COVID-19-associated stress cardiomyopathy
Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: Sara Zand, M.D.[2] José Eduardo Riceto Loyola Junior, M.D.[3]
Synonyms and keywords: Takotsubo syndrome, TTS, Takotsubo cardiomyopathy, broken heart syndrome, Stress cardiomyopathy
Overview
COVID-19-associated stress cardiomyopathy was first described by Elena Roca, an Italian physician, in April 2020. This disorder is the result of extreme sympathetic stimulation due to the abnormal release of catecholamines and cortisol leading to rapid, severe, reversible cardiac dysfunction, as well as, wall motion abnormality of the left ventricle subtending more than one coronary artery territory, without evidence of significant obstructive coronary artery disease. Few cases of stress cardiomyopathy reported in literature due to direct consequences of covid-19 on the myocardium. However, due to increased psychological, social, economical distress during covid-19 pandemic, the incidence of stress cardiomyopathy in non-covid-19 patients increased significantly compared with prepandemic periods. In general, stress cardiomyopathy may develope in the setting of emotional stress or secondary to infections such as covid-19. The latter may have worse prognosis in terms of mortality compared with emotional trigger.
Historical Perspective
- COVID-19-associated stress cardiomyopathy was first described by Elena Roca, an Italian physician, in April 2020.[1]
Classification
- Takotsubo cardiomyopathy is classified as follows:[2]
- Primary takotsubo cardiomyopathy: acute cardiac symptoms resulting from emotional or physical stress, main cause of seeking medical attention
- Secondary takotsubo cardiomyopathy: developing in hospitalized patients for other reasons
| Apical type | Midventricular type | Basal type | Focal type |
|---|---|---|---|
| Common type (>80%), hypokinesia or dyskinesia of midventricular and apical parts of anterior, septal, inferior and lateral walls of left ventricle associated with hyperkinesia of basal segments | Hypokinesia or dyskinesia of midventricular segments, like a cuff in most cases, with normokinesia or hyperkinesia of basal and apical segments | Inverse takotsubo cardiomyopathy, wall motion abnormality is reciprocal to apical type, hypokinesia or dyskinesia of basal segments, normokinesia or hyperkinesia of midventricular, anterior, antroseptal, and antroapikal segments of left ventricle | Focal hypkinesia or dyskinesia of any segments of the left ventricle , commonly antroseptal wall |
Pathophysiology
- Inflammation and cytokine storm are the underlying mechanisms of cathecolamines release in patients with covid-19.
- It is thought that COVID-19-associated stress cardiomyopathy is the result of extreme sympathetic stimulation due to abnormal release of catecholamines such as epinephrine, norepinephrine, dopamine and also high level of cortisol.
- Increase level of cathecolamines and cortisol in patients with covid-19 may cause direct toxic effect on cardiomyocytes and stress cardiomyopathy.
- Direct effect of cathecolamine on cardiomyocytes may lead to myocardial stunning, hyperdynamic contractility, multiple vessles spasm, and/or microvascular dysfunction.
- Increased cortisol level observed in patients with covid-19 may cause isometric tension, reduced relaxasion of papillary muscles, reduced total relaxation time, without any effect on contraction time.[3]
- The mechanisms occurring in COVID-19 patients may lead to myocardial injury and left ventricular dysfunction are:.[4]
- Stress-induced adrenergic discharge as consequence of fever and inflammatory response to infection
- The direct SARS-CoV-2 injury causing endothelial dysfunction, which may cause microvascular vasoconstriction that can manifest in a transient left ventricular apical dysfunction, (apical ballooning).[5]
- Proposed mechanisms that have the potential to cause myocardial injury in acute coronavirus disease 2019 cardiovascular syndrome:[6]
| Stress Induced Cardiomyopathy | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
| Microvascular/Thrombotic Injury | Cytokine Storm | ||||||||||||||||||||||||||||||||||||||||||||||||||||||
| Pre-existing cardiovascular Disease | Acute Myocardial Injury Characterized by Abnormal Troponin | Viral Myocarditis | |||||||||||||||||||||||||||||||||||||||||||||||||||||
| Hypoxemia | Hypotension +/- Shock | ||||||||||||||||||||||||||||||||||||||||||||||||||||||
| Ventricular or atrial arrhythmias | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Causes
Common causes of stress cardiomyopathy include:
- Physical stressors
- Emotional stressors (anger, argument, surgery, natural disasters, grief, happiness)
- Several medications
- General anesthesia
- Infectious disease
- Novel coronavirus disease 2019[5]
Differentiating COVID-19-associated stress cardiomyopathy from other Diseases
- For further information about the differential diagnosis, click here.
