Skip to main content
SpringerLink
Log in

Mechanisms in neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage

  • Review
  • Published:
Neurocritical Care Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Friedman JA, Pichelmann MA, Piepgras DG, et al. Pulmonary complications of aneurysmal subarachnoid hemorrhage. Neurosurgery 2003;52:1025–1031.

    Article  PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  3. Mayer SA, Lin J, Homma S, et al. Myocardial injury and left ventricular performance after subarachnoid hemorrhage. Stroke 1999;30:780–786.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  6. Tung P, Kopelnik A, Banki N, et al. Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke 2004;35:548–551.

    Article  PubMed  Google Scholar 

  7. Mayer SA, Fink ME, Homma S, et al. Cardiac injury associated with neurogenic pulmonary edema following subarachnoid hemorrhage. Neurology 1994;44:815–820.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  10. Mayer SA, Fink FE, Homma S, et al. Cardiac injury associated with neurogenic pulmonary edema following subarachnoid hemorrhage. Neurology 1994;44:815–820.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  12. Brouwers PJ, Wijdicks EF, Hasan D, et al. Serial electrocardiographic recording in aneurysmal subarachnoid hemorrhage. Stroke 1989;20:1162–1167.

    PubMed  CAS  Google Scholar 

  13. Schievink WI, Wijdicks EF, Parisi JE, Piepgras DG, Whisnant JP. Sudden death from aneurysmal subarachnoid hemorrhage. Neurology 1995;45:871–874.

    PubMed  CAS  Google Scholar 

  14. Hunt D, McRae C, Zapf P. Electrocardiographic and serum enzyme changes in subarachnoid hemorrhage. Am Heart J 1969;77:479–488.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  26. Zaroff JG, Rordorf GA, Titus JS, et al. Regional myocardial perfusion after experimental subarachnoid hemorrhage. Stroke 2000;31:1136–1143.

    PubMed  CAS  Google Scholar 

  27. Naredi S, Lambert G, Eden E, et al. Increased sympathetic nervous activity in patients with nontraumatic subarachnoid hemorrhage. Stroke 2000;31:901–906.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  32. Sugiura M, Yozawa Y, Kubo O, et al. Myocardial damage (myocytolysis) caused by subarachnoid hemorrhage. No to Shinkei 1985;37:1155–1161.

    PubMed  CAS  Google Scholar 

  33. Karch SB, Billingham ME. Myocardial contraction bands revisited. Hum Pathol 1986;17:9–13.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  36. Doshi R, Neil-Dwyer G. A clinicopathological study of patients following a subarachnoid hemorrhage. Am Heart J 1969;77:479–488.

    Article  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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. Cebelin MS, Hirsch CS. Human stress cardiomyopathy. Myocardial lesions in victims of homicidal assaults without internal injuries. Hum Pathol 1980;11:123–132.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  42. Shivalkar B, Van Loon J, Wieland W, et al. Increase intracranial pressure on myocardial structure and function. Circulation 1993;87:230–239.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  45. Connelly KA, MacIsaac AI, Jelinek VM. Stress, myocardial infarction, and the “tako-tsubo” phenomenon. Heart 2004;90:e52.

    Article  PubMed  CAS  Google Scholar 

  46. Girod JP, Messerli AW, Zidar F, Tang WHW, Brener SJ. Takotsubo-like transient left ventricular dysfunction. Circulation 2003;107:e120-e121.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  53. Akashi YJ, Tejima T, Sakurada H, et al. Left ventricular rupture associated with takotsubo cardiomyopathy. Mayo Clin Proc 2004;79:821–824.

    Article  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  55. Ueyama T. Emotional stress-induced tako-tsubo cardiomyopathy: animal model and molecular mechanism. Ann N Y Acad Sci 2004;1018:437–444.

    Article  PubMed  CAS  Google Scholar 

  56. Ako J, Honda Y, Fitzgerald PJ. Tako-tsubo-like left ventricular dysfunction. Circulation 2003;108:e158.

    Article  PubMed  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Cardiovascular Diseases, Mayo Clinic College of Medicine, Rochester, MN

    Jae K. Oh & Sharon L. Mulvagh

  2. Department of Neurology Division of Critical Care of Neurology, Mayo Clinic College of Medicine, 200 First Street SW, 55905, Rochester, MN

    Vivien H. Lee & Eelco F. M. Wijdicks MD

Authors
  1. Vivien H. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jae K. Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sharon L. Mulvagh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eelco F. M. Wijdicks MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eelco F. M. Wijdicks MD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, V.H., Oh, J.K., Mulvagh, S.L. et al. Mechanisms in neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage. Neurocrit Care 5, 243–249 (2006). https://doi.org/10.1385/NCC:5:3:243

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/NCC:5:3:243

Key wors

Search

Navigation