Abstract
Takotsubo cardiomyopathy (TC) is a syndrome of transient left ventricular (LV) dysfunction mimicking acute coronary syndrome. Although the mechanisms underlying the occurrence of TC are unknown, several imaging techniques contribute to its diagnosis. Here we review the current knowledge about TC, in particular, the pathophysiology and the role of imaging including nuclear cardiovascular medicine.
Similar content being viewed by others
Abbreviations
- 123I-BMIPP:
-
Iodine-123-labeled beta-methyl-P-iodophenylpentadecanoic acid
- 123I-MIBG:
-
Iodine-123-labeled metaiodobenzylguanidine
- 18F-FDG:
-
Fluorine-18-labeled fluorodeoxyglucose
- ACS:
-
Acute coronary syndrome
- AR:
-
Adrenergic receptor
- CBF:
-
Cerebral blood flow
- CFR:
-
Coronary flow reserve
- CMR:
-
Cardiovascular magnetic resonance
- ECG:
-
Electrocardiography
- LV:
-
Left ventricle/ventricular
- EF:
-
Ejection fraction
- MBF:
-
Myocardial blood flow
- PET:
-
Positron emission tomography
- SPECT:
-
Single-photon emission computed tomography
- TC:
-
Takotsubo cardiomyopathy
References
Sato H, Uchida T, Dote K, Ishihara M. Tako-tsubo-like left ventricular dysfunction due to multivessel coronary spasm. In: Kodama K, Haze K, Hori M, editors. Clinical aspect of myocardial injury: From ischemia to heart failure. Tokyo: Kagakuhyoronsha Publishing; 1990. p. 56–64.
Brandspiegel HZ, Marinchak RA, Rials SJ, Kowey PR. A broken heart. Circulation 1998;98:1349.
Tsuchihashi K, Ueshima K, Uchida T, Oh-mura N, Kimura K, Owa M, et al. 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 2001;38:11–8.
Pessoa PM, Xavier SS, Lima SL, Mansur J, de Almeida AS, Carvalh PAC, et al. Assessment of takotsubo (ampulla) cardiomyopathy using iodine-123 metaiodobenzylguanidine scintigraphy. Acta Radiol 2006;47:1029–35.
Rendl G, Altenberger J, Pirich C. Takotsubo cardiomyopathy in positron emission tomography. Wien Klin Wochenschr 2006;118:520.
Kurowski V, Kaiser A, von Hof K, Killermann DP, Björn M, Franz H, et al. Apical and midventricular transient left ventricular dysfunction syndrome (tako-tsubo cardiomyopathy): frequency, mechanisms, and prognosis. Chest 2007;132:809–16.
Sharkey SW, Windenburg DC, Lesser JR, Maron MS, Hauser RG, Lesser JN, et al. Natural history and expansive clinical profile of stress (tako-tsubo) cardiomyopathy. J Am Coll Cardiol 2010;55:333–41.
Gianni M, Dentali F, Grandi AM, Sumner G, Hiralal R, Lonn E. Apical ballooning syndrome or takotsubo cardiomyopathy: A systematic review. Eur Heart J 2006;27:1523–9.
Templin C, Ghadri JR, Diekmann J, Napp LC, Bataiosu DR, Jaguszewski M, et al. Clinical features and outcomes of takotsubo (stress) cardiomyopathy. N Engl J Med 2015;373:929–38.
Elesber AA, Prasad A, Lennon RJ, Wright RS, Lerman A, Rihal CS. Four-year recurrence rate and prognosis of the apical ballooning syndrome. J Am Coll Cardiol 2007;50:448–52.
Ikeda E, Hisamatsu K, Kijima Y, Mizoguchi H, Urakawa S, Kimura H. Morphologically unique feature of recurrent ampulla (takotsubo) cardiomyopathy. Circ J 2009;73:371–5.
Sharkey SW, Lesser JR, Maron BJ. Cardiology patient page. Takotsubo (stress) cardiomyopathy. Circulation 2011;124:e460–2.
