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Neurogenic Stunned Myocardium in Severe Neurological Injury

  • Benjamin B. Kenigsberg
  • Christopher F. Barnett
  • Jeffrey C. Mai
  • Jason J. ChangEmail author
Critical Care (Stephan A. Mayer, Section Editor)
  • 52 Downloads
Part of the following topical collections:
  1. Topical Collection on Critical Care

Abstract

Purpose of Review

Neurogenic stunned myocardium (NSM) is a poorly recognized cardiac manifestation of neurological illness. This review addresses the contemporary understanding of NSM pathophysiology, epidemiology, diagnosis, and clinical management.

Recent Findings

While the precise pathophysiology and diagnosis remain unclear, NSM is phenotypically atypical stress cardiomyopathy that can be partially attributed to excess catecholaminergic toxicity. NSM is a diagnosis of exclusion where electrocardiography, echocardiography, and cardiac biomarkers are frequently abnormal. Clinical expertise is crucial to evaluate and differentiate NSM from acute coronary syndrome and in the evaluation of potential cardiac transplantation donors after unsalvageable severe neurological injury.

Summary

Neurogenic stunned myocardium is a relatively common and clinically impactful condition. More research is needed, particularly to refine clinical prognostication of NSM and rule out intrinsic cardiac injury in order to optimize donor candidacy in the event of brain death.

Keywords

Neurogenic stunned myocardium Stress cardiomyopathy Takotsubo cardiomyopathy Subarachnoid hemorrhage Severe traumatic brain injury 

