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Cortical Spreading Depolarizations in Aneurysmal Subarachnoid Hemorrhage: An Overview of Current Knowledge and Future Perspectives

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Advances and Technical Standards in Neurosurgery

Part of the book series: Advances and Technical Standards in Neurosurgery ((NEUROSURGERY,volume 45))

Abstract

Despite significant advances in the management of aneurysmal subarachnoid hemorrhage (SAH), morbidity and mortality remain devastating particularly for high-grade SAH. Poor functional outcome usually results from delayed cerebral ischemia (DCI). The pathogenesis of DCI during aneurysmal SAH has historically been attributed to cerebral vasospasm, but spreading depolarizations (SDs) are now considered to play a central role in DCI. During SAH, SDs may produce an inverse hemodynamic response leading to spreading ischemia. Several animal models have contributed to a better understanding of the pathogenesis of SDs during aneurysmal SAH and provided new therapeutic approaches including N-methyl-d-aspartate receptor antagonists and phosphodiesterase inhibitors. Herein we review the current knowledge in the field of SDs’ pathogenesis and we detail the key experimental and clinical studies that have opened interesting new therapeutic approaches to prevent DCI in aneurysmal SAH.

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References

  1. Francoeur CL, Mayer SA. Management of delayed cerebral ischemia after subarachnoid hemorrhage. Crit Care. 2016;20:277.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Geraghty JR, Testai FD. Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Curr Atheroscler Rep. 2017;19:50.

    Article  PubMed  CAS  Google Scholar 

  3. Serrone JC, Maekawa H, Tjahjadi M, Hernesniemi J. Aneurysmal subarachnoid hemorrhage: pathobiology, current treatment and future directions. Expert Rev Neurother. 2015;15:367–80.

    Article  CAS  PubMed  Google Scholar 

  4. James RF, Kramer DR, Aljuboori ZS, Parikh G, Adams SW, Eaton JC, Abou Al-Shaar H, Badjatia N, Mack WJ, Simard JM. Novel treatments in neuroprotection for aneurysmal subarachnoid hemorrhage. Curr Treat Options Neurol. 2016;18:38.

    Article  PubMed  Google Scholar 

  5. Chung DY, Sugimoto K, Fischer P, et al. Real-time non-invasive in vivo visible light detection of cortical spreading depolarizations in mice. J Neurosci Methods. 2018;309:143–6.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sugimoto K, Chung DY. Spreading depolarizations and subarachnoid Hemorrhage. Neurotherapeutics. 2020;17:497–510.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dreier JP, Fabricius M, Ayata C, et al. Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: review and recommendations of the COSBID research group. J Cereb Blood Flow Metab. 2017;37:1595–625.

    Article  PubMed  Google Scholar 

  8. Dreier JP, Major S, Manning A, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain. 2009;132:1866–81.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Shuttleworth CW, Andrew RD, Akbari Y, et al. Which spreading depolarizations are deleterious to brain tissue? Neurocrit Care. 2020;32:317–22.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Leao AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–90.

    Article  Google Scholar 

  11. Leo AA. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol. 1947;10:409–14.

    Article  Google Scholar 

  12. Harris RJ, Symon L, Branston NM, Bayhan M. Changes in extracellular calcium activity in cerebral ischaemia. J Cereb Blood Flow Metab. 1981;1:203–9.

    Article  CAS  PubMed  Google Scholar 

  13. Hansen AJ. The extracellular potassium concentration in brain cortex following ischemia in hypo- and hyperglycemic rats. Acta Physiol Scand. 1978;102:324–9.

    Article  CAS  PubMed  Google Scholar 

  14. Hartings JA, Li C, Hinzman JM, Shuttleworth CW, Ernst GL, Dreier JP, Wilson JA, Andaluz N, Foreman B, Carlson AP. Direct current electrocorticography for clinical neuromonitoring of spreading depolarizations. J Cereb Blood Flow Metab. 2017;37:1857–70.

    Article  PubMed  Google Scholar 

  15. Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med. 2011;17:439–47.

