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Apical Ballooning Resulting from Limbic Encephalitis
BRIEF OBSERVATION
Apical Ballooning Resulting from Limbic Encephalitis Jill Gelow, MD, MPH,a Michael Kruer, MD,b Vijayshree Yadav, MD,c,d Sanjiv Kaul, MDa a
Division of Cardiovascular Medicine, bDepartment of Medicine, Divisions of Pediatric Neurology and Developmental Pediatrics, Department of Pediatrics, and dDivision of Neuroimmunology, Department of Neurology, Oregon Health and Science University, Portland. c
ABSTRACT BACKGROUND: Neurogenic stunned myocardium is an increasingly recognized cause of left ventricular apical ballooning, or takotsubo cardiomyopathy. We report the first case of neurogenic stunned myocardium as a result of limbic encephalitis. METHODS: This 73-year-old woman with anterograde and retrograde amnesia was investigated using electrocardiography, magnetic resonance imaging, and left ventricular angiography. RESULTS: Electrocardiography showed deep T-wave inversions in multiple leads, magnetic resonance imaging demonstrated increased signal on fluid-attenuated inversion recovery images symmetrically within the medial temporal lobes consistent with limbic encephalitis. Left ventricular angiography showed apical ballooning. CONCLUSIONS: Because the insula has extensive interconnections with limbic structures, limbic encephalitis could lead to alterations in the sympathetic regulation of the insular cortex resulting in neurogenic stunned myocardium. © 2009 Elsevier Inc. All rights reserved. • The American Journal of Medicine (2009) 122, 583-586 KEYWORDS: Apical ballooning; Limbic encephalitis; Stunned myocardium
Neurogenic stunned myocardium is an increasingly recognized cause of takotsubo cardiomyopathy, most often attributed to subarachnoid hemorrhage or stroke.1-7 We report the first case of neurogenic stunned myocardium associated with limbic encephalitis.
CASE REPORT A 73-year-old woman was admitted with anterograde and retrograde memory loss. A noncontrast head computed to-
Funding: None. Conflict of Interest: None. Authorship: All authors had access to the data. Drs. Gelow and Kaul were consultant cardiologists to the case. Drs. Kruer and Yadav took care of the patient. All assisted in writing the article and developing the figures. Requests for reprints should be addressed to Sanjiv Kaul, MD, Division of Cardiovascular Medicine, Oregon Health and Science University, UHN62, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239-3098. E-mail address: [email protected]
0002-9343/$ -see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.amjmed.2008.12.016
mography scan was unremarkable, and an electroencephalogram showed no evidence of seizure activity. Cerebral spinal fluid analysis revealed glucose of 90 and protein of 55 mg/dL. There were 27 erythrocytes and 36 leukocytes per cubic mm, with 88% lymphocytes and 12% monocytes. Herpes simplex virus polymerase chain reaction and bacterial culture were negative. Cytology was negative for malignancy. Magnetic resonance imaging demonstrated increased signal on fluid-attenuated inversion recovery images symmetrically within the medial temporal lobes without enhancement or mass effect. There was an area of increased signal in the anterior cerebellar vermis (Figure 1). These findings were consistent with limbic encephalitis. An extensive malignancy work-up was notable only for multiple left axillary lymph nodes, the largest measuring 12 by 15 mm, demonstrated on whole body computed tomography scan, and biopsy demonstrated reactive hyperplasia with no evidence of lymphoma or metastatic disease. Serologic testing for paraneoplastic antibodies was negative. An electrocardiogram showed normal sinus rhythm
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The American Journal of Medicine, Vol 122, No 6, June 2009
