hughes CW. Acute arterial injuries in Vietnam: 1,000 cases. J Trauma. 1970;10:359–69.PubMedGoogle Scholar
  8. 8.
    White JM, Stannard A, Burkhardt GE, Eastridge BJ, Blackbourne LH, Rasmussen TE. The epidemiology of vascular injury in the wars in Iraq and Afghanistan. Ann Surg. 2011;253(6):1184–9.PubMedGoogle Scholar
  9. 9.
    Patel JA, White JM, White PW, Rich NM, Rasmussen TE. A contemporary, 7-year analysis of vascular injury from the war in Afghanistan. J Vasc Surg. 2018;68(6):1872.PubMedGoogle Scholar
  10. 10.
    Halestrap AP. A pore way to die: the role of mitochondria in reperfusion injury and cardioprotection. Biochem Soc Trans. 2010;38(4):841–60.PubMedGoogle Scholar
  11. 11.
    Haworth RA, Hunter DR. The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site. Arch Biochem Biophys. 1979;195(2):460–7.PubMedGoogle Scholar
  12. 12.
    Piper HM, Garcia-Dorado D, Ovize M. A fresh look at reperfusion injury. Cardiovasc Res. 1998;38:291–300.PubMedGoogle Scholar
  13. 13.
    Halestrap AP. Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans. 2006;34(Pt 2):232–7.PubMedGoogle Scholar
  14. 14.
    Halestrap AP, Richardson AP. The mitochondrial permeability transition: a current perspective on its identity and role in ischaemia/reperfusion injury. J Mol Cell Cardiol. 2015;78:129–41.PubMedGoogle Scholar
  15. 15.
    Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994;76:301–14.Google Scholar
  16. 16.
    Tamura DY, Moore EE, Partrick DA, Johnson JL, Offner PJ, Silliman CC. Acute hypoxemia in humans enhances the neutrophil inflammatory response. Shock. 2002;17:269–73.PubMedGoogle Scholar
  17. 17.
    Gautam N, Olofsson AM, Herwald H, Iversen LF, Lundgren-Akerlund E, Hedqvist P, Arfors KE, Flodgaard H, Lindbom L. Heparin-binding protein (HBP/CAP37): a missing link in neutrophil-evoked alteration of vascular permeability. Nat Med. 2001;7:1123–7.PubMedGoogle Scholar
  18. 18.
    Collard CD, et al. Neutrophil-derived glutamate regulates vascular endothelial barrier function. J Biol Chem. 2002;277:14801–11.PubMedGoogle Scholar
  19. 19.
    Eltzschig HK, Collard CD. Vascular ischaemia and reperfusion injury. Br Med Bull. 2004;70:71–86.PubMedGoogle Scholar
  20. 20.
    Eltzschig HK, Thompson LF, Karhausen J, Cotta RJ, Ibla JC, Robson SC, Colgan SP. Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism. Blood. 2004;104:3986–92.PubMedGoogle Scholar
  21. 21.
    Halestrap AP, et al. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta. 2009;1787(11):1402–15.PubMedGoogle Scholar
  22. 22.
    Ha T, et al. Toll-like receptors: new players in myocardial ischemia/reperfusion injury. Antioxid Redox Signal. 2011;15(7):1875–93.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Zhang M, et al. Natural antibody mediated innate autoimmune response. Mol Immunol. 2007;44(1-3):103–10.PubMedGoogle Scholar
  24. 24.
    Tang PS, Mura M, Seth R, Liu M. Acute lung injury and cell death: how many ways can cells die? Am J Physiol Lung Cell Mol Physiol. 2008;294(4):L632–41.PubMedGoogle Scholar
  25. 25.
    DuBose JJ, Scalea TM, Brenner M, Skiada D, Inaba K, Cannon J, Moore L, Holcomb J, Turay D, Arbabi CN, Kirkpatrick A, Xiao J, Skarupa D, Poulin N. AAST AORTA Study Group. The AAST prospective Aortic Occlusion for Resuscitation in Trauma and Acute Care Surgery (AORTA) registry: data on contemporary utilization and outcomes of aortic occlusion and resuscitative balloon occlusion of the aorta (REBOA). J Trauma Acute Care Surg. 2016;81(3):409–19.PubMedGoogle Scholar
  26. 26.