    Article  CAS  PubMed  Google Scholar 

  16. Somjen GG. Ions in the brain: normal function, seizures, and stroke. New York: OUP USA; 2004.

    Google Scholar 

  17. Menyhárt Á, Frank R, Farkas AE, et al. Malignant astrocyte swelling and impaired glutamate clearance drive the expansion of injurious spreading depolarization foci. J Cereb Blood Flow Metab. 2020;42(4):584–99.

    Article  Google Scholar 

  18. Herreras O, Makarova J. Mechanisms of the negative potential associated with Leão’s spreading depolarization: a history of brain electrogenesis. J Cereb Blood Flow Metab. 2020;40:1934–52.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Makarova J, Gómez-Galán M, Herreras O. Variations in tissue resistivity and in the extension of activated neuron domains shape the voltage signal during spreading depression in the CA1 in vivo. Eur J Neurosci. 2008;27:444–56.

    Article  PubMed  Google Scholar 

  20. Dreier JP, Isele T, Reiffurth C, Offenhauser N, Kirov SA, Dahlem MA, Herreras O. Is spreading depolarization characterized by an abrupt, massive release of Gibbs free energy from the human brain cortex? Neuroscientist. 2013;19:25–42.

    Article  PubMed  Google Scholar 

  21. Kirov SA, Fomitcheva IV, Sword J. Rapid neuronal ultrastructure disruption and recovery during spreading depolarization-induced cytotoxic edema. Cereb Cortex. 2020;30:5517–31.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Risher WC, Ard D, Yuan J, Kirov SA. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci. 2010;30:9859–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Van Harreveld A. Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle. J Neurochem. 1959;3:300–15.

    Article  Google Scholar 

  24. Rogers ML, Feuerstein D, Leong CL, Takagaki M, Niu X, Graf R, Boutelle MG. Continuous online microdialysis using microfluidic sensors: dynamic neurometabolic changes during spreading depolarization. ACS Chem Neurosci. 2013;4:799–807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hinzman JM, DiNapoli VA, Mahoney EJ, Gerhardt GA, Hartings JA. Spreading depolarizations mediate excitotoxicity in the development of acute cortical lesions. Exp Neurol. 2015;267:243–53.

    Article  PubMed  Google Scholar 

  26. Cesarini KG, Enblad P, Ronne-Engström E, Marklund N, Salci K, Nilsson P, Hårdemark H-G, Hillered L, Persson L. Early cerebral hyperglycolysis after subarachnoid haemorrhage correlates with favourable outcome. Acta Neurochir. 2002;144:1121–31.

    Article  CAS  PubMed  Google Scholar 

  27. Balança B, Meiller A, Bezin L, Dreier JP, Marinesco S, Lieutaud T. Altered hypermetabolic response to cortical spreading depolarizations after traumatic brain injury in rats. J Cereb Blood Flow Metab. 2017;37:1670–86.

    Article  PubMed  Google Scholar 

  28. Leo AAP. Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:391–6.

    Article  Google Scholar 

  29. Kao Y-CJ, Li W, Lai H-Y, Oyarzabal EA, Lin W, Shih Y-YI. Dynamic perfusion and diffusion MRI of cortical spreading depolarization in photothrombotic ischemia. Neurobiol Dis. 2014;71:131–9.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sukhotinsky I, Dilekoz E, Moskowitz MA, Ayata C. Hypoxia and hypotension transform the blood flow response to cortical spreading depression from hyperemia into hypoperfusion in the rat. J Cereb Blood Flow Metab. 2008;28:1369–76.

    Article  PubMed  Google Scholar 

  31. Shin HK, Dunn AK, Jones PB, Boas DA, Moskowitz MA, Ayata C. Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. J Cereb Blood Flow Metab. 2006;26:1018–30.

    Article  PubMed  Google Scholar 

  32. Feuerstein D, Takagaki M, Gramer M, Manning A, Endepols H, Vollmar S, Yoshimine T, Strong AJ, Graf R, Backes H. Detecting tissue deterioration after brain injury: regional blood flow level versus capacity to raise blood flow. J Cereb Blood Flow Metab. 2014;34:1117–27.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Bere Z, Obrenovitch TP, Kozák G, Bari F, Farkas E. Imaging reveals the focal area of spreading depolarizations and a variety of hemodynamic responses in a rat microembolic stroke model. J Cereb Blood Flow Metab. 2014;34:1695–705.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Dreier JP, Körner K, Ebert N, et al. Nitric oxide scavenging by hemoglobin or nitric oxide synthase inhibition by N-nitro-l-arginine induces cortical spreading ischemia when K+ is increased in the subarachnoid space. J Cereb Blood Flow Metab. 1998;18:978–90.

