Tako-tsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: an underappreciated ventricular dysfunction

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Object

Neurogenic stunned myocardium in aneurysmal subarachnoid hemorrhage (SAH) is associated with a wide spectrum of reversible left ventricular wall motion abnormalities and includes a subset of patients with a pattern of apical akinesia and concomitant sparing of basal segments called “tako-tsubo cardiomyopathy.”

Methods

After obtaining institutional review board approval, the authors retrospectively identified among all patients admitted to the Mayo Clinic’s Neurological Intensive Care Unit between January 1990 and January 2005 those with aneurysmal SAH who had met the echocardiographic criteria for tako-tsubo cardiomyopathy. Among 24 patients with SAH-induced reversible cardiac dysfunction, the authors identified eight with SAH-induced tako-tsubo cardiomyopathy. All eight patients were women with a mean age of 55.5 years (range 38.6–71.1). Seven patients presented with a poor-grade SAH, reflected by a Hunt and Hess grade of III or IV. Four patients underwent aneurysm clip application, and four underwent endovascular coil occlusion. The initial mean ejection fraction (EF) was 38% (range 25–55%), and the mean EF at recovery was 55% (range 40–68%). Cerebral vasospasm developed in six patients, but cerebral infarction developed in only three patients.

Conclusions

The authors describe the largest cohort with aneurysmal SAH–induced tako-tsubo cardiomyopathy. In the SAH population, tako-tsubo cardiomyopathy predominates in postmenopausal women and is often associated with pulmonary edema, prolonged intubation, and cerebral vasospasm. Additional studies are warranted to understand the complex mechanism involved in tako-tsubo cardiomyopathy and its intriguing relationship to neurogenic stunned myocardium.

Abbreviations used in this paper:CK-MB = creatine kinase MB isoenzyme;; CT = computed tomography;; ECG = electrocardiography;; EF = ejection fraction;; LV = left ventricular;; NICU = neurological intensive care unit;; SAH = subarachnoid hemorrhage.

Article Information

Address reprint requests to: Eelco F. M. Wijdicks, M.D., Department of Neurology, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, Minnesota 55905. email: wijde@mayo.edu.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Photograph illustrating a tako-tsubo, a Japanese octopus catcher pot, which is strung by rope from Japanese fishing boats. Anachoresis (living in crevices and holes) is typical behavior of octopuses. Photograph by Sarah H. Lee.

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    Illustration of the heart depicting a normal (left) and abnormal (right) cardiac contraction. After aneurysmal SAH, the cardiac contraction becomes abnormal, with apical and midventricle akinesia consistent with tako-tsubo cardiomyopathy.

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    Schematic demonstrating initial echocardiographic regional wall motion abnormalities. Note the preferential involvement of apical and midventricle segments. From left to right, the segments shown are base, middle, and apex.

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    Graph showing the initial and final EFs in SAH-induced tako-tsubo cardiomyopathy.

References

  • 1

    Abe YKondo MMatsuoka RAraki MDohyama KTanio H: Assessment of clinical features in transient left ventricular apical ballooning. J Am Coll Cardiol 41:7377422003

  • 2

    Akashi YJTejima TSakurada HMatsuda HSuzuki KKawa-saki K: Left ventricular rupture associated with Takotsubo cardiomyopathy. Mayo Clin Proc 79:8218242004

  • 3

    Ako JHonda YFitzgerald PJ: Tako-tsubo-like left ventricular dysfunction. Circulation 108:e1582003. (Letter)

  • 4

    Bulsara KRMcGirt MJLiao LVillavicencio ATBorel CAlexander MJ: Use of the peak troponin value to differentiate myocardial infarction from reversible neurogenic left ventricular dysfunction associated with aneurysmal subarachnoid hemorrhage. J Neurosurg 98:5245282003

  • 5

    Bybee KAKara TPrasad ALerman ABarsness GWWright RS: Systemic review: transient left ventricular apical ballooning: a syndrome that mimics st-segment elevation myocardial infarction. Ann Intern Med 141:8588652004

  • 6

    Bybee KAPrasad ABarsness GWLerman AJaffe ASMurphy JG: Clinical characteristics and thrombolysis in myocardial infarction frame counts in women with transient left ventricular apical ballooning syndrome. Am J Cardiol 94:3433462004

  • 7

    Cebelin MSHirsch CS: Human stress cardiomyopathy Myocar-dial lesions in victims of homicidal assaults without internal injuries. Hum Pathol 11:1231321980