Citro R, Previtali M, Bovelli D, Vriz O, Astarita C, Patella MM, et al. Chronobiological patterns of onset of Tako-Tsubo cardiomyopathy: A multicenter Italian study. J Am Coll Cardiol 2009;54:180–1.
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;41:737–42.
Sharkey SW, Lesser JR, Zenovich AG, Maron MS, Lindberg J, Longe TF. Acute and reversible cardiomyopathy provoked by stress in women from the United States. Circulation 2005;111:472–9.
Sharkey SW, LessWittstein IS, Thiemann DR, Lima JA, Baughman KL, Schulman SP. Neurohumoral features of myocardial stunning due to sudden emotional stress. N Engl J Med 2005;352:539–48.
Akashi YJ, Goldstein DS, Barbaro G, Ueyama T. Takotsubo cardiomyopathy: a new form of acute, reversible heart failure. Circulation 2008;118:2754–62.
Dorfman T, Aqel R, Allred J, Woodham R, Iskandrian AE. Takotsubo cardiomyopathy induced by treadmill exercise testing: an insight into the pathophysiology of transient left ventricular apical (or midventricular) ballooning in the absence of obstructive coronary artery disease. J Am Coll Cardiol 2007;49:1223–5.
Bossone E, Citro R, Eagle KA, Manfredini R. Tako-tsubo cardiomyopathy: Is there a preferred time of onset? Intern Emerg Med 2011;6:221–6.
Ruiz S, Martinez-Marin M, Luque P, Nassar N, Oros D. Takotsubo cardiomyopathy after cesarean section: A case report and literature review. J Obstet Gynaecol Res 2017;43:392–6.
Crimi E, Baggish A, Leffert L, Pian-Smith MC, Januzzi JL, Jiang Y. Images in cardiovascular medicine. Acute reversible stress-induced cardiomyopathy associated with cesarean delivery under spinal anesthesia. Circulation 2008;117:3052–3.
Citro R, Giudice R, Mirra M, Petta R, Baldi C, Bossone E. Is Tako-tsubo syndrome in the postpartum period a clinical entity different from peripartum cardiomyopathy? J Cardiovasc Med (Hagerstown) 2013;14:568–75.
Wittstein IS. The sympathetic nervous system in the pathogenesis of takotsubo syndrome. Heart Fail Clin 2016;12:485–98.
Jamali HK, Waqar F, Gerson MC. Cardiac autonomic innervation. J Nucl Cardiol 2017;24:1558–70.
Wybraniec MT, Mizia-Stec K, Krzych L. Neurocardiogenic injury in subarachnoid hemorrhage: A wide spectrum of catecholamin-mediated brain-heart interactions. Cardiol J 2014;21:220–8.
Golbidi S, Frisbee JC, Laher I. Chronic stress impacts the cardiovascular system: animal models and clinical outcomes. Am J Physiol Heart Circ Physiol 2015;308:H1476–98.
Paur H, Wright PT, Sikkel MB, Tranter MH, Mansfield C, O’Gara P. High levels of circulating epinephrine trigger apical cardiodepression in a beta2-adrenergic receptor/Gi-dependent manner: A new model of takotsubo cardiomyopathy. Circulation 2012;126:697–706.
Ueyama T, Hano T, Kasamatsu K, Yamamoto K, Tsuruo Y, Nishio I. Estrogen attenuates the emotional stress-induced cardiac responses in the animal model of Tako-tsubo (Ampulla) cardiomyopathy. J Cardiovasc Pharmacol 2003;42:S117–9.
Izumi Y, Okatani H, Shiota M, Nakao T, Ise R, Kitoe G. Effects of metoprolol on epinephrine-induced takotsubo-like left ventricular dysfunction in non-human primates. Hypertens Res 2009;32:339–46.
Lyon AR, Rees PS, Prasad S, Poole-Wilson PA, Harding SE. Stress (takotsubo) cardiomyopathy: A novel pathophysiological hypothesis to explain catecholamine-induced acute myocardial stunning. Nat Clin Pract Cardiovasc Med 2008;5:22–9.