Notes

Compliance with Ethical Standards

Conflict of Interest

Benjamin B. Kenigsberg, Christopher F. Barnett, Jeffrey C. Mai, and Jason J. Chang each declare no potential conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Kerro A, Woods T, Chang JJ. Neurogenic stunned myocardium in subarachnoid hemorrhage. J Crit Care. 2017;38:27–34.PubMedGoogle Scholar
  2. 2.
    Krishnamoorthy V, Wilson T, Sharma D, Vavilala MS. Prolonged cardiac dysfunction after intraparenchymal hemorrhage and neurogenic stunned myocardium. A A Case Rep. 2016;6:3–5.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Cheah CF, Kofler M, Schiefecker AJ, Beer R, Klug G, Pfausler B, et al. Takotsubo cardiomyopathy in traumatic brain injury. Neurocrit Care. 2017;26:284–91.PubMedGoogle Scholar
  4. 4.
    Murthy SB, Shah S, Venkatasubba Rao CP, Suarez JI, Bershad EM. Clinical characteristics of myocardial stunning in acute stroke. J Clin Neurosci. 2014;21:1279–82.PubMedGoogle Scholar
  5. 5.
    Al-Najafi S, Rosman H. Seizure-induced myocardial stunning: a possible cardiac link to sudden unexpected death in epilepsy (SUDEP). Seizure. 2015;24:137–9.PubMedGoogle Scholar
  6. 6.
    Losonczy LI, Lovallo E, Schnorr CD, Mantuani D, et al. Am J Emerg Med. 2016;34:119.e3–4.Google Scholar
  7. 7.
    Lopez Chiriboga AS, Yoon JW, Freeman WD, Odunukan OW, Cheshire WP Jr. Takotsubo cardiomyopathy in the setting of acute hydrocephalus secondary to neurocysticercosis. Clin Auton Res. 2016;26:235–41.PubMedGoogle Scholar
  8. 8.
    Lin W-S, Sung Y-F. Neurogenic stunned myocardium as a manifestation of encephalitis involving cerebellar tonsils. Am J Emerg Med. 2012;2083(30):e1–2.Google Scholar
  9. 9.
    Beauchamp GA, McMullan JT, Bonomo JB. Neurogenic stunned myocardium associated with acute spinal cord infarction: a case report. Case Rep Crit Care. 2012;2012:439528.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Moriya S, Inamasu J, Oheda M, Hirose Y. Neurogenic stunned myocardium associated with pediatric brain tumor may not be catecholamine-induced. Ann Pediatr Cardiol. 2015;8:240.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Messina AG, Paranicas M, Katz B, Markowitz J, Yao FS, Devereux RB. Effect of electroconvulsive therapy on the electrocardiogram and echocardiogram. Anesth Analg. 1992;75:511–4.PubMedGoogle Scholar
  12. 12.
    Magid-Bernstein J, Al-Mufti F, Merkler AE, Roh D, Patel S, May TL, et al. Unexpected rapid improvement and neurogenic stunned myocardium in a patient with acute motor axonal neuropathy. J Clin Neuromuscul Dis. 2016;17:135–41.PubMedGoogle Scholar
  13. 13.
    Cushing H. Concerning a definite regulatory mechanism of the vaso-motor centre which controls blood pressure during cerebral compression. 1901.Google Scholar
  14. 14.
    Fodstad H, Kelly PJ, Buchfelder M. History of the cushing reflex. Neurosurgery. 2006;59:1132–7 discussion 1137.PubMedGoogle Scholar
  15. 15.
    Braunwald E, Kloner RA. The stunned myocardium: prolonged, postischemic ventricular dysfunction. Circulation. 1982;66:1146–9.PubMedGoogle Scholar
  16. 16.
    •• de Chazal HM, de Chazal HM, Del Buono MG, Keyser-Marcus L, Ma L, Gerard Moeller F, et al. Stress cardiomyopathy diagnosis and treatment. J Am Coll Cardiol. 2018;72:1955–71 This paper provides a contemporary review of stress cardiomyopathy and proposed pathophysiologic mechanisms for neurocardiogenic myocardial stunning from emotional and physical triggers. Google Scholar
  17. 17.
    Wittstein IS, Thiemann DR, Lima JAC, Baughman KL, Schulman SP, Gerstenblith G, et al. Neurohumoral features of myocardial stunning due to sudden emotional stress. N Engl J Med. 2005;352:539–48.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Ancona F, Bertoldi LF, Ruggieri F, Cerri M, Magnoni M, Beretta L, et al. Takotsubo cardiomyopathy and neurogenic stunned myocardium: similar albeit different. Eur Heart J. 2016;37:2830–2.PubMedGoogle Scholar
  19. 19.
    Kolin A, Norris JW. Myocardial damage from acute cerebral lesions. Stroke. 1984;15:990–3.PubMedGoogle Scholar