- To view the differential diagnosis of COVID-19, click here.
| Differentiating diagnosis | Takotsubo cardiomyopathy | STEMI |
|---|---|---|
| Stressful trigger | Prominent stressful event (79%) | 8% |
| Elevated troponin on admission | 91% | 37% |
| LVEF<40% | Higher incidence of decreased LVEF at presentation (80%) | 31% |
| Symptoms | Chest pain (73%) | Higher rate of chest pain (100%) |
| Sex | Female | Male |
| Age | Older age (66 years old) | Mean age 60 years old |
| Risk factors | Lower incidence of HLP, smoking, diabetes mellitus | HLP, smoking, diabetes mellitus |
| Coronary angiography | Lower incidence of stenosis> 50% (15%) | Stenosis> 50% in 100% |
| In-hospital mortality | 1.3% | 3.6% |
Epidemiology and Demographics
- The incidence of stress cardiomyopathyassociated covid-19 is approximately 7.8% of all patients presenting acute coronary syndrome which is higher than pre-pandemic period.[5]
- In critically ill covid-19 patients, the incidence of stress cardiomyopathy is approximitely 2-4%, compared to 1-2% among general population.[7]
Age
- Stress cardiomyopathy is more commonly observed among elderly patients with a mean age of 64.6 years.
Gender
- Male are more commonly affected with stress cardiomyopathy secondary to covid-19.
- Primary stress cardiomyopathy is much more common in women..
Race
- There is no racial predilection for stress cardiomyopathy in covid-19 patients.
Risk Factors
- There are no established risk factors for COVID-19-associated stress cardiomyopathy.
- In general population, secondary stress cardiomyopathy is much more commen in older men , as well as with higher incidence of conventional risk factors including HTN, diabetes mellitus, dyslipidemia, cerebrovascular disease, cardiac arrhythmia.
- Common risk factors in reported takotsubo cardiomyopathy secondary to covid-19 include:
- Atrial fibrillation
- Psychiatric illness
- Hypoxia
- Severe covid-19 pneumonia requiring mechanical ventilation support
- Common triggers associated with development of secondary takotsubo cardiomyopathy in severe covid-19 pneumonia include:[8][2]
- Respiratory condition
- Intubation
- Medication use
- Epinephrine use
- Anxiety
- Betablocker withdraw
Screening
- There is insufficient evidence to recommend routine screening for COVID-19-associated stress cardiomyopathy.
Natural History, Complications, and Prognosis
- There are varied degree of the recovery of patients with stress cardiomyopathy associated covid-19 reported in literature within two months.[9] [10][11]
- Early clinical features include acute coronary syndrome with chest pain and ECG changes and rise of troponin, acute pulmonary edema, decreased oxygen saturation without response to O2 therapy, hemodynamic instability.
- Patients with stress cardiomyopathy associated with covid-19 had a longer hospital days admission compared with the pre-pandemic period.[5]
- In the presence of cardiogenic shock, stress cardiomyopathy in critically ill covid-19 patients may progress to develop pulmonary edema, hemodynamic collapse, and death.
- Patients with secondary takotsubo cardiomyopathy may experience cardiogenic shock, respiratory failure requiring mechanical ventilation support and coagulation disorder. However, in reported patients with takotsubo cardiomyopathy exacerbation of respiratory status may be due to covid-19 complicating takotsubo cardiomyopathy.