    Article  CAS  PubMed  Google Scholar 

  35. Dreier JP, Ebert N, Priller J, et al. Products of hemolysis in the subarachnoid space inducing spreading ischemia in the cortex and focal necrosis in rats: a model for delayed ischemic neurological deficits after subarachnoid hemorrhage? J Neurosurg. 2000;93:658–66.

    Article  CAS  PubMed  Google Scholar 

  36. Petzold GC, Windmüller O, Haack S, et al. Increased extracellular K+ concentration reduces the efficacy of N-methyl-d-aspartate receptor antagonists to block spreading depression-like depolarizations and spreading ischemia. Stroke. 2005;36:1270–7.

    Article  CAS  PubMed  Google Scholar 

  37. Dreier JP, Windmüller O, Petzold G, Lindauer U, Einhäupl KM, Dirnagl U. Ischemia triggered by red blood cell products in the subarachnoid space is inhibited by nimodipine administration or moderate volume expansion/hemodilution in rats. Neurosurgery. 2002;51:1457–65. discussion 1465–1467

    Article  PubMed  Google Scholar 

  38. Sugimoto K, Nomura S, Shirao S, et al. Cilostazol decreases duration of spreading depolarization and spreading ischemia after aneurysmal subarachnoid hemorrhage. Ann Neurol. 2018;84:873–85.

    Article  CAS  PubMed  Google Scholar 

  39. Hamming AM, van der Toorn A, Rudrapatna US, et al. Valproate reduces delayed brain injury in a rat model of subarachnoid hemorrhage. Stroke. 2017;48:452–8.

    Article  CAS  PubMed  Google Scholar 

  40. Woitzik J, Hecht N, Pinczolits A, et al. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology. 2013;80:1095–102.

    Article  PubMed  Google Scholar 

  41. Santos E, Schöll M, Sánchez-Porras R, Dahlem MA, Silos H, Unterberg A, Dickhaus H, Sakowitz OW. Radial, spiral and reverberating waves of spreading depolarization occur in the gyrencephalic brain. Neuroimage. 2014;99:244–55.

    Article  PubMed  Google Scholar 

  42. Helbok R, Hartings JA, Schiefecker A, et al. What should a clinician do when spreading depolarizations are observed in a patient? Neurocrit Care. 2020;32:306–10.

    Article  PubMed  Google Scholar 

  43. Dreier JP, Woitzik J, Fabricius M, et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006;129:3224–37.

    Article  PubMed  Google Scholar 

  44. Hossmann KA. Viability thresholds and the penumbra of focal ischemia. Ann Neurol. 1994;36:557–65.

    Article  CAS  PubMed  Google Scholar 

  45. Lückl J, Lemale CL, Kola V, et al. The negative ultraslow potential, electrophysiological correlate of infarction in the human cortex. Brain. 2018;141:1734–52.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Dreier JP, Major S, Pannek H-W, et al. Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain. 2012;135:259–75.

    Article  PubMed  Google Scholar 

  47. Hartings JA, Wilson JA, Look AC, Vagal A, Shutter LA, Dreier JP, Ringer A, Zuccarello M. Full-band electrocorticography of spreading depolarizations in patients with aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl. 2013;115:131–41.

    PubMed  Google Scholar 

  48. Woitzik J, Dreier JP, Hecht N, et al. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2012;32:203–12.

    Article  PubMed  Google Scholar 

  49. Sugimoto K, Shirao S, Koizumi H, et al. Continuous monitoring of spreading depolarization and cerebrovascular autoregulation after aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis. 2016;25:e171–7.

    Article  PubMed  Google Scholar 

  50. von Bornstädt D, Houben T, Seidel JL, et al. Supply-demand mismatch transients in susceptible peri-infarct hot zones explain the origins of spreading injury depolarizations. Neuron. 2015;85:1117–31.