  20. 20.
    Guglin M, Omar HR, Ray G, Wright C. Prevalence, determinants, and correlates of coagulation necrosis and contraction band necrosis in donor hearts. Clin Transpl. 2019;33:e13472.Google Scholar
  21. 21.
    Inamasu J, Watanabe E, Okuda K, Kumai T, Sugimoto K, Ozaki Y, et al. Are there differences between Takotsubo cardiomyopathy and neurogenic stunned myocardium? A prospective observational study. Int J Cardiol. 2014;177:1108–10.PubMedGoogle Scholar
  22. 22.
    Bybee KA, Prasad A. Stress-related cardiomyopathy syndromes. Circulation. 2008;118:397–409.PubMedGoogle Scholar
  23. 23.
    Krishnamoorthy V, Mackensen GB, Gibbons EF, Vavilala MS. Cardiac dysfunction after neurologic injury: what do we know and where are we going? Chest. 2016;149:1325–31.PubMedGoogle Scholar
  24. 24.
    Pelliccia F, Kaski JC, Crea F, Camici PG. Pathophysiology of Takotsubo syndrome. Circulation. 2017;135:2426–41.PubMedGoogle Scholar
  25. 25.
    Angelini P. Transient left ventricular apical ballooning: a unifying pathophysiologic theory at the edge of Prinzmetal angina. Catheter Cardiovasc Interv. 2008;71:342–52.PubMedGoogle Scholar
  26. 26.
    Yuki K, Kodama Y, Onda J, Emoto K, Morimoto T, Uozumi T. Coronary vasospasm following subarachnoid hemorrhage as a cause of stunned myocardium. Case report. J Neurosurg. 1991;75:308–11.PubMedGoogle Scholar
  27. 27.
    Galiuto L, De Caterina AR, Porfidia A, Paraggio L, Barchetta S, Locorotondo G, et al. Reversible coronary microvascular dysfunction: a common pathogenetic mechanism in apical ballooning or Tako-Tsubo syndrome. Eur Heart J. 2010;31:1319–27.PubMedGoogle Scholar
  28. 28.
    Naegele M, Flammer AJ, Enseleit F, Roas S, Frank M, Hirt A, et al. Endothelial function and sympathetic nervous system activity in patients with Takotsubo syndrome. Int J Cardiol. 2016;224:226–30.PubMedGoogle Scholar
  29. 29.
    Heusch G, Baumgart D, Camici P, Chilian W, Gregorini L, Hess O, et al. Alpha-adrenergic coronary vasoconstriction and myocardial ischemia in humans. Circulation. 2000;101:689–94.PubMedGoogle Scholar
  30. 30.
    Natelson BH, Suarez RV, Terrence CF, Turizo R. Patients with epilepsy who die suddenly have cardiac disease. Arch Neurol. 1998;55:857–60.PubMedGoogle Scholar
  31. 31.
    Van Bogaert A, Van Bogaert PP, Boddin M, Dierick W, Wellens D, De Wilde A. Vascular and noradrenalic reactions in the musculocutaneous bed during hypothalamic stimulation. Arch Int Physiol Biochim. 1975;83:309–23.PubMedGoogle Scholar
  32. 32.
    Banki NM, Kopelnik A, Dae MW, Miss J, Tung P, Lawton MT, et al. Acute neurocardiogenic injury after subarachnoid hemorrhage. Circulation. 2005;112:3314–9.PubMedGoogle Scholar
  33. 33.
    Novitzky D, Wicomb WN, Cooper DK, Rose AG, Reichart B. Prevention of myocardial injury during brain death by total cardiac sympathectomy in the Chacma baboon. Ann Thorac Surg. 1986;41:520–4.PubMedGoogle Scholar
  34. 34.
    Van Vliet PD, Burchell HB, Titus JL. Focal myocarditis associated with pheochromocytoma. N Engl J Med. 1966;274:1102–8.PubMedGoogle Scholar
  35. 35.
    Mann DL, Kent RL, Parsons B, Cooper G. Adrenergic effects on the biology of the adult mammalian cardiocyte. Circulation. 1992;85:790–804.PubMedGoogle Scholar
  36. 36.
    Ferreira VM, Marcelino M, Piechnik SK, Marini C, Karamitsos TD, Ntusi NAB, et al. Pheochromocytoma is characterized by catecholamine-mediated myocarditis, focal and diffuse myocardial fibrosis, and myocardial dysfunction. J Am Coll Cardiol. 2016;67:2364–74.PubMedGoogle Scholar
  37. 37.
    Zaroff JG, Pawlikowska L, Miss JC, Yarlagadda S, Ha C, Achrol A, et al. Adrenoceptor polymorphisms and the risk of cardiac injury and dysfunction after subarachnoid hemorrhage. Stroke. 2006;37:1680–5.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Shao Y, Redfors B, Ståhlman M, Täng MS, Miljanovic A, Möllmann H, et al. A mouse model reveals an important role for catecholamine-induced lipotoxicity in the pathogenesis of stress-induced cardiomyopathy. Eur J Heart Fail. 2013;15:9–22.PubMedGoogle Scholar