    Stannard A, Eliason JL, Rasmussen TE. Resuscitative endovascular balloon occlusion of the aorta (REBOA) as an adjunct for hemorrhagic shock. J Trauma. 2011;71(6):1869–72.PubMedGoogle Scholar
  27. 27.
    Marrocco-Trischitta MM, Melissano G, Kahlberg A, Vezzoli G, Calori G, Chiesa R. The impact of aortic clamping site on glomerular filtration rate after juxtarenal aneurysm repair. Ann Vasc Surg. 2009;23(6):770–7.PubMedGoogle Scholar
  28. 28.
    Reva VA, Matsumura Y, Hörer T, Sveklov DA, Denisov AV, Telickiy SY, Seleznev AB, Bozhedomova ER, Matsumoto J, Samokhvalov IM, Morrison JJ. Resuscitative endovascular balloon occlusion of the aorta: what is the optimum occlusion time in an ovine model of hemorrhagic shock? Eur J Trauma Emerg Surg. 2018;44:511.PubMedGoogle Scholar
  29. 29.
    Markov NP, Percival TJ, Morrison JJ, Ross JD, Scott DJ, Spencer JR, Rasmussen TE. Physiologic tolerance of descending thoracic aortic balloon occlusion in a swine model of hemorrhagic shock. Surgery. 2013;153(6):848–56.PubMedGoogle Scholar
  30. 30.
    Morrison JJ, Ross JD, Markov NP, Scott DJ, Spencer JR, Rasmussen TE. The inflammatory sequelae of aortic balloon occlusion in hemorrhagic shock. J Surg Res. 2014;191(2):423–31.PubMedGoogle Scholar
  31. 31.
    Avaro JP, Mardelle V, Roch A, Gil C, de Biasi C, Oliver M, Fusai T, Thomas P. Forty-minute endovascular aortic occlusion increases survival in an experimental model of uncontrolled hemorrhagic shock caused by abdominal trauma. J Trauma. 2011;71(3):720–5; discussion 725–6.PubMedGoogle Scholar
  32. 32.
    White JM, Cannon JW, Stannard A, Markov NP, Spencer JR, Rasmussen TE. Endovascular balloon occlusion of the aorta is superior to resuscitative thoracotomy with aortic clamping in a porcine model of hemorrhagic shock. Surgery. 2011;150(3):400–9.PubMedGoogle Scholar
  33. 33.
    Martinelli T, Thony F, Decléty P, Sengel C, Broux C, Tonetti J, Payen JF, Ferretti G. Intra-aortic balloon occlusion to salvage patients with life-threatening hemorrhagic shocks from pelvic fractures. J Trauma. 2010;68(4):942–8.PubMedGoogle Scholar
  34. 34.
    Russo RM, Williams TK, Grayson JK, Lamb CM, Cannon JW, Clement NF, Galante JM, Neff LP. Extending the golden hour: partial resuscitative endovascular balloon occlusion of the aorta in a highly lethal swine liver injury model. J Trauma Acute Care Surg. 2016;80(3):372–8; discussion 378–80.PubMedGoogle Scholar
  35. 35.
    Russo RM, Neff LP, Lamb CM, Cannon JW, Galante JM, Clement NF, Grayson JK, Williams TK. Partial resuscitative endovascular balloon occlusion of the aorta in swine model of hemorrhagic shock. J Am Coll Surg. 2016;223(2):359–68.PubMedGoogle Scholar
  36. 36.
    Johnson MA, Davidson AJ, Russo RM, Ferencz SE, Gotlib O, Rasmussen TE, Neff LP, Williams TK. Small changes, big effects: the hemodynamics of partial and complete aortic occlusion to inform next generation resuscitation techniques and technologies. J Trauma Acute Care Surg. 2017;82(6):1106–11.PubMedGoogle Scholar
  37. 37.
    Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, Hussain P, Vecoli C, Paolocci N, Ambs S, Colton CA, Harris CC, Roberts DD, Wink DA. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med. 2008;45(1):18–31.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Widgerow AD. Ischemia-reperfusion injury: influencing the microcirculatory and cellular environment. Ann Plast Surg. 2014;72(2):253–60.PubMedGoogle Scholar
  39. 39.
    Rabkin SW, Klassen SS. Metalloporphyrins as a therapeutic drug class against peroxynitrite in cardiovascular diseases involving ischemic reperfusion injury. Eur J Pharmacol. 2008;586(1-3):1–8.PubMedGoogle Scholar
  40. 40.