Mantravadi R, Gabris B, Liu T, Choi BR, de Groat WC, Ng GA. Autonomic nerve stimulation reverses ventricular repolarization sequence in rabbit hearts. Circ Res 2007;100:e72–80.
Ueyama T, Kasamatsu K, Hano T, Yamamoto K, Tsuruo Y, Nishio I. Emotional stress induces transient left ventricular hypocontraction in the rat via activation of cardiac adrenoceptors: a possible animal model of ‘tako-tsubo’ cardiomyopathy. Circ J 2002;66:712–3.
Steptoe A, Kivimaki M. Stress and cardiovascular disease. Nat Rev Cardiol 2012;9:360–70.
Mendelsohn ME, Karas RH. The protective effects of estrogen on the cardiovascular system. N Engl J Med 1999;340:1801–11.
Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 1997;388:507–25.
Ueyama T, Ishikura F, Matsuda A, Asanuma T, Ueda K, Ichinose M. Chronic estrogen supplementation following ovariectomy improves the emotional stress-induced cardiovascular responses by indirect action on the nervous system and by direct action on the heart. Circ J 2007;71:565–73.
Akashi YJ, Nef HM, Lyon AR. Epidemiology and pathophysiology of takotsubo syndrome. Nat Rev Cardiol 2015;12:387–97.
Suzuki H, Matsumoto Y, Kaneta T, Sugimura K, Takahashi J, Fukumoto Y. Evidence for brain activation in patients with takotsubo cardiomyopathy. Circ J 2014;78:256–8.
Smeijers L, Szabó BM, van Dammen L, Wonnink W, Jakobs BS, Bosch JA. Emotional, neurohormonal, and hemodynamic responses to mental stress in Tako-Tsubo cardiomyopathy. Am J Cardiol 2015;115:1580–6.
Feola M, Chauvie S, Rosso GL, Biggi A, Ribichini F, Bobbio M. Reversible impairment of coronary flow reserve in takotsubo cardiomyopathy: A myocardial PET study. J Nucl Cardiol 2008;15:811–7.
Kawai S, Kitabatake A, Tomoike H, Takotsubo Cardiomyopathy G. Guidelines for diagnosis of takotsubo (ampulla) cardiomyopathy. Circ J 2007;71:990–2.
Prasad A, Lerman A, Rihal CS. Apical ballooning syndrome (Tako-Tsubo or stress cardiomyopathy): a mimic of acute myocardial infarction. Am Heart J 2008;155:408–17.
Donohue D, Ahsan C, Sanaei-Ardekani M, Movahed MR. Early diagnosis of stress-induced apical ballooning syndrome based on classic echocardiographic findings and correlation with cardiac catheterization. J Am Soc Echocardiogr 2005;18:1423.
Kagiyama N, Okura H, Kume T, Hayashida A, Yoshida K. Isolated right ventricular takotsubo cardiomyopathy. Eur Heart J Cardiovasc Imaging 2015;16:285.
Kagiyama N, Okura H, Tamada T, Imai K, Yamada R, Kume T. Impact of right ventricular involvement on the prognosis of takotsubo cardiomyopathy. Eur Heart J Cardiovasc Imaging 2016;17:210–6.
Manabe O, Kikuchi T, Scholte A, Mahdiui M, Zhang M-R, Mahdiui M. Radiopharmaceutical tracers for cardiac imaging. J Nucl Cardiol 2017. https://doi.org/10.1007/s12350-017-1131-5.
Owa M, Aizawa K, Urasawa N, Ichinose H, Yamamoto K, Karasawa K. Emotional stress-induced ‘ampulla cardiomyopathy’: Discrepancy between the metabolic and sympathetic innervation imaging performed during the recovery course. Jpn Circ J 2001;65:349–52.
Christensen TE, Ahtarovski KA, Bang LE, Holmvang L, Søholm H, Ghotbi AA. Basal hyperaemia is the primary abnormality of perfusion in Takotsubo cardiomyopathy: A quantitative cardiac perfusion positron emission tomography study. Eur Heart J Cardiovasc Imaging 2015;16:1162–9.