  39. 39.
    Beesley SJ, Weber G, Sarge T, Nikravan S, Grissom CK, Lanspa MJ, et al. Septic cardiomyopathy. Crit Care Med. 2018;46:625–34.PubMedGoogle Scholar
  40. 40.
    Chaikittisilpa N, Krishnamoorthy V, Lele AV, Qiu Q, Vavilala MS. Characterizing the relationship between systemic inflammatory response syndrome and early cardiac dysfunction in traumatic brain injury. J Neurosci Res. 2018;96:661–70.PubMedGoogle Scholar
  41. 41.
    Szabó G, Hackert T, Sebening C, Vahl CF, Hagl S. Modulation of coronary perfusion pressure can reverse cardiac dysfunction after brain death. Ann Thorac Surg. 1999;67:18–25 discussion 25–6.PubMedGoogle Scholar
  42. 42.
    Ranasinghe AM, Bonser RS. Endocrine changes in brain death and transplantation. Best Pract Res Clin Endocrinol Metab. 2011;25:799–812.PubMedGoogle Scholar
  43. 43.
    Templin C, Hänggi J, Klein C, Topka MS, Hiestand T, Levinson RA, et al. Altered limbic and autonomic processing supports brain-heart axis in Takotsubo syndrome. Eur Heart J. 2019;40:1183–7.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Dujardin KS, McCully RB, Wijdicks EF, Tazelaar HD, Seward JB, McGregor CG, et al. Myocardial dysfunction associated with brain death: clinical, echocardiographic, and pathologic features. J Heart Lung Transplant. 2001;20:350–7.PubMedGoogle Scholar
  45. 45.
    Banki N, Kopelnik A, Tung P, Lawton MT, Gress D, Drew B, et al. Prospective analysis of prevalence, distribution, and rate of recovery of left ventricular systolic dysfunction in patients with subarachnoid hemorrhage. J Neurosurg. 2006;105:15–20.PubMedGoogle Scholar
  46. 46.
    Prathep S, Sharma D, Hallman M, Joffe A, Krishnamoorthy V, Mackensen GB, et al. Preliminary report on cardiac dysfunction after isolated traumatic brain injury. Crit Care Med. 2014;42:142–7.PubMedGoogle Scholar
  47. 47.
    Yoshimura S, Toyoda K, Ohara T, Nagasawa H, Ohtani N, Kuwashiro T, et al. Takotsubo cardiomyopathy in acute ischemic stroke. Ann Neurol. 2008;64:547–54.PubMedGoogle Scholar
  48. 48.
    • Krishnamoorthy V, Rowhani-Rahbar A, Gibbons EF, Rivara FP, Temkin NR, Pontius C, et al. Early systolic dysfunction following traumatic brain injury: a cohort study. Crit Care Med. 2017;45:1028–36 This prospective cohort study assessed cardiac function with screening transthoracic echocardiograms after traumatic brain injury. Incident early systolic dysfunction occurred only in patients with at least moderate severity brain injury and resolved within 1 week. PubMedPubMedCentralGoogle Scholar
  49. 49.
    Kothavale A, Banki NM, Kopelnik A, Yarlagadda S, Lawton MT, Ko N, et al. Predictors of left ventricular regional wall motion abnormalities after subarachnoid hemorrhage. Neurocrit Care. 2006;4:199–205.PubMedGoogle Scholar
  50. 50.
    Kilbourn KJ, Levy S, Staff I, Kureshi I, McCullough L. Clinical characteristics and outcomes of neurogenic stress cardiomyopathy in aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2013;115:909–14.PubMedGoogle Scholar
  51. 51.
    Malik AN, Gross BA, Rosalind Lai PM, Moses ZB, Du R. Neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2015;83:880–5.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Chen Z, Venkat P, Seyfried D, Chopp M, Yan T, Chen J. Brain-heart interaction: cardiac complications after stroke. Circ Res. 2017;121:451–68.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Thygesen K, Alpert JS, Jaffe AS, Chaitman BR, Bax JJ, Morrow DA, et al. Fourth universal definition of myocardial infarction (2018). Circulation. 2018;138:e618–51.PubMedGoogle Scholar
  54. 54.
    Jangra K, Grover VK, Bhagat H, Bhardwaj A, Tewari MK, Kumar B, et al. Evaluation of the effect of aneurysmal clipping on electrocardiography and echocardiographic changes in patients with subarachnoid hemorrhage: a prospective observational study. J Neurosurg Anesthesiol. 2017;29:335–40.PubMedGoogle Scholar
  55. 55.