  • 8

    Connelly KAMacIsaac AIJelinek VM: Stress, myocardial infarction, and the “tako-tsubo” phenomenon. Heart 90:e522004

  • 9

    de Chazal IParham WM IIILiopyris PWijdicks EF: Delayed cardiogenic shock and acute lung injury after aneurysmal subarachnoid hemorrhage. Anesth Analg 100:114711492005

  • 10

    Donaldson JWPritz MB: Myocardial stunning secondary to aneurysmal subarachnoid hemorrhage. Surg Neurol 55:12162001

  • 11

    Doshi RNeil-Dwyer G: A clinicopathological study of patients following a subarachnoid hemorrhage. J Neurosurg 52:2953011980

  • 12

    Dote KSato HTateishi HUchida TIshihara M: [Myocardial stunning due to simultaneous multivessel coronary spasms: a review of 5 cases.]. J Cardiol 21:2032141991. (Jpn)

  • 13

    Drislane FWSamuels MAKozakewich HSchoen FJStrunk RC: Myocardial contraction band lesions in patients with fatal asthma: possible neurocardiologic mechanism. Am Rev Respir Dis 135:4985011987

  • 14

    Dujardin KSMcCully RBWijdicks EFTazelaar HDSeward JBMcGregor CG: Myocardial dysfunction associated with brain death: clinical, echocardiographic, and pathologic features. J Heart Lung Transplant 20:3503572001

  • 15

    Elrifai AMBailes JEShih SRDianzumba SBrillman J: Characterization of the cardiac effects of acute subarachnoid hemorrhage in dogs. Stroke 27:7377421996

  • 16

    Girod JPMesserli AWZidar FTang WHWBrener SJ: Images in cardiovascular medicine Tako-tsubo-like transient left ventricular dysfunction. Circulation 107:e120e1212003

  • 17

    Handlin LRKindred LHBeauchamp GDVacek JLRowe SK: Reversible left ventricular dysfunction after subarachnoid hemorrhage. Am Heart J 126:2352401993

  • 18

    Hunt DMcRae CZapf P: Electrocardiographic and serum enzyme change in subarachnoid hemorrhage. Am Heart J 77:4794881969

  • 19

    Jain RDeveikis JThompson BG: Management of patients with stunned myocardium associated with subarachnoid hemorrhage. AJNR Am J Neuroradiol 25:1261292004

  • 20

    Karch SBBillingham ME: Myocardial contraction bands revisited. Hum Pathol 17:9131986

  • 21

    Kawai SSuzuki HYamaguchi HTanaka KSawada HAiza-wa T: Ampulla cardiomyopathy (‘Takotsubo’ cardiomyopa-thy)—reversible left ventricular dysfunction: with ST segment elevation. Jpn Circ J 64:1561592000

  • 22

    Kono TMorita HKuroiwa TOnaka HTakatsuka HFujiwara A: Left ventricular wall motion abnormalities in patients with subarachnoid hemorrhage: neurogenic stunned myocardium. J Am Coll Cardiol 24:6366401994

  • 23

    Kyuma MTsuchihashi KShinshi YHase MNakata TOoiwa H: Effect of intravenous propranolol on left ventricular apical ballooning without coronary artery stenosis (ampulla cardiomyopathy): three cases. Circ J 66:118111842002

  • 24

    Lambert EDu XJPercy ELambert G: Cardiac response to nor-epinephrine and sympathetic nerve stimulation following experimental subarachnoid hemorrhage. J Neurol Sci 198:43502002

  • 25

    Manno EMPfeifer EACascino GDNoe KHWijdicks EFM: Cardiac pathology in status epilepticus. Ann Neurol 58:9549572005

  • 26

    Masuda TSato KYamamoto SMatsuyama NShimohama TMatsunaga A: Sympathetic nervous activity and myocardial damage immediately after subarachnoid hemorrhage in a unique animal model. Stroke 33:167116762002

  • 27

    Mayer SAFink MEHomma SSherman DLiMandri GLenni-han L: Cardiac injury associated with neurogenic pulmonary edema following subarachnoid hemorrhage. Neurology 44:8158201994

  • 28

    Mayer SALiMandri GSherman DLennihan LFink MESolomon RA: Electrocardiographic markers of abnormal left ventricular wall motion in acute subarachnoid hemorrhage. J Neurosurg 83:8898961995

  • 29

    Mayer SALin JHomma SSolomon RALennihan LSherman D: Myocardial injury and left ventricular performance after subarachnoid hemorrhage. Stroke 30:7807861999