    Li XL, Zou XM, Gao P, Li YL, Wang H, Chen XW. Role of nitric oxide in ischemia-reperfusion injury and acute rejection in rat intestinal transplantation. Transplant Proc. 2008;40(10):3342–5.PubMedGoogle Scholar
  41. 41.
    Ashwal S, Cole DJ, Osborne TN, Pearce WJ. Low dose L-NAME reduces infarct volume in the rat MCAO/reperfusion model. J Neurosurg Anesthesiol. 1993;5(4):241–9.PubMedGoogle Scholar
  42. 42.
    Sosnowski P, Krauss H, Bogdanski P, Suliburska J, Jablecka A, Cieslewicz A, Pupek-Musialik D, Jastak R. The influence of short-term L-arginine supplementation on rats’ muscular and hepatic cells in ischemia-reperfusion syndrome. J Physiol Biochem. 2012;68(1):1–9.PubMedGoogle Scholar
  43. 43.
    Wu SY, Tang SE, Ko FC, Wu GC, Huang KL, Chu SJ. Valproic acid attenuates acute lung injury induced by ischemia-reperfusion in rats. Anesthesiology. 2015;122(6):1327–37.PubMedGoogle Scholar
  44. 44.
    Costalonga EC, Silva FM, Noronha IL. Valproic acid prevents renal dysfunction and inflammation in the ischemia-reperfusion injury model. Biomed Res Int. 2016;2016:5985903.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Zacharias N, Sailhamer EA, Li Y, Liu B, Butt MU, Shuja F, Velmahos GC, de Moya M, Alam HB. Histone deacetylase inhibitors prevent apoptosis following lethal hemorrhagic shock in rodent kidney cells. Resuscitation. 2011;82(1):105–9.PubMedGoogle Scholar
  46. 46.
    Li Y, Liu B, Sailhamer EA, Yuan Z, Shults C, Velmahos GC, deMoya M, Shuja F, Butt MU, Alam HB. Cell protective mechanism of valproic acid in lethal hemorrhagic shock. Surgery. 2008;144(2):217–24.PubMedGoogle Scholar
  47. 47.
    Causey MW, Miller S, Hoffer Z, Hempel J, Stallings JD, Jin G, Alam H, Martin M. Beneficial effects of histone deacetylase inhibition with severe hemorrhage and ischemia-reperfusion injury. J Surg Res. 2013;184(1):533–40.PubMedGoogle Scholar
  48. 48.
    Shults C, Sailhamer EA, Li Y, Liu B, Tabbara M, Butt MU, Shuja F, Demoya M, Velmahos G, Alam HB. Surviving blood loss without fluid resuscitation. J Trauma. 2008;64(3):629–38; discussion 638–40.PubMedGoogle Scholar
  49. 49.
    Nelson DW, Porta CR, McVay DP, Salgar SK, Martin MJ. Effects of histone deacetylase inhibition on 24-hour survival and end-organ injury in a porcine trauma model: a prospective, randomized trial. J Trauma Acute Care Surg. 2013;75(6):1031–9.PubMedGoogle Scholar
  50. 50.
    Ely SW, Berne RM. Protective effects of adenosine in myocardial ischemia. Circulation. 1992;85(3):893–904.PubMedGoogle Scholar
  51. 51.
    Forman MB, Velasco CE, Jackson EK. Adenosine attenuates reperfusion injury following regional myocardial ischaemia. Cardiovasc Res. 1993;27(1):9–17.PubMedGoogle Scholar
  52. 52.
    Mahaffey KW, Puma JA, Barbagelata NA, DiCarli MF, Leesar MA, Browne KF, Eisenberg PR, Bolli R, Casas AC, Molina-Viamonte V, Orlandi C, Blevins R, Gibbons RJ, Califf RM, Granger CB. Adenosine as an adjunct to thrombolytic therapy for acute myocardial infarction: results of a multicenter, randomized, placebo-controlled trial: the Acute Myocardial Infarction STudy of ADenosine (AMISTAD) trial. J Am Coll Cardiol. 1999;34(6):1711–20.PubMedGoogle Scholar
  53. 53.