    Bulsara KR, McGirt MJ, Liao L, Villavicencio AT, Borel C, Alexander MJ, et al. Use of the peak troponin value to differentiate myocardial infarction from reversible neurogenic left ventricular dysfunction associated with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2003;98:524–8.PubMedGoogle Scholar
  56. 56.
    Parekh N, Venkatesh B, Cross D, Leditschke A, Atherton J, Miles W, et al. Cardiac troponin I predicts myocardial dysfunction in aneurysmal subarachnoid hemorrhage. J Am Coll Cardiol. 2000;36:1328–35.PubMedGoogle Scholar
  57. 57.
    Cheng C-Y, Hsu C-Y, Wang T-C, Jeng Y-C, Yang W-H. Evaluation of cardiac complications following hemorrhagic stroke using 5-year centers for disease control and prevention (CDC) database. J Clin Med Res. 2018;7.  https://doi.org/10.3390/jcm7120519.PubMedCentralGoogle Scholar
  58. 58.
    Yu Z, Fan B, Wu H, Wang X, Li C, Xu R, et al. Multiple systemic embolism in infective endocarditis underlying in Barlow’s disease. BMC Infect Dis. 2016;16:403.  https://doi.org/10.1186/s12879-016-1726-5.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    • Ghadri JR, Wittstein IS, Prasad A, Sharkey S, Dote K, Akashi YJ, et al. International expert consensus document on Takotsubo syndrome (part I): clinical characteristics, diagnostic criteria, and pathophysiology. Eur Heart J. 2018;39:2032–46 This clinical expert consensus document updated diagnostic criteria for stress cardiomyopathy and included acute neurological disorders as a predisposing trigger. PubMedPubMedCentralGoogle Scholar
  60. 60.
    Ghadri JR, Cammann VL, Jurisic S, Seifert B, Napp LC, Diekmann J, et al. A novel clinical score (InterTAK Diagnostic Score) to differentiate takotsubo syndrome from acute coronary syndrome: results from the International Takotsubo Registry. Eur J Heart Fail. 2017;19:1036–42.PubMedGoogle Scholar
  61. 61.
    Burch GE, Meyers R, Abildskov JA. A new electrocardiographic pattern observed in cerebrovascular accidents. Circulation. 1954;9:719–23.PubMedGoogle Scholar
  62. 62.
    de Zwaan C, Bär FW, Wellens HJ. Characteristic electrocardiographic pattern indicating a critical stenosis high in left anterior descending coronary artery in patients admitted because of impending myocardial infarction. Am Heart J. 1982;103:730–6.PubMedGoogle Scholar
  63. 63.
    Chen W-L, Huang C-H, Chen J-H, Tai HC-H, Chang S-H, Wang Y-C. ECG abnormalities predict neurogenic pulmonary edema in patients with subarachnoid hemorrhage. Am J Emerg Med. 2016;34:79–82.PubMedGoogle Scholar
  64. 64.
    Khechinashvili G, Asplund K. Electrocardiographic changes in patients with acute stroke: a systematic review. Cerebrovasc Dis. 2002;14:67–76.PubMedGoogle Scholar
  65. 65.
    Zaroff JG, Rordorf GA, Ogilvy CS, Picard MH. Regional patterns of left ventricular systolic dysfunction after subarachnoid hemorrhage: evidence for neurally mediated cardiac injury. J Am Soc Echocardiogr. 2000;13:774–9.PubMedGoogle Scholar
  66. 66.
    Citro R, Lyon AR, Meimoun P, Omerovic E, Redfors B, Buck T, et al. Standard and advanced echocardiography in takotsubo (stress) cardiomyopathy: clinical and prognostic implications. J Am Soc Echocardiogr. 2015;28:57–74.PubMedGoogle Scholar
  67. 67.
    Kono T, Morita H, Kuroiwa T, Onaka H, Takatsuka H, Fujiwara A. Left ventricular wall motion abnormalities in patients with subarachnoid hemorrhage: neurogenic stunned myocardium. J Am Coll Cardiol. 1994;24:636–40.PubMedGoogle Scholar
  68. 68.
    Abd TT, Hayek S, Cheng J-W, Samuels OB, Wittstein IS, Lerakis S. Incidence and clinical characteristics of takotsubo cardiomyopathy post-aneurysmal subarachnoid hemorrhage. Int J Cardiol. 2014;176:1362–4.PubMedGoogle Scholar
  69. 69.
    Cinotti R, Piriou N, Launey Y, Le Tourneau T, Lamer M, Delater A, et al. Speckle tracking analysis allows sensitive detection of stress cardiomyopathy in severe aneurysmal subarachnoid hemorrhage patients. Intensive Care Med. 2016;42:173–82.PubMedGoogle Scholar
  70. 70.
    Cai L, Addetia K, Medvedofsky D, Spencer KT. Myocardial strain may be useful in differentiating Takotsubo cardiomyopathy from left anterior descending coronary artery ischemia. Int J Cardiol. 2017;230:359–63.PubMedGoogle Scholar
