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Neurocritical Care

, Volume 5, Issue 3, pp 243–249 | Cite as

Mechanisms in neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage

  • Vivien H. Lee
  • Jae K. Oh
  • Sharon L. Mulvagh
  • Eelco F. M. WijdicksEmail author
Review

Abstract

Cardiac dysfunction after aneurysmal subarachnoid hemorrhage (SAH) is often referred to as “neurogenic stunned myocardium,” which does not accurately reflect the suspected pathophysiology. We propose an alternativeterminology,” neurogenic stress cardiomyopathy,” as a more appropriate label based on our review of the current literature. This article will review the distinctive characteristics of SAH-induced cardiac dysfunction, hypotheses to explain the pathophysiology, and the supporting clinical and animal studies. Recognition of the unique features associated with SAH-induced cardiac complications allows optimal management of patients with SAH. We will also discuss the clinical and theoretical overlap of SAH-induced cardiac dysfunction with a syndrome known as tako-tsubocardiomyopathy and explore therapeutic opportunities.

Key wors

Subarachnoid hemorrhage cardiac apical ballooning tako-tsubo cardiomyopathy neurogenic stunned myocardium 

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References

  1. 1.
    Friedman JA, Pichelmann MA, Piepgras DG, et al. Pulmonary complications of aneurysmal subarachnoid hemorrhage. Neurosurgery 2003;52:1025–1031.PubMedCrossRefGoogle Scholar
  2. 2.
    Handlin LR, Kindred LH, Beauchamp GD, Vacek JL, Rowe SK. Reversible left ventricular dysfunction after subarachnoid hemorrhage. Am Heart J 1993;126:235–240.PubMedGoogle Scholar
  3. 3.
    Mayer SA, Lin J, Homma S, et al. Myocardial injury and left ventricular performance after subarachnoid hemorrhage. Stroke 1999;30:780–786.PubMedGoogle Scholar
  4. 4.
    Parekh N, Venkatesh B, Cross D, et al. Cardiac troponin I predicts myocardial dysfunction in aneurysmal subarachnoid hemorrhage. J Am Coll Cardiol 2000;36:1328–1335.PubMedCrossRefGoogle Scholar
  5. 5.
    Pollick C, Cujec B, Parker S, Tator C. Left ventricular wall motion abnormalities in subarachnoid hemorrhage: an echocardiographic study. J Am Coll Cardiol 1988;12:600–605.PubMedGoogle Scholar
  6. 6.
    Tung P, Kopelnik A, Banki N, et al. Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke 2004;35:548–551.PubMedCrossRefGoogle Scholar
  7. 7.
    Mayer SA, Fink ME, Homma S, et al. Cardiac injury associated with neurogenic pulmonary edema following subarachnoid hemorrhage. Neurology 1994;44:815–820.PubMedGoogle Scholar
  8. 8.
    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;13:774–779.PubMedCrossRefGoogle Scholar
  9. 9.
    Fontes RB, Aguiar PH, Zanetti MV, Andrade F, Mandel M. Teixeira MJ. Acute neurogenic pulmonary edema: case reports and literature review. J Neurosurg Anesthesiol 2003;15:144–150.PubMedCrossRefGoogle Scholar
  10. 10.
    Mayer SA, Fink FE, Homma S, et al. Cardiac injury associated with neurogenic pulmonary edema following subarachnoid hemorrhage. Neurology 1994;44:815–820.PubMedGoogle Scholar
  11. 11.
    Mayer SA, LiMandri G, Sherman D, et al. Electrocardiographic markers of abnormal left ventricular wall motion in acute subarachnoid hemorrhage. J Neurosurg 1995;83:889–896.PubMedGoogle Scholar