    Ross AM, Gibbons RJ, Stone GW, Kloner RA, Alexander RW, AMISTAD-II Investigators. A randomized, double-blinded, placebo-controlled multicenter trial of adenosine as an adjunct to reperfusion in the treatment of acute myocardial infarction (AMISTAD-II). J Am Coll Cardiol. 2005;45(11):1775–80.PubMedGoogle Scholar
  54. 54.
    Maines MD, Mayer RD, Ewing JF, McCoubrey WK Jr. Induction of kidney heme oxygenase-1 (HSP32) mRNA and protein by ischemia/reperfusion: possible role of heme as both promotor of tissue damage and regulator of HSP32. J Pharmacol Exp Ther. 1993;264(1):457–62.PubMedGoogle Scholar
  55. 55.
    Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86(2):583–650.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Misra HP, Fridovich I. The generation of superoxide radical during the autoxidation of hemoglobin. J Biol Chem. 1972;247(21):6960–2.PubMedGoogle Scholar
  57. 57.
    Ward R, Souder N, Stahl D, Hunter F, Probe R, Chaput C, Childs E. The role of nitric oxide synthase and heme oxygenase in the protective effect of hypothermia in ischemia-reperfusion injury. J Bone Joint Surg Am. 2009;91(11):2637–45.PubMedGoogle Scholar
  58. 58.
    Laws PE, Spark JI, Cowled PA, Fitridge RA. The role of statins in vascular disease. Eur J Vasc Endovasc Surg. 2004;27(1):6–16.PubMedGoogle Scholar
  59. 59.
    Cowled PA, Khanna A, Laws PE, Field JB, Varelias A, Fitridge RA. Statins inhibit neutrophil infiltration in skeletal muscle reperfusion injury. J Surg Res. 2007;141(2):267–76.PubMedGoogle Scholar
  60. 60.
    Dillon JP, Laing AJ, Chandler JR, Wang JH, McGuinness A, Redmond HP. Pravastatin attenuates tourniquet-induced skeletal muscle ischemia reperfusion injury. Acta Orthop. 2006;77(1):27–32.PubMedGoogle Scholar
  61. 61.
    Black JH, Davison JK, Cambria RP. Regional hypothermia with epidural cooling for prevention of spinal cord ischemic complications after thoracoabdominal aortic surgery. Semin Thorac Cardiovasc Surg. 2003;15(4):345–52.PubMedGoogle Scholar
  62. 62.
    Cambria RP, Davison JK, Carter C, Brewster DC, Chang Y, Clark KA, Atamian S. Epidural cooling for spinal cord protection during thoracoabdominal aneurysm repair: a five-year experience. J Vasc Surg. 2000;31(6):1093–102.PubMedGoogle Scholar
  63. 63.
    Wright JG, Kerr JC, Valeri CR, Hobson RW. Regional hypothermia protects against ischemia-reperfusion injury in isolated canine gracilis muscle. J Trauma. 1988;28(7):1026–31.PubMedGoogle Scholar
  64. 64.
    Stahl D, Souder N, Probe R, Sampson W, Tharakan B, Ward R. The effects of hypothermia and L-arginine on skeletal muscle function in ischemia-reperfusion injury. J Orthop Trauma. 2012;26(10):579–84.PubMedGoogle Scholar
  65. 65.
    Polderman KH. Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med. 2009;37(7 Suppl):S186–202.PubMedGoogle Scholar
  66. 66.
    Kharbanda RK. Cardiac conditioning: a review of evolving strategies to reduce ischaemia-reperfusion injury. Heart. 2010;96(15):1179–86.PubMedGoogle Scholar
  67. 67.
    Menting TP, Wever KE, Ozdemir-van Brunschot DM, Van der Vliet DJ, Rovers MM, Warle MC. Ischaemic preconditioning for the reduction of renal ischaemia reperfusion injury. Cochrane Database Syst Rev. 2017;3:CD010777.PubMedGoogle Scholar
  68. 68.
    Khan AR, Binabdulhak AA, Alastal Y, Khan S, Faricy-Beredo BM, Luni FK, Lee WM, Khuder S, Tinkel J. Cardioprotective role of ischemic postconditioning in acute myocardial infarction: a systematic review and meta-analysis. Am Heart J. 2014;168(4):512–521.e4.PubMedGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.The Department of Surgery, Walter Reed National Military Medical CenterUniformed Services University of the Health SciencesBethesdaUSA

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