- Some patients may recover and have a normalized cardiac function within a few weeks. .[12][13][14]
- Prognosis of stress cardiomyopathy associated covid-19 is not clearly described yet, and mortality rate of patients with stress cardiomyopathy without covid-19 infection is approximately 5% during pandemic (similar to pre-pandemic covid-19 period). However, the mortality rate of takotsubo cardiomyopathy secondary to covid-19 pneumonia is 10 times higher than non-covid-19 patients.[5]
- Complications of stress cardiomyopathy include:[12][15][16][14][17][18][19][20][21][22]
- Severe Heart failure
- Acute pulmonary edema
- Cardiogenic shock
- Dynamic left ventricular outflow tract obstruction (peak gradients >25 mmhg in echo or cath)
- Hypotesion
- Moderete to severe acute functional mitral regurgitation
- Bradycardia
- QT prolongation and ventricular arrhythmias
- Torsade de pointes
- Left ventricular mural thrombus
- Mitral valve dysfunction
- Pulmonary embolism
- Systemic embolism, stroke
- LV free wall rupture
- Acute renal failure
- In-hospital death
Diagnosis
- In the development of new hypotension and tachycardia in intubated covid-19 patients with comorbidities ( HTN, dyslipidemia, atrial fibrillation, previous stroke) or the need for vasodepressor and presence of hypoxia, investigation about stress cardiomyopathy should be done by taking ECG and check of cardiac biomarkers ( troponin, NT-Pro BNP.
- In the presence of any ECG changes or cardiac biomarkers abnormality, transthoracic echocardiography should be done
Diagnostic Study of Choice
- Echocardiography is the gold standard of diagnosis of takotsubo cardiomyopathy.
- High risk feature of takotsubo cardiomyopathy on echocardiography include: LVEF<45%, Moderate to severe MR, right ventricular involvement.
- The diagnosis of stress cardiomyopathy is made when all 4 of the following diagnostic criteria are met:
- Transient hypokinesis, akinesis, or dyskinesis of the left ventricular mid segments with or without apical involvement; the regional wall motion abnormalities extend beyond a single epicardial vascular distribution; a stressful trigger is often, but not always present.
- Absence of obstructive coronary disease or angiographic evidence of acute plaque rupture.
- New electrocardiographic abnormalities (either ST-segment elevation and/or T-wave inversion) or modest elevation in cardiac troponin.
- Absence of pheochromocytoma and myocarditis.[13][12]
- The diagnosis of COVID-19-associated stress cardiomyopathy is largely the same, but happening in the context of a SARS-CoV2 infection.
History and Symptoms
Symptoms of stress cardiomyopathy can mimic acute coronary syndrome. The most common presenting symptoms are:[12][16][13][18][23][17]
- Chest pain or chest tightness
- Shortness of breath
- Vomiting
- Loss of consciousness due to syncope or cardiac arrest in rare cases
- Considering emotional factors such as fear of severity of covid-19, contact with a hospitalized family member, worry about socioeconomic costs, intrusive thoughts about morbidity of covid-19 that may lead to stress cardiomyopathy. [11]
Physical Examination
- The following physical examination findings may be seen in patients with stress cardiomyopathy:[24][12][15][16][14][17][18][19][25][21][26]
| Organ System | Findings | Suggestive Of |
|---|---|---|
| General appearance | Patient may be anxious, ill-appearing or diaphoretic | |
| Vital signs | Cardiogenic shock | |
| Cardiac | Murmurs, S3, gallop rhythm, Displaced point of maximal impulse (PMI) | Heart failure |
| Respiratory | Rales, crackles | Pulmonary edema |
Laboratory Findings
- Laboratory findings consistent with the diagnosis of stress cardiomyopathy in covid-19 patients include elevated troponin and Pro-BNP.[5]
- Elevated levels of serum catecholamines may also be found in patients with stress cardiomyopathy.[12][16][18][17]
- Evidence of ongoing COVID-19 disease is required to establish the diagnosis.
Electrocardiogram
The ECG findings are largely the same of the regular stress cardiomyopathy, and are often confused with those of an acute anterior wall myocardial infarction.[12][18] Findings on ECG include:[12][16][13][14][18][23][17]
- ST elevation in the precordial leads
- T wave inversion
- Q wave formation
- QT prolongation
- New-onset bundle branch block (BBB)
- Rarely, malignant ventricular arrhythmias may be seen
X-ray
Takotsubo refers to a ceramic pot used to trap octopuses in the Japanese language. The typical chest x-ray findings in patients with stress cardiomyopathy include a takotsubo-shaped heart, in which there is apical ballooning and narrowing of the proximal portion near the great vessels.