with deep T-wave inversions in multiple leads (Figure 2). an extreme emotional experience.8-12 It also has been Laboratory studies were notable for troponin I of 0.22 described in sepsis, acute pulmonary disease, pheochrong/mL and creatine kinase of 48 mg/mL. Coronary anmocytoma, postoperative states, and with neurologic disgiography showed no obstructive disease. Left ventricueases such as subarachnoid hemorrhage, stroke, seizures, lar (LV) angiography demonstrated classical apical baland head injury.1-7,13-17 Neurogenic stunned myocardium looning (Figure 3). is transient, associated with disThere was no change in memproportionately low levels of ory loss or confusion despite treatcardiac troponin and creatine kiCLINICAL SIGNIFICANCE ment with intravenous immunonase compared to the extent of globulin and high-dose steroids. dysfunction, and occurs in the ● Electrocardiogram changes in a patient Plasma exchange was initiated and, absence of obstructive coronwith a neurogenic syndrome should raise after 3 sessions, the patient’s ary artery disease. Characteristic the suspicion for stunned myocardium memory improved. Repeat echoelectrocardiogram findings inwith apical ballooning. cardiography before discharge clude QT prolongation and ST● Documentation of apical ballooning can showed significant improvement segment and T-wave abnormain LV systolic function. lities.2,3,18,19 be performed by cardiac imaging. Following discharge, the patient Neurogenic stunned myocar● If hemodynamic compromise occurs developed progressive lymphadedium results from autonomic nerfrom apical ballooning, it should be nopathy. Lymph node biopsy was vous imbalance, causing an excess treated until the dysfunction reverses. repeated and demonstrated highof sympathetic activity.1 Multiple grade B-cell lymphoma, consistent mechanisms for catecholamine-inwith Burkitt’s lymphoma. The paduced cardiac toxicity have been tient expired shortly after the initiation of chemotherapy. postulated, including myocardial oxygen supply-demand mismatch, coronary artery vasospasm, transient dynamic LV outflow tract obstruction, direct toxic effects of high DISCUSSION levels of norepinepherine on the myocardium, and free LV apical ballooning syndrome, or takotsubo cardiomyradical injury due to catecholamine autoxidation.20-28 An opathy, has been classically described in association with adrenoreceptor polymorphism also may lead to genetic predisposition for cardiac injury associated with acute central nervous system disease.29 The end result of excess sympathetic activity is coagulative myocytolysis, or contraction band necrosis that causes cells to die in a hypercontracted state with early myofibrillar damage and irregular cross-band formations.1 This form of necrosis has a subendocardial predisposition, a tendency towards early calcification, and elicits a mononuclear response. It is readily distinguished from coagulation necrosis, the cause of cell death in myocardial infarction.1 The insular cortex plays an essential role in regulation of the autonomic nervous system. Stimulation of the right (nondominant) insula accentuates sympathetic activity, elevating heart rate and blood pressure. In contrast, stimulation of the left (dominant) insula leads to the opposite effects. Additionally, stimulation of the adjacent frontoparietal cortex may decrease sympathoadrenal tone by inhibiting the insula, whereas destruction of this area may have the opposite effect and lead to excessive sympathetic activity.30 Stroke involving the left insular cortex has been shown to increase the probability of adverse cardiac outcomes and is associated with reduced global LV function.21 Further, different areas of the right insula Figure 1 Coronal fluid-attenuated inversion recovery seare significantly associated with stroke-related myocarquence imaging on magnetic resonance imaging demondial injury.31 strating bilateral signal hyperintensity (arrows) in the meMost of the insula, particularly its anteroventral redial temporal lobes, including the hippocampi. gion, has extensive interconnections with limbic struc-
Gelow et al
Figure 2 sion.
Apical Ballooning from Limbic Encephalitis
585
Standard 12-lead electrocardiogram with a 3-lead rhythm strip showing diffuse symmetrical T-wave inver-
tures. Thus, it is plausible that limbic encephalitis could lead to alterations in the sympathetic regulation of the insular cortex, resulting in the development of neurogenic stunned myocardium.32 To our knowledge, this is the first case of LV apical ballooning associated with limbic encephalitis.
Figure 3 Left ventricular angiogram in end-systole with classical apical ballooning with a narrow neck (arrows).