Sestini S, Pestelli F, Leoncini M, Bellandi F, Mazzeo C, Mansi L, et al. The natural history of takotsubo syndrome: A 2-year follow-up study with myocardial sympathetic and perfusion G-SPECT imaging. Eur J Nucl Med Mol Imaging 2017;44:267–83.
Ito K, Sugihara H, Kinoshita N, Azuma A, Matsubara H. Assessment of Takotsubo cardiomyopathy (transient left ventricular apical ballooning) using 99mTc-tetrofosmin, 123I-BMIPP, 123I-MIBG and 99mTc-PYP myocardial SPECT. Ann Nucl Med 2005;19:435–45.
Sato A, Aonuma K, Nozato T, Sekiguchi Y, Okazaki O, Kubota K, et al. Stunned myocardium in transient left ventricular apical ballooning: a serial study of dual I-123 BMIPP and Tl-201 SPECT. J Nucl Cardiol 2008;15:671–9.
Marfella R, Barbieri M, Sardu C, Rizzo MR, Siniscalchi M, Paolisso P. Effects of alpha-lipoic acid therapy on sympathetic heart innervation in patients with previous experience of transient takotsubo cardiomyopathy. J Cardiol 2016;67:153–61.
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.
Cheung RT, Hachinski V. The insula and cerebrogenic sudden death. Arch Neurol 2000;57:1685–8.
Nef HM, Möllmann H, Kostin S, Troidl C, Voss S, Weber M. Tako-Tsubo cardiomyopathy: Intraindividual structural analysis in the acute phase and after functional recovery. Eur Heart J 2007;28:2456–64.
Yoshida T, Hibino T, Kako N, Murai S, Oguri M, Kato K, et al. A pathophysiologic study of tako-tsubo cardiomyopathy with F-18 fluorodeoxyglucose positron emission tomography. Eur Heart J 2007;28:2598–604.
Kobylecka M, Budnik M, Kochanowski J, Piatkowski R, Chojnowski M, Fronczewska-Wieniawska K, et al. Takotsubo cardiomyopathy: FDG myocardial uptake pattern in fasting patients. Comparison of PET/CT, SPECT, and ECHO results. J Nucl Cardiol 2017. https://doi.org/10.1007/s12350-016-0775-x.
Akutsu Y, Kaneko K, Kodama Y, Li HL, Nishimura H, Hamazaki Y. Technetium-99m pyrophosphate/thallium-201 dual-isotope SPECT imaging predicts reperfusion injury in patients with acute myocardial infarction after reperfusion. Eur J Nucl Med Mol Imaging 2009;36:230–6.
Prasad A, Madhavan M, Chareonthaitawee P. Cardiac sympathetic activity in stress-induced (takotsubo) cardiomyopathy. Nat Rev Cardiol 2009;6:430–4.
Eitel I, von Knobelsdorff-Brenkenhoff F, Bernhardt P, Carbone I, Muellerleile K, Aldrovandi A, et al. Clinical characteristics and cardiovascular magnetic resonance findings in stress (takotsubo) cardiomyopathy. JAMA 2011;306:277–86.
Haghi D, Athanasiadis A, Papavassiliu T, Suselbeck T, Fluechter S, Mahrholdt H, et al. Right ventricular involvement in takotsubo cardiomyopathy. Eur Heart J 2006;27:2433–9.
Crimizade U, Messas N, Blondet C, Jesel L, Duculescu E, Ohlmann P, et al. Biventricular takotsubo cardiomyopathy triggered by myocardial ischemic injury: Insights from multimodal imaging approach. Int J Cardiol 2016;207:104–6.
Christensen TE, Bang LE, Holmvang L, Ghotbi AA, Lassen ML, Andersen F, et al. Cardiac 99mTc sestamibi SPECT and 18F FDG PET as viability markers in takotsubo cardiomyopathy. Int J Cardiovasc Imaging 2014;30:1407–16.