    Article  CAS  Google Scholar 

  51. Bosche B, Graf R, Ernestus R-I, Dohmen C, Reithmeier T, Brinker G, Strong AJ, Dreier JP, Woitzik J, Members of the Cooperative Study of Brain Injury Depolarizations (COSBID). Recurrent spreading depolarizations after subarachnoid hemorrhage decreases oxygen availability in human cerebral cortex. Ann Neurol. 2010;67:607–17.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Seule M, Keller E, Unterberg A, Sakowitz O. The hemodynamic response of spreading depolarization observed by near infrared spectroscopy after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2015;23:108–12.

    Article  CAS  PubMed  Google Scholar 

  53. Sarrafzadeh A, Santos E, Wiesenthal D, Martus P, Vajkoczy P, Oehmchen M, Unterberg A, Dreier JP, Sakowitz O. Cerebral glucose and spreading depolarization in patients with aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl. 2013;115:143–7.

    PubMed  Google Scholar 

  54. Mayevsky A, Doron A, Manor T, Meilin S, Zarchin N, Ouaknine GE. Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Res. 1996;740:268–74.

    Article  CAS  PubMed  Google Scholar 

  55. Strong AJ, Fabricius M, Boutelle MG, Hibbins SJ, Hopwood SE, Jones R, Parkin MC, Lauritzen M. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke. 2002;33:2738–43.

    Article  PubMed  Google Scholar 

  56. Drenckhahn C, Winkler MKL, Major S, et al. Correlates of spreading depolarization in human scalp electroencephalography. Brain. 2012;135:853–68.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Hofmeijer J, van Kaam CR, van de Werff B, Vermeer SE, Tjepkema-Cloostermans MC, van Putten MJAM. Detecting cortical spreading depolarization with full band scalp electroencephalography: an illusion? Front Neurol. 2018;9:17.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Dreier JP, Major S, Lemale CL, Kola V, Reiffurth C, Schoknecht K, Hecht N, Hartings JA, Woitzik J. Correlates of spreading depolarization, spreading depression, and negative ultraslow potential in epidural versus subdural electrocorticography. Front Neurosci. 2019;13:373.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Lehmenkühler A, Richter F. Cortical spreading depolarization (CSD) recorded from intact skin, from surface of dura mater or cortex: comparison with intracortical recordings in the neocortex of adult rats. Neurochem Res. 2020;45:34–41.

    Article  PubMed  CAS  Google Scholar 

  60. Masvidal-Codina E, Illa X, Dasilva M, et al. High-resolution mapping of infraslow cortical brain activity enabled by graphene microtransistors. Nat Mater. 2019;18:280–8.

    Article  CAS  PubMed  Google Scholar 

  61. Berhouma M, Picart T, Dumot C, et al. Alterations of cerebral microcirculation in peritumoral edema: feasibility of in vivo sidestream dark-field imaging in intracranial meningiomas. Neurooncol Adv. 2020;2:vdaa108.

    PubMed  PubMed Central  Google Scholar 

  62. Lal C, Leahy MJ. An updated review of methods and advancements in microvascular blood flow imaging. Microcirculation. 2016;23:345–63.

    Article  PubMed  Google Scholar 

  63. Balança B, Ritzenthaler T, Gobert F, Richet C, Bodonian C, Carrillon R, Terrier A, Desmurs L, Perret-Liaudet A, Dailler F. Significance and diagnostic accuracy of early S100B serum concentration after aneurysmal subarachnoid hemorrhage. J Clin Med. 2020;9:1746. https://doi.org/10.3390/jcm9061746.

    Article  CAS  PubMed Central  Google Scholar 

  64. Rass V, Helbok R. Early brain injury after poor-grade subarachnoid hemorrhage. Curr Neurol Neurosci Rep. 2019;19:78.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Vergouwen MDI, Vermeulen M, van Gijn J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41:2391–5.

    Article  PubMed  Google Scholar 

  66. Macdonald RL, Higashida RT, Keller E, et al. Clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid haemorrhage undergoing surgical clipping: a randomised, double-blind, placebo-controlled phase 3 trial (CONSCIOUS-2). Lancet Neurol. 2011;10:618–25.