References 1. Samuels MA. The brain-heart connection. Circulation. 2007;116: 77-84. 2. Mayer SA, Lin J, Homma S, et al. Myocardial injury and left ventricular performances after subarachnoid hemorrhage. Stroke. 1999;30: 780-786. 3. Lee VH, Connolly HM, Fulgham JR, et al. Takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: an underappreciated cause of ventricular dysfunction. J Neurosurg. 2006;105:264-270. 4. Yuki K, Kodama Y, Onda J, et al. Coronary vasospasm following subarachnoid hemorrhage as a cause of stunned myocardium. Case report. J Neurosurg. 1991;75:308-311. 5. Kono T, Morita H, Kuroiwa T, et al. Left ventricular wall motion abnormalities in patients with subarachnoid hemorrhage: neurogenic stunned myocardium. J Am Coll Cardiol. 1994;24:636-640. 6. Wang TD, Wu CC, Lee YT. Myocardial stunning after cerebral infarction. Int J Cardiol. 1997;58:308-311. 7. Seifert T, Klein E, Legat-Wallner S, et al. Bilateral vertebral artery dissection and infratentorial stroke complicated by stress-induced cardiomyopathy. J Neurol Neurosurg Psychiatry. 2008;79:480-481. 8. Bybee KA, Kara T, Prasad A, et al. Systematic review: transient left ventricular apical ballooning: a syndrome that mimics ST-segment elevation myocardial infarction. Ann Intern Med. 2004;141:858865. 9. Gianna M, Dentali F, Grandi AM, et al. Apical ballooning syndrome or takotsubo cardiomyopathy: a systematic review. Eur Heart J. 2006; 27:1523-1529. 10. Fazio G, Barbaro G, Sutera L, et al. Clinical findings of Takotsubo cardiomyopathy: results from a multicenter international study. J Cardiovasc Med. 2008;9:239-244. 11. Sharkey SW, Lesser JR, Zenovich AG, et al. Acute and reversible cardiomyopathy provoked by stress in women from the United States. Circulation. 2005;111:471-479.
586 12. Wittstein IS, Thiemann DR, Lima JA, et al. Neurohormonal features of myocardial stunning due to sudden emotional stress. N Engl J Med. 2005;352:539-548. 13. Sharkey SW, Shear W, Hodges M, Herzog CA. Reversible myocardial contraction abnormalities in patients with an acute noncardiac illness. Chest. 1998;114:98-105. 14. Takizawa M, Kobayakawa N, Uozumi H, et al. A case of transient left ventricular ballooning with pheochromocytoma, supporting the pathologic role of catecholamines in stress-induced cardiomyopathy or takotsubo cardiomyopathy. Int J Cardiol. 2007;114:e15-e17. 15. Ramakirshna G, Ravi BS, Chandrasekaran K. Apical ballooning syndrome in a post-operative patient with normal microvascular perfusion by myocardial contrast echocardiography. Echocardiography. 2005; 22:606-610. 16. Lemke DM, Hussain SI, Wolfe TJ, et al. Takotsubo cardiomyopathy associated with seizures. Neurocrit Care. 2008;9:112-117. 17. Phu KK, Chan MY, Chiba B-L. Images in cardiology: reversible left ventricular apical ballooning after head injury. Clin Cardiol. 2005;28:30. 18. Kurowski V, Kaiser A, von Hof K, et al. Apical and mid-ventricular transient left ventricular dysfunction syndrome (tako-tsubo cardiomyopathy): frequency, mechanisms and prognosis. Chest. 2007;132:809-816. 19. Tung P, Kopelnik A, Banki N, et al. Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke. 2004;35:548-553. 20. Hessell EA. The brain and the heart. Anesth Analg. 2006;103:522-526. 21. Laowattana S, Zeger SL, Lima JAC, et al. Left insular stroke is associated with adverse cardiac outcome. Neurology. 2006;66:477-483. 22. Simon M, Downing SE. Coronary vasoconstriction and catecholamine cardiomyopathy. Am Heart J. 1985;109:297-303.