  71. 71.
    • Kagiyama N, Sugahara M, Crago EA, Qi Z, Lagattuta TF, Yousef KM, et al. Neurocardiac injury assessed by strain imaging is associated with in-hospital mortality in patients with subarachnoid hemorrhage. JACC Cardiovasc Imaging. 2019.  https://doi.org/10.1016/j.jcmg.2019.02.023 This prospective cohort study assessed speckle tracking strain echocardiography after acute subarachnoid hemorrhage. Left ventricular global longitudinal strain and right ventricular strain abnormalities associated with in-hospital mortality after SAH.
  72. 72.
    Asch FM, Medvedofsky D. Myocardial strain, subarachnoid hemorrhage, and the expanding spectrum of stress-induced cardiomyopathy. JACC Cardiovasc Imaging. 2019.  https://doi.org/10.1016/j.jcmg.2019.03.014.
  73. 73.
    Liesirova K, Abela E, Pilgrim T, Bickel L, Meinel T, Meisterernst J, et al. Baseline troponin T level in stroke and its association with stress cardiomyopathy. PLoS One. 2018;13:e0209764.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Bustamante A, Díaz-Fernández B, Pagola J, Blanco-Grau A, Rubiera M, Penalba A, et al. Admission troponin-I predicts subsequent cardiac complications and mortality in acute stroke patients. Eur Stroke J. 2016;1:205–12.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Salim A, Hadjizacharia P, Brown C, Inaba K, Teixeira PGR, Chan L, et al. Significance of troponin elevation after severe traumatic brain injury. J Trauma. 2008;64:46–52.PubMedGoogle Scholar
  76. 76.
    El-Menyar A, Sathian B, Wahlen BM, Al-Thani H. Serum cardiac troponins as prognostic markers in patients with traumatic and non-traumatic brain injuries: a meta-analysis. Am J Emerg Med. 2019;37:133–42.PubMedGoogle Scholar
  77. 77.
    van der Bilt IA, Hasan D, van den Brink RB, Cramer MJ, van der Jagt M, van Kooten F, et al. Time course and risk factors for myocardial dysfunction after aneurysmal subarachnoid hemorrhage. Neurosurgery. 2015;76:700–5 discussion 705–6.PubMedGoogle Scholar
  78. 78.
    Tung P, Kopelnik A, Banki N, Ong K, Ko N, Lawton MT, et al. Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke. 2004;35:548–51.PubMedGoogle Scholar
  79. 79.
    Duello KM, Nagel JP, Thomas CS, Blackshear JL, Freeman WD. Relationship of troponin T and age- and sex-adjusted BNP elevation following subarachnoid hemorrhage with 30-day mortality. Neurocrit Care. 2015;23:59–65.PubMedGoogle Scholar
  80. 80.
    Amsterdam EA, Wenger NK, Brindis RG, Casey DE Jr, Ganiats TG, Holmes DR Jr, et al. 2014 AHA/ACC guideline for the management of patients with non-ST-elevation acute coronary syndromes: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014;64:e139–228.PubMedGoogle Scholar
  81. 81.
    SCOT-HEART Investigators, Newby DE, Adamson PD, Berry C, Boon NA, Dweck MR, et al. Coronary CT angiography and 5-year risk of myocardial infarction. N Engl J Med. 2018;379:924–33.Google Scholar
  82. 82.
    Luo H, Song W-X, Jiang J-W, Zhao J-L, Rong W-L, Li M-H. Effects of preadmission beta-blockers on neurogenic stunned myocardium after aneurysmal subarachnoid hemorrhage: a meta- analysis. Clin Neurol Neurosurg. 2017;158:77–81.PubMedGoogle Scholar
  83. 83.
    Neil-Dwyer G, Walter P, Cruickshank JM, Doshi B, O’Gorman P. Effect of propranolol and phentolamine on myocardial necrosis after subarachnoid haemorrhage. Br Med J. 1978;2:990–2.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Colvin MM, et al. 2017 ACC/AHA/HFSA focused update of the 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines and the Heart Failure Society of America. J Card Fail. 2017;23:628–51.PubMedGoogle Scholar
  85. 85.
    St-Onge M, Anseeuw K, Cantrell FL, Gilchrist IC, Hantson P, Bailey B, et al. Experts consensus recommendations for the management of calcium channel blocker poisoning in adults. Crit Care Med. 2017;45:e306–15.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Vanderschuren A, Hantson P. Hyperinsulinemic euglycemia therapy for stunned myocardium following subarachnoid hemorrhage. J Neurosurg. 2009;110:64–6.PubMedGoogle Scholar