Echocardiography or Ultrasound
The following echocardiographic findings may be seen in patients with stress cardiomyopathy:[16][13][14][17]
- Apical ballooning
- Apical or mid-segment dyskinesia or akinesia
- Left ventricular systolic dysfunction
- Reduced ejection fraction
CT scan
A cardiac CT scan can also help differentiate between stress cardiomyopathy and acute MI. Regional abnormalities in the wall motion of the heart, along with absence of coronary atherosclerosis support the diagnosis of stress cardiomyopathy over an acute MI.[17]
Chest CT scan may also show findings associated with COVID-19 and they can include:
- Unilateral or bilateral pneumonia[27][28][29]
- Mottling and ground-glass opacity
- Focal or multifocal opacities
- Consolidation
- Septal thickening
- Subpleural and lower lobe involvement more likely
MRI
- Cardiac magnetic resonance (CMR) is a useful imaging modality in distinguishing between stress cardiomyopathy and myocarditis or MI. In the case of myocarditis or MI, there is delayed hyper-enhancement of gadolinium. However, absence of gadolinium hyper-enhancement supports the diagnosis of stress cardiomyopathy. Also, stress cardiomyopathy results in regional wall abnormality and its extent can best be documented using cardiac magnetic resonance.[13][20][30][31][32][33][34][35][20][36][37]
- CMR in stress cardiomyopathy shows absence of irreversible damage and segmental LV dysfunction.[31]
Other findings on CMR include:[17][20]
- Hypokinetic or dyskinetic areas in the wall of the heart
- Myocardial edema
- Apical thrombi
Other Imaging Findings
Positron Emission Tomography (PET) Scan
In patients with stress cardiomyopathy, a PET scan may be done. Areas of hypokinesia or dyskinesia have reduced glucose utilization compared to normal regions.[38]
Coronary Angiography
- Stress cardiomyopathy can mimic an acute MI, mainly anterior MI, since the clinical presentation, ECG and laboratory findings are similar. Hence, coronary angiography is considered a great diagnostic modality to differentiate between the two diagnoses.
- A normal angiography or absence of substantial coronary stenosis supports the diagnosis of stress cardiomyopathy.[18][12][17]
Other Diagnostic Studies
Cardiac Catheterization
When patients with stress cardiomyopathy undergo cardiac catheterization, the following findings are usually reported:[16][18][14]
- Normal anatomy of the coronary arteries, without evidence of acute plaque rupture
- Low ejection fraction (EF)
- Minimal or no evidence of coronary vasospasm
- Minimal disturbance of microcirculation
Myocardial Biopsy
- Myocardial biopsy, although not necessary for diagnosis, can distinguish between stress cardiomyopathy and MI.
- The histological findings on myocardial biopsy in patients with stress cardiomyopathy include:[12][16]
- Inflammatory infiltrates, consisting of mononuclear lymphocytes, leukocytes and macrophages
- Myocardial fibrosis
- Contraction bands, which may or may not be associated with necrosis
- The combination of inflammatory changes and contraction bands distinguish stress cardiomyopathy from coagulative necrosis seen in MI.[12]
Treatment
Medical Therapy
- The mainstay of therapy is supportive care, which is the same for the stress cardiomyopathy not related to COVID-19.
- In mild TTS without signs of heart failure, beta-blocker and ACEI or ARB are recommended and inotropes such as epinephrine, norepinephrine, dobutamine, milrinone, isoproterenol should be avoided.
- In the presence of pulmonary edema without evidence of left ventricular outflow obstruction,administration of ACEI, betablocker, diuretic and nitroglycerin is recommended.
- In the presence of cardiogenic shock and left ventricular outflow obstruction ( in the absent if heart failure), short acting betablocker, IV fluide, impella are recommended.
- Diuretic, nitroglycerin, intraaortic ballon pump should be avoided in the evidence of cardiogenic shock and left ventricular outflow obstruction.
- If there is evidence of pump failure in the context of cardiogenic shock, levosimentan, ECMO, impella are considered.
- Arrhythmia such as VT, VF, torsades de pointes, bradycardia, long QT interval should be managed.
- Temporary RV pacing is recommended in the presence of AV block and placement of permanent device is not recommended.
- In the presence of bradycardia and long QTc>500 ms, betablocker should be avoided.