  • 30

    Naredi SLambert GEden EZall SRunnerstam MRydenhag B: Increased sympathetic nervous activity in patients with nontraumatic subarachnoid hemorrhage. Stroke 31:9019062000

  • 31

    Novitzky DWicomb WNCooper KCRose AGReichart B: Prevention of myocardial injury during brain death by total cardiac sympathectomy in the chacma baboon. Ann Thorac Surg 41:5205241986

  • 32

    Parekh NVenkatesh BCross DLeditschke AAtherton JMiles W: Cardiac troponin I predicts myocardial dysfunction in aneurysmal subarachnoid hemorrhage. J Am Coll Cardiol 36:132813352000

  • 33

    Pollick CCujec BParker STator C: Left ventricular wall motion abnormalities in subarachnoid hemorrhage: an echocardiographic study. J Am Coll Cardiol 12:6006051988

  • 34

    Sakka SGHuettemann EReinhart K: Acute left ventricular dysfunction and subarachnoid hemorrhage. J Neurosurg Anesthe-siol 11:2092131999

  • 35

    Sharkey SWLesser JRZenovich AGMaron MSLindberg JLonge TF: Acute and reversible cardiomyopathy provoked by stress in women from the United States. Circulation 111:4724792005

  • 36

    Sugiura MYozawa YKubo OKitamura KKimata SHagiwara H: [Myocardial damage (myocytolysis) caused by subarach-noid hemorrhage.]. No To Shinkei 37:115511611985. (Jpn)

  • 37

    Takaki AOgawa HWakeyama TIwami TKimura MTanaka T: [Ampulla cardiomyopathy with left ventricular apical mural thrombi resolved by anticoagulant therapy without systemic complication: a case report.]. J Cardiol 44:2432502004. (Jpn)

  • 38

    Takeno YEno SHondo TMatsuda KZushi N: [Pheochromo-cytoma with reversal of tako-tsubo-like transient left ventricular dysfunction: a case report.]. J Cardiol 43:2812872004. (Jpn)

  • 39

    Temes RESchmidt JMNaidech AMFrontera JAWartenberg KEOstapkovich ND: Association of lowest left ventricular function by transthoracic echocardiography (TTE), stroke from delayed vasospasm and 14 day functional outcome after acute aneurysmal subarachnoid hemorrhage. Neurocritical Care 2:2212005. (Abstract)

  • 40

    Tsuchihashi KUeshima KUchida TOh-mura NKimura KOwa M: Transient left-ventricular apical ballooning without coronary artery stenosis: a novel heart syndrome mimicking acute myocardial infarction Angina Pectoris-Myocardial infarction Investigations in Japan. J Am Coll Cardiol 38:11182001

  • 41

    Tung PKopelnik ABanki NOng KKo NLawton MT: Predictors of neurocardiogenic injury after subarachnoid hemorrhage. Stroke 35:5485512004

  • 42

    Ueyama T: Emotional stress-induced Tako-tsubo cardiomyopa-thy: animal model and molecular mechanism. Ann N Y Acad Sci 1018:4374442004

  • 43

    Wittstein ISThieman DRLima JABaughman KLSchulman SPGerstenblith G: Neurohumoral features of myocardi-al stunning due to sudden emotional stress. N Engl J Med 352:5395482005

  • 44

    Yoshikawa DHara TTakahashi KMorita TGoto F: An association between QTc prolongation and left ventricular hypokinesis during sequential episodes of subarachnoid hemorrhage. Anesth Analg 89:9629641999

  • 45

    Yuki KKodama YOnda JEmoto KMorimoto TUozumi T: Coronary vasospasm following subarachnoid hemorrhage as a cause of stunned myocardium Case report. J Neurosurg 75:3083111991

  • 46

    Zaroff JGRordorf GANewell JBOgilvy CSLevinson JR: Cardiac outcome in patients with subarachnoid hemorrhage and electrocardiographic abnormalities. Neurosurgery 44:34401999

  • 47

    Zaroff JGRordorf GAOgilvy CSPicard MH: Regional patterns of left ventricular systolic dysfunction after subarachnoid hemorrhage: evidence for neurally mediated cardiac injury. J Am Soc Echocardiogr 13:7747792000

  • 48

    Zaroff JGRordorf GATitus JSNewell JBNowak NJTorchiana DF: Regional myocardial perfusion after experimental subarachnoid hemorrhage. Stroke 31:113611432000

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