  12. 12.
    Brouwers PJ, Wijdicks EF, Hasan D, et al. Serial electrocardiographic recording in aneurysmal subarachnoid hemorrhage. Stroke 1989;20:1162–1167.PubMedGoogle Scholar
  13. 13.
    Schievink WI, Wijdicks EF, Parisi JE, Piepgras DG, Whisnant JP. Sudden death from aneurysmal subarachnoid hemorrhage. Neurology 1995;45:871–874.PubMedGoogle Scholar
  14. 14.
    Hunt D, McRae C, Zapf P. Electrocardiographic and serum enzyme changes in subarachnoid hemorrhage. Am Heart J 1969;77:479–488.PubMedCrossRefGoogle Scholar
  15. 15.
    Yoshikawa D, Hara T, Takahasi K, Morita T, Goto F. An association between QTc prolongation and left ventricular hypokinesis during sequential episodes of subarachnoid hemorrhage. Anesth Analg 1999;89:962–964.PubMedCrossRefGoogle Scholar
  16. 16.
    Zaroff JG, Rordorf GA, Newell JB, Ogilvy CS, Levinson JR. Cardiac outcome in patients with subarachnoid hemorrhage and electrocardiographic abnormalities. Neurosurgery 1999;44:34–39; discussion 39-40.PubMedCrossRefGoogle Scholar
  17. 17.
    Deibert E, Barzilai B, Braverman AC, et al. Clinical significance of elevated troponin I levels in patients with nontraumatic subarachnoid hemorrhage. J Neurosurg 2003;98:741–746.PubMedGoogle Scholar
  18. 18.
    Luscher MS, Thygesen K, Ravkilde J, Heickendorff L. Applicability of cardiac troponin T and I for early risk stratification in unstable coronary artery disease. TRIM Study Group. Thrombin Inhibition in Myocardial ischemia. Circulation 1997;96:2578–2585.PubMedGoogle Scholar
  19. 19.
    Tung PP, Olmsted E, Kopelnik A, et al. Plasma B-type natriuretic peptide levels are associated with early cardiac dysfunction after subarachnoid hemorrhage. Stroke 2005;36:1567–1571.PubMedCrossRefGoogle Scholar
  20. 20.
    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;24:636–640.PubMedCrossRefGoogle Scholar
  21. 21.
    Bulsara KR, McGirt MJ, Liao L, 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;98:524–528.PubMedGoogle Scholar
  22. 22.
    Hess EP, Boie ET, White RD. Survival of a neurologically intact patient with subarachnoid hemorrhage and cardiopulmonary arrest. Mayo Clin Proc 2005;80:1073–1076.PubMedGoogle Scholar
  23. 23.
    De Chazal, I, Parham WM, Liopyris P, Wijdicks E. Delayed cardiogenic shock and acute lung injury after aneurysmal subarachnoid hemorrhage. Anesth Analg 2005;100:1147–1149.PubMedCrossRefGoogle Scholar
  24. 24.
    Chang PC, Lee SH, Hung HF, Kaun P, Cheng JJ. Transient ST elevation and left ventricular asynergy associated with normal coronary artery and Tc-99m PYP myocardial infarct scan in subarachnoid hemorrhage. Int J Cardiol 1998;63:189–192.PubMedCrossRefGoogle Scholar
  25. 25.
    Yuki K, Kodama Y, Onda J, Emoto K, Morimoto T, Uozumi T. Coronary vasospasm following subarachnoid hemorrhage as a cause of stunned myocardium. J Neurosurg 1991;75:308–311.PubMedGoogle Scholar
  26. 26.
    Zaroff JG, Rordorf GA, Titus JS, et al. Regional myocardial perfusion after experimental subarachnoid hemorrhage. Stroke 2000;31:1136–1143.PubMedGoogle Scholar
  27. 27.
    Naredi S, Lambert G, Eden E, et al. Increased sympathetic nervous activity in patients with nontraumatic subarachnoid hemorrhage. Stroke 2000;31:901–906.PubMedGoogle Scholar
  28. 28.