The American Journal of Medicine, Vol 122, No 6, June 2009 23. Mann DL, Kent RL, Parsons B, Cooper G. Adrenergic effects on the biology of the adult mammalian cardiocytes. Circulation. 1993;85: 790-804. 24. Yates JC, Beamish RE, Dhalla NS. Ventricular dysfunction and necrosis produced by adrenochorme metabolites of epinephrine: Relation to pathogenesis of catecholamine cardiomyopathy. Am Heart J. 1981; 102:210-221. 25. Yates JC, Dhalla NS. Introduction of necrosis and failure in the isolated perfused rat heart with oxidized isoproterenol. J Mol Cell Cardiol. 1975;7:807-816. 26. Dhalla NS, Yates JC, Lee SL, Singh A. Functional and subcellular changes in the isolated rat heart perfused with oxidized isoproterenol. J Mol Cell Cardiol. 1978;10:31-41. 27. Downing SE, Chen V. Myocardial injury following endogenous catecholamine release in rabbits. J Mol Cell Cardiol. 1985;17:377-387. 28. Lee JC, Sponenberg DP. Role of alpha-1-adrenoceptors in norepinephrine induced cardiomyopathy. Am J Pathol. 1985;121:316-321. 29. Zaroff JG, Pawlikowska L, Miss JC, et al. Adrenoreceptor polymorphism and the risk of cardiac injury and dysfunction after subarachnoid hemorrhage. Stroke. 2006;37:1680-1685. 30. Oppenheimer SM. Neurogenic cardiac effects of cerebrovascular disease. Curr Opin Neurol. 1994;7:20-24. 31. Ay H, Koroshetz WJ, Benner T, et al. Neuroanatomic correlates of stroke-related myocardial injury. Neurology. 2006;66:1325-1329. 32. Mesulam MM, Mufson EJ. Insula of the old-world monkey. III: efferent cortical output and comments on function. J Comp Neurol. 1982;212:38-52.
Apical Ballooning Resulting from Limbic Encephalitis Jill Gelow, MD, MPH,a Michael Kruer, MD,b Vijayshree Yadav, MD,c,d Sanjiv Kaul, MDa a
Division of Cardiovascular Medicine, bDepartment of Medicine, Divisions of Pediatric Neurology and Developmental Pediatrics, Department of Pediatrics, and dDivision of Neuroimmunology, Department of Neurology, Oregon Health and Science University, Portland. c
ABSTRACT BACKGROUND: Neurogenic stunned myocardium is an increasingly recognized cause of left ventricular apical ballooning, or takotsubo cardiomyopathy. We report the first case of neurogenic stunned myocardium as a result of limbic encephalitis. METHODS: This 73-year-old woman with anterograde and retrograde amnesia was investigated using electrocardiography, magnetic resonance imaging, and left ventricular angiography. RESULTS: Electrocardiography showed deep T-wave inversions in multiple leads, magnetic resonance imaging demonstrated increased signal on fluid-attenuated inversion recovery images symmetrically within the medial temporal lobes consistent with limbic encephalitis. Left ventricular angiography showed apical ballooning. CONCLUSIONS: Because the insula has extensive interconnections with limbic structures, limbic encephalitis could lead to alterations in the sympathetic regulation of the insular cortex resulting in neurogenic stunned myocardium. © 2009 Elsevier Inc. All rights reserved. • The American Journal of Medicine (2009) 122, 583-586 KEYWORDS: Apical ballooning; Limbic encephalitis; Stunned myocardium
Neurogenic stunned myocardium is an increasingly recognized cause of takotsubo cardiomyopathy, most often attributed to subarachnoid hemorrhage or stroke.1-7 We report the first case of neurogenic stunned myocardium associated with limbic encephalitis.