    Article  CAS  PubMed  Google Scholar 

  67. Helbok R, Kurtz P, Schmidt MJ, et al. Effects of the neurological wake-up test on clinical examination, intracranial pressure, brain metabolism and brain tissue oxygenation in severely brain-injured patients. Crit Care. 2012;16:R226.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Diringer MN, Bleck TP, Claude Hemphill J, et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit Care. 2011;15:211–40.

    Article  PubMed  Google Scholar 

  69. Gathier CS, van den Bergh WM, van der Jagt M, Verweij BH, Dankbaar JW, Müller MC, Oldenbeuving AW, GJE R, AJC S, HIMALAIA Study Group. Induced hypertension for delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: a randomized clinical trial. Stroke. 2018;49:76–83.

    Article  PubMed  Google Scholar 

  70. Engquist H, Lewén A, Hillered L, Ronne-Engström E, Nilsson P, Enblad P, Rostami E. CBF changes and cerebral energy metabolism during hypervolemia, hemodilution, and hypertension therapy in patients with poor-grade subarachnoid hemorrhage. J Neurosurg. 2020;134:1–10.

    Google Scholar 

  71. Rass V, Helbok R. How to diagnose delayed cerebral ischaemia and symptomatic vasospasm and prevent cerebral infarction in patients with subarachnoid haemorrhage. Curr Opin Crit Care. 2021;27:103–14.

    Article  PubMed  Google Scholar 

  72. Sánchez-Porras R, Santos E, Schöll M, Kunzmann K, Stock C, Silos H, Unterberg AW, Sakowitz OW. Ketamine modulation of the haemodynamic response to spreading depolarization in the gyrencephalic swine brain. J Cereb Blood Flow Metab. 2017;37:1720–34.

    Article  PubMed  Google Scholar 

  73. Hertle DN, Dreier JP, Woitzik J, et al. Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain. 2012;135:2390–8.

    Article  PubMed  Google Scholar 

  74. Carlson AP, Alchbli A, Hänggi D, Macdonald RL, Shuttleworth CW. Effect of locally delivered nimodipine microparticles on spreading depolarization in aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2020;34(1):345–9. https://doi.org/10.1007/s12028-020-00935-1.

    Article  CAS  Google Scholar 

  75. Golub D, Yanai A, Darzi K, Papadopoulos J, Kaufman B. Potential consequences of high-dose infusion of ketamine for refractory status epilepticus: case reports and systematic literature review. Anaesth Intensive Care. 2018;46:516–28.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurosurgical Oncology and Vascular Neurosurgery, Pierre Wertheimer Neurological and Neurosurgical Hospital, Hospices Civils de Lyon (Lyon University Hospital), Lyon, France

    Moncef Berhouma

  2. Creatis Lab, CNRS UMR 5220, INSERM U1206, Lyon 1 University, INSA Lyon, Lyon, France

    Moncef Berhouma & Omer Faruk Eker

  3. Department of Interventional Neuroradiology, Pierre Wertheimer Neurological and Neurosurgical Hospital, Hospices Civils de Lyon (Lyon University Hospital), Lyon, France

    Omer Faruk Eker

  4. Department of Neuro-Anesthesia and Neuro-Critical Care, Pierre Wertheimer Neurological and Neurosurgical Hospital, Hospices Civils de Lyon (Lyon University Hospital), Lyon, France

    Frederic Dailler & Baptiste Balanca

  5. Department of Functional Neurology and Epileptology, Pierre Wertheimer Neurological and Neurosurgical Hospital, Hospices Civils de Lyon (Lyon University Hospital), Lyon, France

    Sylvain Rheims

  6. Lyon’s Neurosciences Research Center, INSERM U1028/CNRS, UMR 5292, University of Lyon, Lyon, France

    Sylvain Rheims & Baptiste Balanca

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  1. International Neuroscience Institute, Hannover, Germany

    Concezio Di Rocco

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Berhouma, M., Eker, O.F., Dailler, F., Rheims, S., Balanca, B. (2022). Cortical Spreading Depolarizations in Aneurysmal Subarachnoid Hemorrhage: An Overview of Current Knowledge and Future Perspectives. In: Di Rocco, C. (eds) Advances and Technical Standards in Neurosurgery. Advances and Technical Standards in Neurosurgery, vol 45. Springer, Cham. https://doi.org/10.1007/978-3-030-99166-1_7

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