- In the presence of left ventricular clot or large portion of akinesia of left ventricle involving apex, anticougulat is recommende.
- Classic treatment of heart failure including ACEI and betablocker should be kept at least three months or untill recovery of regional wall motion abnormality.
- Treatment of underlying disorders such as coronary artery disease is reasonable by continuing asprine and statin.
Surgery
- Surgical intervention is not recommended for the management of COVID-19-associated stress cardiomyopathy.
Primary Prevention
- There are no established measures for the primary prevention of COVID-19-associated stress cardiomyopathy.
- Preventive measures should be taken to avoid COVID-19 infection.
Secondary Prevention
- There are no established measures for the secondary prevention of COVID-19-associated stress cardiomyopathy.
References
- ↑ Roca E, Lombardi C, Campana M, Vivaldi O, Bigni B, Bertozzi B; et al. (2020). "Takotsubo Syndrome Associated with COVID-19". Eur J Case Rep Intern Med. 7 (5): 001665. doi:10.12890/2020_001665. PMC 7213829 Check
|pmc=value (help). PMID 32399453 Check|pmid=value (help). - ↑ 2.0 2.1 Templin C, Ghadri JR, Diekmann J, Napp LC, Bataiosu DR, Jaguszewski M, Cammann VL, Sarcon A, Geyer V, Neumann CA, Seifert B, Hellermann J, Schwyzer M, Eisenhardt K, Jenewein J, Franke J, Katus HA, Burgdorf C, Schunkert H, Moeller C, Thiele H, Bauersachs J, Tschöpe C, Schultheiss HP, Laney CA, Rajan L, Michels G, Pfister R, Ukena C, Böhm M, Erbel R, Cuneo A, Kuck KH, Jacobshagen C, Hasenfuss G, Karakas M, Koenig W, Rottbauer W, Said SM, Braun-Dullaeus RC, Cuculi F, Banning A, Fischer TA, Vasankari T, Airaksinen KE, Fijalkowski M, Rynkiewicz A, Pawlak M, Opolski G, Dworakowski R, MacCarthy P, Kaiser C, Osswald S, Galiuto L, Crea F, Dichtl W, Franz WM, Empen K, Felix SB, Delmas C, Lairez O, Erne P, Bax JJ, Ford I, Ruschitzka F, Prasad A, Lüscher TF (September 2015). "Clinical Features and Outcomes of Takotsubo (Stress) Cardiomyopathy". N Engl J Med. 373 (10): 929–38. doi:10.1056/NEJMoa1406761. PMID 26332547.
- ↑ Tan T, Khoo B, Mills EG, Phylactou M, Patel B, Eng PC, Thurston L, Muzi B, Meeran K, Prevost AT, Comninos AN, Abbara A, Dhillo WS (August 2020). "Association between high serum total cortisol concentrations and mortality from COVID-19". Lancet Diabetes Endocrinol. 8 (8): 659–660. doi:10.1016/S2213-8587(20)30216-3. PMC 7302794 Check
|pmc=value (help). PMID 32563278 Check|pmid=value (help). - ↑ Pasqualetto MC, Secco E, Nizzetto M, Scevola M, Altafini L, Cester A; et al. (2020). "Stress Cardiomyopathy in COVID-19 Disease". Eur J Case Rep Intern Med. 7 (6): 001718. doi:10.12890/2020_001718. PMC 7279910 Check
|pmc=value (help). PMID 32523926 Check|pmid=value (help). - ↑ 5.0 5.1 5.2 5.3 5.4 5.5 Jabri A, Kalra A, Kumar A, Alameh A, Adroja S, Bashir H; et al. (2020). "Incidence of Stress Cardiomyopathy During the Coronavirus Disease 2019 Pandemic". JAMA Netw Open. 3 (7): e2014780. doi:10.1001/jamanetworkopen.2020.14780. PMC 7348683 Check
|pmc=value (help). PMID 32644140 Check|pmid=value (help). - ↑ Hendren NS, Drazner MH, Bozkurt B, Cooper LT (2020). "Description and Proposed Management of the Acute COVID-19 Cardiovascular Syndrome". Circulation. 141 (23): 1903–1914. doi:10.1161/CIRCULATIONAHA.120.047349. PMC 7314493 Check
|pmc=value (help). PMID 32297796 Check|pmid=value (help). - ↑ Beppu M, Terao T, Osawa T, Jentsch F (November 1975). "Photoaffinity labeling of concanavalin A. Preparation of a concanavalin A derivative with reduced valence". J Biochem. 78 (5): 1013–9. doi:10.1093/oxfordjournals.jbchem.a130978. PMID 2589.