CASE REPORT A 73-year-old woman was admitted with anterograde and retrograde memory loss. A noncontrast head computed to-
Funding: None. Conflict of Interest: None. Authorship: All authors had access to the data. Drs. Gelow and Kaul were consultant cardiologists to the case. Drs. Kruer and Yadav took care of the patient. All assisted in writing the article and developing the figures. Requests for reprints should be addressed to Sanjiv Kaul, MD, Division of Cardiovascular Medicine, Oregon Health and Science University, UHN62, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239-3098. E-mail address: [email protected]
0002-9343/$ -see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.amjmed.2008.12.016
mography scan was unremarkable, and an electroencephalogram showed no evidence of seizure activity. Cerebral spinal fluid analysis revealed glucose of 90 and protein of 55 mg/dL. There were 27 erythrocytes and 36 leukocytes per cubic mm, with 88% lymphocytes and 12% monocytes. Herpes simplex virus polymerase chain reaction and bacterial culture were negative. Cytology was negative for malignancy. Magnetic resonance imaging demonstrated increased signal on fluid-attenuated inversion recovery images symmetrically within the medial temporal lobes without enhancement or mass effect. There was an area of increased signal in the anterior cerebellar vermis (Figure 1). These findings were consistent with limbic encephalitis. An extensive malignancy work-up was notable only for multiple left axillary lymph nodes, the largest measuring 12 by 15 mm, demonstrated on whole body computed tomography scan, and biopsy demonstrated reactive hyperplasia with no evidence of lymphoma or metastatic disease. Serologic testing for paraneoplastic antibodies was negative. An electrocardiogram showed normal sinus rhythm
584
The American Journal of Medicine, Vol 122, No 6, June 2009
with deep T-wave inversions in multiple leads (Figure 2). an extreme emotional experience.8-12 It also has been Laboratory studies were notable for troponin I of 0.22 described in sepsis, acute pulmonary disease, pheochrong/mL and creatine kinase of 48 mg/mL. Coronary anmocytoma, postoperative states, and with neurologic disgiography showed no obstructive disease. Left ventricueases such as subarachnoid hemorrhage, stroke, seizures, lar (LV) angiography demonstrated classical apical baland head injury.1-7,13-17 Neurogenic stunned myocardium looning (Figure 3). is transient, associated with disThere was no change in memproportionately low levels of ory loss or confusion despite treatcardiac troponin and creatine kiCLINICAL SIGNIFICANCE ment with intravenous immunonase compared to the extent of globulin and high-dose steroids. dysfunction, and occurs in the ● Electrocardiogram changes in a patient Plasma exchange was initiated and, absence of obstructive coronwith a neurogenic syndrome should raise after 3 sessions, the patient’s ary artery disease. Characteristic the suspicion for stunned myocardium memory improved. Repeat echoelectrocardiogram findings inwith apical ballooning. cardiography before discharge clude QT prolongation and ST● Documentation of apical ballooning can showed significant improvement segment and T-wave abnormain LV systolic function. lities.2,3,18,19 be performed by cardiac imaging. Following discharge, the patient Neurogenic stunned myocar● If hemodynamic compromise occurs developed progressive lymphadedium results from autonomic nerfrom apical ballooning, it should be nopathy. Lymph node biopsy was vous imbalance, causing an excess treated until the dysfunction reverses. repeated and demonstrated highof sympathetic activity.1 Multiple grade B-cell lymphoma, consistent mechanisms for catecholamine-inwith Burkitt’s lymphoma. The paduced cardiac toxicity have been tient expired shortly after the initiation of chemotherapy. postulated, including myocardial oxygen supply-demand mismatch, coronary artery vasospasm, transient dynamic LV outflow tract obstruction, direct toxic effects of high DISCUSSION levels of norepinepherine on the myocardium, and free LV apical ballooning syndrome, or takotsubo cardiomyradical injury due to catecholamine