    Kawahara E, Ikeda S, Miyahara Y, Kohno S. Role of autonomic nervous dysfunction in electrocardiographic abnormalities and cardiac injury in patients with acute subarachnoid hemorrhage. Circ J 2003;67:753–756.PubMedCrossRefGoogle Scholar
  29. 29.
    Masuda T, Sato K, Yamamoto S, et al. Sympathetic nervous activity and myocardial damage immediately after subarachnoid hemorrhage in a unique animal model. Stroke 2002;33:1671–1676.PubMedCrossRefGoogle Scholar
  30. 30.
    Lambert E, Du XJ, Percy E, Lambert G. Cardiac response to norepinephrine and sympathetic nerve stimulation following experimental subarachnoid hemorrhage. J Neurol Sci 2002;198:43–50.PubMedCrossRefGoogle Scholar
  31. 31.
    Elrifai AM, Bailes JE, Shih SR, Dianzumba S, Brillman J. Characterization of the cardiac effects of acute subarachnoid hemorrhage in dogs. Stroke 1996;27:737–741.PubMedGoogle Scholar
  32. 32.
    Sugiura M, Yozawa Y, Kubo O, et al. Myocardial damage (myocytolysis) caused by subarachnoid hemorrhage. No to Shinkei 1985;37:1155–1161.PubMedGoogle Scholar
  33. 33.
    Karch SB, Billingham ME. Myocardial contraction bands revisited. Hum Pathol 1986;17:9–13.PubMedCrossRefGoogle Scholar
  34. 34.
    Cruickshank JM, Neil-Dwyer G, Degaute JP, et al. Reduction of stress/catecholamine-induced cardiac necrosis by beta 1-selective blockade. Lancet 1987;2:585–589.PubMedCrossRefGoogle Scholar
  35. 35.
    Wittstein IS, Thierman DR, Lima JA, et al. Neurohumoral features of myocardial stunning due to sudden emotional stress. N Engl J Med 2005;352:539–548.PubMedCrossRefGoogle Scholar
  36. 36.
    Doshi R, Neil-Dwyer G. A clinicopathological study of patients following a subarachnoid hemorrhage. Am Heart J 1969;77:479–488.CrossRefGoogle Scholar
  37. 37.
    Takeno Y, Eno S, Hondo T, Matsuda K, Zushi N. Pheochromocytoma with reversal of tako-tsubo-like transient left ventricular dysfunction: a case report. J Cardiol 2004;43:281–287.PubMedGoogle Scholar
  38. 38.
    Drislane FW, Samuels MA, Kozakewich H, Schoen FJ, Strunk RC. Myocardial contraction band lesions in patients with fatal asthma: possible neurocardiologic mechanism. Am Rev Respir Dis 1987;135:498–501.PubMedGoogle Scholar
  39. 39.
    Manno EM, Pfeifer EA, Noe KH, Wijdicks EFM, Cascino GD. Cardiac pathology in patients with status epilepticus. Neurocrit Care 2005;2:231 (Abstract).Google Scholar
  40. 40.
    Cebelin MS, Hirsch CS. Human stress cardiomyopathy. Myocardial lesions in victims of homicidal assaults without internal injuries. Hum Pathol 1980;11:123–132.PubMedGoogle Scholar
  41. 41.
    Novitzky D, Wicomb WN, Cooper KC, Rose AG, Reichart B. Prevention of myocardial injury during brain death by total cardiac sympathectomy in the chacma baboon. Ann Thorac Surg 1986;41:520–524.PubMedCrossRefGoogle Scholar
  42. 42.
    Shivalkar B, Van Loon J, Wieland W, et al. Increase intracranial pressure on myocardial structure and function. Circulation 1993;87:230–239.PubMedGoogle Scholar
  43. 43.
    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;2:990–992.PubMedGoogle Scholar
  44. 44.
    Abe Y, Kondo M, Matsuoka R, Araki M, Dohyama K, Tanio H. Assessment of clinical features in transient left ventricular apical ballooning. J Am Coll Cardiol 2003;41:737–742.PubMedCrossRefGoogle Scholar
  45. 45.
    Connelly KA, MacIsaac AI, Jelinek VM. Stress, myocardial infarction, and the “tako-tsubo” phenomenon. Heart 2004;90:e52.PubMedCrossRefGoogle Scholar