  87. 87.
    Chandler BT, Pernu P. Hyperinsulinaemic euglycaemic therapy use in neurogenic stunned myocardium following subarachnoid haemorrhage. Anaesth Intensive Care. 2018;46:575–8.PubMedGoogle Scholar
  88. 88.
    Frontera JA, Parra A, Shimbo D, Fernandez A, Schmidt JM, Peter P, et al. Cardiac arrhythmias after subarachnoid hemorrhage: risk factors and impact on outcome. Cerebrovasc Dis. 2008;26:71–8.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Taggart P, Critchley H, Lambiase PD. Heart-brain interactions in cardiac arrhythmia. Heart. 2011;97:698–708.PubMedGoogle Scholar
  90. 90.
    Taccone FS, Lubicz B, Piagnerelli M, Van Nuffelen M, Vincent J-L, De Backer D. Cardiogenic shock with stunned myocardium during triple-H therapy treated with intra-aortic balloon pump counterpulsation. Neurocrit Care. 2009;10:76–82.PubMedGoogle Scholar
  91. 91.
    Lazaridis C, Pradilla G, Nyquist PA, Tamargo RJ. Intra-aortic balloon pump counterpulsation in the setting of subarachnoid hemorrhage, cerebral vasospasm, and neurogenic stress cardiomyopathy. Case report and review of the literature. Neurocrit Care. 2010;13:101–8.PubMedGoogle Scholar
  92. 92.
    Levy ML, Rabb CH, Zelman V, Giannotta SL. Cardiac performance enhancement from dobutamine in patients refractory to hypervolemic therapy for cerebral vasospasm. J Neurosurg. 1993;79:494–9.PubMedGoogle Scholar
  93. 93.
    Naidech A, Du Y, Kreiter KT, Parra A, Fitzsimmons B-F, Lavine SD, et al. Dobutamine versus milrinone after subarachnoid hemorrhage. Neurosurgery. 2005;56:21–6l discussion 26–7.PubMedGoogle Scholar
  94. 94.
    Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, et al. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2013;62:e147–239.PubMedPubMedCentralGoogle Scholar
  95. 95.
    Ghadri JR, Kato K, Cammann VL, Gili S, Jurisic S, Di Vece D, et al. Long-term prognosis of patients with Takotsubo syndrome. J Am Coll Cardiol. 2018;72:874–82.PubMedGoogle Scholar
  96. 96.
    Pelliccia F, Pasceri V, Patti G, Tanzilli G, Speciale G, Gaudio C, et al. Long-term prognosis and outcome predictors in Takotsubo syndrome: a systematic review and meta-regression study. JACC Heart Fail. 2019;7:143–54.PubMedGoogle Scholar
  97. 97.
    van der Bilt I, Hasan D, van den Brink R, Cramer M-J, van der Jagt M, van Kooten F, et al. Cardiac dysfunction after aneurysmal subarachnoid hemorrhage: relationship with outcome. Neurology. 2014;82:351–8.PubMedGoogle Scholar
  98. 98.
    Mohamedali B, Bhat G, Tatooles A, Zelinger A. Neurogenic stress cardiomyopathy in heart donors. J Card Fail. 2014;20:207–11.PubMedGoogle Scholar
  99. 99.
    Mohamedali B, Bhat G, Zelinger A. Frequency and pattern of left ventricular dysfunction in potential heart donors: implications regarding use of dysfunctional hearts for successful transplantation. J Am Coll Cardiol. 2012;60:235–6.PubMedGoogle Scholar
  100. 100.
    • Madan S, Saeed O, Vlismas P, Katsa I, Patel SR, Shin JJ, et al. Outcomes after transplantation of donor hearts with improving left ventricular systolic dysfunction. J Am Coll Cardiol. 2017;70:1248–58 This study identified donor hearts in the United Network of Organ Sharing database with transient pre-transplant left ventricular systolic dysfunction and found comparable post-transplant clinical outcomes to transplanted hearts from donors with normal ventricular function. PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Benjamin B. Kenigsberg
    • 1
    • 2
  • Christopher F. Barnett
    • 1
    • 2
  • Jeffrey C. Mai
    • 3
  • Jason J. Chang
    • 1
    • 4
    Email author
  1. 1.Department of Critical Care MedicineMedStar Washington Hospital CenterWashingtonUSA
  2. 2.Department of CardiologyMedStar Washington Hospital CenterWashingtonUSA
  3. 3.Department of NeurosurgeryGeorgetown University and MedStar Washington Hospital CenterWashingtonUSA
  4. 4.Department of NeurologyGeorgetown University School of MedicineWashingtonUSA

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