autoxidation.20-28 An opathy, has been classically described in association with adrenoreceptor polymorphism also may lead to genetic predisposition for cardiac injury associated with acute central nervous system disease.29 The end result of excess sympathetic activity is coagulative myocytolysis, or contraction band necrosis that causes cells to die in a hypercontracted state with early myofibrillar damage and irregular cross-band formations.1 This form of necrosis has a subendocardial predisposition, a tendency towards early calcification, and elicits a mononuclear response. It is readily distinguished from coagulation necrosis, the cause of cell death in myocardial infarction.1 The insular cortex plays an essential role in regulation of the autonomic nervous system. Stimulation of the right (nondominant) insula accentuates sympathetic activity, elevating heart rate and blood pressure. In contrast, stimulation of the left (dominant) insula leads to the opposite effects. Additionally, stimulation of the adjacent frontoparietal cortex may decrease sympathoadrenal tone by inhibiting the insula, whereas destruction of this area may have the opposite effect and lead to excessive sympathetic activity.30 Stroke involving the left insular cortex has been shown to increase the probability of adverse cardiac outcomes and is associated with reduced global LV function.21 Further, different areas of the right insula Figure 1 Coronal fluid-attenuated inversion recovery seare significantly associated with stroke-related myocarquence imaging on magnetic resonance imaging demondial injury.31 strating bilateral signal hyperintensity (arrows) in the meMost of the insula, particularly its anteroventral redial temporal lobes, including the hippocampi. gion, has extensive interconnections with limbic struc-
Gelow et al
Figure 2 sion.
Apical Ballooning from Limbic Encephalitis
585
Standard 12-lead electrocardiogram with a 3-lead rhythm strip showing diffuse symmetrical T-wave inver-
tures. Thus, it is plausible that limbic encephalitis could lead to alterations in the sympathetic regulation of the insular cortex, resulting in the development of neurogenic stunned myocardium.32 To our knowledge, this is the first case of LV apical ballooning associated with limbic encephalitis.
Figure 3 Left ventricular angiogram in end-systole with classical apical ballooning with a narrow neck (arrows).
References 1. Samuels MA. The brain-heart connection. Circulation. 2007;116: 77-84. 2. Mayer SA, Lin J, Homma S, et al. Myocardial injury and left ventricular performances after subarachnoid hemorrhage. Stroke. 1999;30: 780-786. 3. Lee VH, Connolly HM, Fulgham JR, et al. Takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: an underappreciated cause of ventricular dysfunction. J Neurosurg. 2006;105:264-270. 4. Yuki K, Kodama Y, Onda J, et al. Coronary vasospasm following subarachnoid hemorrhage as a cause of stunned myocardium. Case report. J Neurosurg. 1991;75:308-311. 5. Kono T, Morita H, Kuroiwa T, et al. Left ventricular wall motion abnormalities in patients with subarachnoid hemorrhage: neurogenic stunned myocardium. J Am Coll Cardiol. 1994;24:636-640. 6. Wang TD, Wu CC, Lee YT. Myocardial stunning after cerebral infarction. Int J Cardiol. 1997;58:308-311. 7. Seifert T, Klein E, Legat-Wallner S, et al. Bilateral vertebral artery dissection and infratentorial stroke complicated by stress-induced cardiomyopathy. J Neurol Neurosurg Psychiatry. 2008;79:480-481. 8. Bybee KA, Kara T, Prasad A, et al. Systematic review: transient left ventricular apical ballooning: a syndrome that mimics ST-segment elevation myocardial infarction. Ann Intern Med. 2004;141:858865. 9. Gianna M, Dentali F, Grandi AM, et al. Apical ballooning syndrome or takotsubo cardiomyopathy: a systematic review. Eur Heart J. 2006; 27:1523-1529. 10. Fazio G, Barbaro G, Sutera L, et al. Clinical findings of Takotsubo cardiomyopathy: results from a multicenter international study. J Cardiovasc Med. 2008;9:239-244. 11. Sharkey SW, Lesser JR, Zenovich AG, et al. Acute and reversible cardiomyopathy provoked by stress in women from the United States. Circulation. 2005;111:471-479.