  46. 46.
    Girod JP, Messerli AW, Zidar F, Tang WHW, Brener SJ. Takotsubo-like transient left ventricular dysfunction. Circulation 2003;107:e120-e121.PubMedCrossRefGoogle Scholar
  47. 47.
    Tsuchihashi K, Ueshima K, Uchida T, et al. Angina pectorismyocardial infarction investigations in Japan. Transient left-ventricular apical ballooning without coronary artery stenosis: a novel heart syndrome mimicking acute myocardial infarction. J Am Coll Cardiol 2001;38:11–18.PubMedCrossRefGoogle Scholar
  48. 48.
    Dote K, Sato H, Tateishi H, Uchida T, Ishihara M. Myocardial stunning due to simultaneous multivessel coronary spasms: a review of 5 cases. J Cardiol 1994;21:203–214.Google Scholar
  49. 49.
    Bybee KA, Prasad A, Barsness GW, et al. Clinical characteristics and thrombolysis in myocardial infarction frame counts in women with transient left ventricular apical ballooning syndrome. Am J Cardiol 2004;94:343–346.PubMedCrossRefGoogle Scholar
  50. 50.
    Bybee KA, Kara T, Prasad A, et al. Systemic review: transient left ventricular apical ballooning: a syndrome that mimics ST-segment elevation myocardial infarction. Ann Intern Med 2004;141:858–865.PubMedGoogle Scholar
  51. 51.
    Kyuma M, Tsuchihashi K, Shinshi Y, et al. Effect of intravenous propranolol on left ventricular apical ballooning without coronary artery stenosis (ampulla cardiomyopathy): three cases. Circ J 2002;66:1181–1184.PubMedCrossRefGoogle Scholar
  52. 52.
    Kawai S, Suzuki H, Yamaguchi H, et al. Ampulla cardiomyopathy (‘takotsubo’ cardiomyopathy)—reversible left ventricular dysfunction: with ST segment elevation. Jpn Circ J 2000;64:156–159.PubMedCrossRefGoogle Scholar
  53. 53.
    Akashi YJ, Tejima T, Sakurada H, et al. Left ventricular rupture associated with takotsubo cardiomyopathy. Mayo Clin Proc 2004;79:821–824.PubMedCrossRefGoogle Scholar
  54. 54.
    Takaki A, Ogawa H, Wakeyama T, et al. Ampulla cardiomyopathy with left ventricular apical mural thrombi resolved by anticoagulant therapy without systemic complication: a case report. J Cardiol 2004;44:243–250.PubMedGoogle Scholar
  55. 55.
    Ueyama T. Emotional stress-induced tako-tsubo cardiomyopathy: animal model and molecular mechanism. Ann N Y Acad Sci 2004;1018:437–444.PubMedCrossRefGoogle Scholar
  56. 56.
    Ako J, Honda Y, Fitzgerald PJ. Tako-tsubo-like left ventricular dysfunction. Circulation 2003;108:e158.PubMedCrossRefGoogle Scholar
  57. 57.
    Lee VH, Connolly HM, Fulgham JR, Manno EM, Brown RD Jr, Wijdicks EF. Tako-tsubo cardiomyopathy in aneurismal subarachnoid hemorrhage: an under-appreciated ventricular dysfunction. J Neurosurg 2006;105:1–7.Google Scholar
  58. 58.
    Cruickshank JM, Neil-Dwyer G, Lane J. The effect of oral propranolol upon the ECG changes occurring in subarachnoid haemorrhage. Cardiovasc Res 1975;9:236–245.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 2006

Authors and Affiliations

  • Vivien H. Lee
    • 2
  • Jae K. Oh
    • 1
  • Sharon L. Mulvagh
    • 1
  • Eelco F. M. Wijdicks
    • 2
    Email author
  1. 1.Division of Cardiovascular DiseasesMayo Clinic College of MedicineRochester
  2. 2.Department of Neurology Division of Critical Care of NeurologyMayo Clinic College of MedicineRochester

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