Ghadri JR, Dougoud S, Maier W, Kaufmann PA, Gaemperli O, Prasad A. A PET/CT-follow-up imaging study to differentiate takotsubo cardiomyopathy from acute myocardial infarction. Int J Cardiovasc Imaging 2014;30:207–9.
Ibrahim T, Nekolla SG, Langwieser N, Rischpler C, Groha P, Laugwitz KL, et al. Simultaneous positron emission tomography/magnetic resonance imaging identifies sustained regional abnormalities in cardiac metabolism and function in stress-induced transient midventricular ballooning syndrome: A variant of takotsubo cardiomyopathy. Circulation 2012;126:324–6.
Miyachi H, Kumita S, Tanaka K. PET/CT and SPECT/CT cardiac fusion imaging in a patient with takotsubo cardiomyopathy. Eur Heart J 2013;34:397.
Skovgaard D, Holmvang L, Bang LE, Lonborg J, Hasbak P. Imaging of takotsubo cardiomyopathy. Clin Nucl Med 2010;35:967–71.
Bonnemeier H, Demming T, Weidtmann B, Ortak J, Burgdorf C, Reppel M, et al. Differential heart rate dynamics in transient left ventricular apical and midventricular ballooning. Heart Rhythm 2010;7:1825–32.
Cimarelli S, Sauer F, Morel O, Ohlmann P, Constantinesco A, Imperiale A. Transient left ventricular dysfunction syndrome: Patho-physiological bases through nuclear medicine imaging. Int J Cardiol 2010;144:212–8.
Morel O, Sauer F, Imperiale A, Cimarelli S, Blondet C, Jesel L, et al. Importance of inflammation and neurohumoral activation in takotsubo cardiomyopathy. J Card Fail 2009;15:206–13.
Burgdorf C, Bonnemeier H, von Hof K, Schunkert H, Kurowski V. Coronary artery vasospasm or true transient left ventricular apical ballooning? Differentiation by nuclear imaging. J Nucl Cardiol 2008;15:599–603.
Cimarelli S, Imperiale A, Ben-Sellem D, Rischner J, Detour J, Morel O, et al. Nuclear medicine imaging of takotsubo cardiomyopathy: Typical form and midventricular ballooning syndrome. J Nucl Cardiol 2008;15:137–41.
Obunai K, Misra D, Van Tosh A, Bergmann SR. Metabolic evidence of myocardial stunning in takotsubo cardiomyopathy: A positron emission tomography study. J Nucl Cardiol 2005;12:742–4.
Ito S, Endo A, Morita Y, Tanabe K. Midventricular takotsubo cardiomyopathy on 99mTc-tetrofosmin and (123)I-BMIPP SPECT. Intern Med 2018;57:449–51.
Iida K, Matsumoto N, Makita A, Suzuki Y, Yoda S, Hirayama A. Depiction of the discrepancy between fatty-acid metabolism and myocardial perfusion in takotsubo cardiomyopathy using dedicated cardiac semiconductor gamma camera. Int J Cardiol 2016;223:161–2.
Nagai T, Konishi T, Arakawa J, Hisadome H, Tabata H. Synchronicity of echocardiography and cardiac nuclear medicine in mid-ventricular ballooning syndrome: Paired ‘ring signs’ on polar maps. Eur Heart J Cardiovasc Imaging 2014;15:947.
Shimizu M, Nishizaki M, Yamawake N, Fujii H, Sakurada H, Isobe M, et al. J wave and fragmented QRS formation during the hyperacute phase in Takotsubo cardiomyopathy. Circ J 2014;78:943–9.
Matsuo S, Nakajima K, Kinuya S, Yamagishi M. Diagnostic utility of 123I-BMIPP imaging in patients with Takotsubo cardiomyopathy. J Cardiol 2014;64:49–56.
Ishibashi K, Osamura T, Yamahara Y. Myocardial stunning with partial aneurysmal formation generated during the recovering process of tachycardia-induced cardiomyopathy. J Cardiol 2009;54:121–7.