586 12. Wittstein IS, Thiemann DR, Lima JA, et al. Neurohormonal features of myocardial stunning due to sudden emotional stress. N Engl J Med. 2005;352:539-548. 13. Sharkey SW, Shear W, Hodges M, Herzog CA. Reversible myocardial contraction abnormalities in patients with an acute noncardiac illness. Chest. 1998;114:98-105. 14. Takizawa M, Kobayakawa N, Uozumi H, et al. A case of transient left ventricular ballooning with pheochromocytoma, supporting the pathologic role of catecholamines in stress-induced cardiomyopathy or takotsubo cardiomyopathy. Int J Cardiol. 2007;114:e15-e17. 15. Ramakirshna G, Ravi BS, Chandrasekaran K. Apical ballooning syndrome in a post-operative patient with normal microvascular perfusion by myocardial contrast echocardiography. Echocardiography. 2005; 22:606-610. 16. Lemke DM, Hussain SI, Wolfe TJ, et al. Takotsubo cardiomyopathy associated with seizures. Neurocrit Care. 2008;9:112-117. 17. Phu KK, Chan MY, Chiba B-L. Images in cardiology: reversible left ventricular apical ballooning after head injury. Clin Cardiol. 2005;28:30. 18. Kurowski V, Kaiser A, von Hof K, et al. Apical and mid-ventricular transient left ventricular dysfunction syndrome (tako-tsubo cardiomyopathy): frequency, mechanisms and prognosis. Chest. 2007;132:809-816. 19. Tung P, Kopelnik A, Banki N, et al. Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke. 2004;35:548-553. 20. Hessell EA. The brain and the heart. Anesth Analg. 2006;103:522-526. 21. Laowattana S, Zeger SL, Lima JAC, et al. Left insular stroke is associated with adverse cardiac outcome. Neurology. 2006;66:477-483. 22. Simon M, Downing SE. Coronary vasoconstriction and catecholamine cardiomyopathy. Am Heart J. 1985;109:297-303.
The American Journal of Medicine, Vol 122, No 6, June 2009 23. Mann DL, Kent RL, Parsons B, Cooper G. Adrenergic effects on the biology of the adult mammalian cardiocytes. Circulation. 1993;85: 790-804. 24. Yates JC, Beamish RE, Dhalla NS. Ventricular dysfunction and necrosis produced by adrenochorme metabolites of epinephrine: Relation to pathogenesis of catecholamine cardiomyopathy. Am Heart J. 1981; 102:210-221. 25. Yates JC, Dhalla NS. Introduction of necrosis and failure in the isolated perfused rat heart with oxidized isoproterenol. J Mol Cell Cardiol. 1975;7:807-816. 26. Dhalla NS, Yates JC, Lee SL, Singh A. Functional and subcellular changes in the isolated rat heart perfused with oxidized isoproterenol. J Mol Cell Cardiol. 1978;10:31-41. 27. Downing SE, Chen V. Myocardial injury following endogenous catecholamine release in rabbits. J Mol Cell Cardiol. 1985;17:377-387. 28. Lee JC, Sponenberg DP. Role of alpha-1-adrenoceptors in norepinephrine induced cardiomyopathy. Am J Pathol. 1985;121:316-321. 29. Zaroff JG, Pawlikowska L, Miss JC, et al. Adrenoreceptor polymorphism and the risk of cardiac injury and dysfunction after subarachnoid hemorrhage. Stroke. 2006;37:1680-1685. 30. Oppenheimer SM. Neurogenic cardiac effects of cerebrovascular disease. Curr Opin Neurol. 1994;7:20-24. 31. Ay H, Koroshetz WJ, Benner T, et al. Neuroanatomic correlates of stroke-related myocardial injury. Neurology. 2006;66:1325-1329. 32. Mesulam MM, Mufson EJ. Insula of the old-world monkey. III: efferent cortical output and comments on function. J Comp Neurol. 1982;212:38-52.