Uchida Y, Nanjo S, Fujimoto S, Yamashina S, Wagatsma K, Nakano H. Scintigraphic studies on the etiology of ampulla cardiomyopathy. J Cardiol 2008;51:121–30.
Sakuragi S, Tokunaga N, Okawa K, Kakishita M, Ohe T. A case of takotsubo cardiomyopathy associated with epileptic seizure: Reversible left ventricular wall motion abnormality and ST-segment elevation. Heart Vessel 2007;22:59–63.
Fukui M, Mori Y, Tsujimoto S, Takehana K, Sakamoto N, Kishimoto N. Takotsubo cardiomyopathy in a maintenance hemodialysis patient. Ther Apher Dial 2006;10:94–100.
Ohwada R, Hotta M, Kimura H, Takagi S, Matsuda N, Nomura K. Ampulla cardiomyopathy after hypoglycemia in three young female patients with anorexia nervosa. Intern Med 2005;44:228–33.
Suzuki K, Osada N, Akasi YJ, Suzuki N, Sakakibara M, Miyake F, et al. An atypical case of “takotsubo cardiomyopathy” during alcohol withdrawal: Abnormality in the transient left ventricular wall motion and a remarkable elevation in the ST segment. Intern Med 2004;43:300–5.
Messas N, Blondet C, Jesel L, Hess S, Girardey M, Imperiale A. Diagnostic relevance of optical coherence tomography imaging in aborted acute myocardial infarction with a “takotsubo component”. Int J Cardiol 2015;195:123–5.
Harris D, Wong TC, Soman P. Direct visualization of regional cardiac sympathetic dysfunction in stress-induced cardiomyopathy. J Nucl Cardiol 2015;22:1317–9.
Ikutomi M, Yamasaki M, Matsusita M, Watari Y, Arashi H, Endo G. Takotsubo cardiomyopathy in siblings. Heart Vessel 2014;29:119–22.
Chrapko BE, Tomaszewski A, Jaroszynski AJ, Furmaga J, Wysokinski A, Rudzki S. Takotsubo syndrome in a patient after renal transplantation. Med Sci Monit 2012;18:CS26–30.
Lerida MJC, Cerrato MCM, Arias CD, Ruiz AL, Gueto JC. Transient apical dysfunction syndrome (Tako-Tsubo) simulating acute myocardial infarction. J Revista Espanola de Medicina Nuclear 2011;30:107–11.
Izumi K, Tada S, Yamada T. A case of Takotsubo cardiomyopathy complicated by ventricular septal perforation. Circ J 2008;72:1540–3.
Burgdorf C, von Hof K, Schunkert H, Kurowski V. Regional alterations in myocardial sympathetic innervation in patients with transient left-ventricular apical ballooning (Tako-Tsubo cardiomyopathy). J Nucl Cardiol 2008;15:65–72.
Takeoka Y, Nakamae M, Nakamae H, Hagihara K, Sakamoto E, Nakane T. Two cases of ampulla (takotsubo-shaped) cardiomyopathy associated with hemophagocytic lymphohistiocytosis. Acta Haematol 2007;117:205–10.
Miyazaki S, Kamiishi T, Hosokawa N, Komura M, Konagai H, Sagai H. Reversible left ventricular dysfunction “takotsubo” cardiomyopathy associated with hyperthyroidism. Jpn Heart J 2004;45:889–94.
Acknowledgments
We thank Mitsunori Ohtsubo and Eriko Suzuki for their support.
Disclosures
All authors have nothing to disclose.
Author information
Authors and Affiliations
Corresponding author
Additional information
The authors of this article have provided a PowerPoint file, available for download at SpringerLink, which summarizes the contents of the paper and is free for re-use at meetings and presentations. Search for the article DOI on SpringerLink.com.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Manabe, O., Naya, M., Oyama-Manabe, N. et al. The role of multimodality imaging in takotsubo cardiomyopathy. J. Nucl. Cardiol. 26, 1602–1616 (2019). https://doi.org/10.1007/s12350-018-1312-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12350-018-1312-x