- ↑ Singh K, Carson K, Shah R, Sawhney G, Singh B, Parsaik A, Gilutz H, Usmani Z, Horowitz J (April 2014). "Meta-analysis of clinical correlates of acute mortality in takotsubo cardiomyopathy". Am J Cardiol. 113 (8): 1420–8. doi:10.1016/j.amjcard.2014.01.419. PMID 24685327.
- ↑ Sala S, Peretto G, Gramegna M, Palmisano A, Villatore A, Vignale D, De Cobelli F, Tresoldi M, Cappelletti AM, Basso C, Godino C, Esposito A (May 2020). "Acute myocarditis presenting as a reverse Tako-Tsubo syndrome in a patient with SARS-CoV-2 respiratory infection". Eur Heart J. 41 (19): 1861–1862. doi:10.1093/eurheartj/ehaa286. PMC 7184339 Check
|pmc=value (help). PMID 32267502 Check|pmid=value (help). - ↑ Dabbagh MF, Aurora L, D'Souza P, Weinmann AJ, Bhargava P, Basir MB (July 2020). "Cardiac Tamponade Secondary to COVID-19". JACC Case Rep. 2 (9): 1326–1330. doi:10.1016/j.jaccas.2020.04.009. PMC 7177077 Check
|pmc=value (help). PMID 32328588 Check|pmid=value (help). - ↑ 11.0 11.1 Sharma K, Desai HD, Patoliya JV, Jadeja DM, Gadhiya D (January 2021). "Takotsubo Syndrome a Rare Entity in COVID-19: a Systemic Review-Focus on Biomarkers, Imaging, Treatment, and Outcome". SN Compr Clin Med: 1–11. doi:10.1007/s42399-021-00743-4. PMC 7799869 Check
|pmc=value (help). PMID 33458567 Check|pmid=value (help). - ↑ 12.00 12.01 12.02 12.03 12.04 12.05 12.06 12.07 12.08 12.09 12.10 Akashi YJ, Goldstein DS, Barbaro G, Ueyama T (2008). "Takotsubo cardiomyopathy: a new form of acute, reversible heart failure". Circulation. 118 (25): 2754–62. doi:10.1161/CIRCULATIONAHA.108.767012. PMC 4893309. PMID 19106400.
- ↑ 13.0 13.1 13.2 13.3 13.4 13.5 Prasad A, Lerman A, Rihal CS (2008). "Apical ballooning syndrome (Tako-Tsubo or stress cardiomyopathy): a mimic of acute myocardial infarction". Am. Heart J. 155 (3): 408–17. doi:10.1016/j.ahj.2007.11.008. PMID 18294473.
- ↑ 14.0 14.1 14.2 14.3 14.4 14.5 Tsai TT, Nallamothu BK, Prasad A, Saint S, Bates ER (2009). "Clinical problem-solving. A change of heart". N. Engl. J. Med. 361 (10): 1010–6. doi:10.1056/NEJMcps0903023. PMID 19726776.
- ↑ 15.0 15.1 Omerovic E (2011). "How to think about stress-induced cardiomyopathy?--Think "out of the box"!". Scand. Cardiovasc. J. 45 (2): 67–71. doi:10.3109/14017431.2011.565794. PMID 21401402.
- ↑ 16.0 16.1 16.2 16.3 16.4 16.5 16.6 16.7 Brenner ZR, Powers J (2008). "Takotsubo cardiomyopathy". Heart Lung. 37 (1): 1–7. doi:10.1016/j.hrtlng.2006.12.003. PMID 18206521.
- ↑ 17.0 17.1 17.2 17.3 17.4 17.5 17.6 17.7 17.8 Efferth T, Banerjee M, Paul NW (2016). "Broken heart, tako-tsubo or stress cardiomyopathy? Metaphors, meanings and their medical impact". Int. J. Cardiol. doi:10.1016/j.ijcard.2016.12.129. PMID 28041712.
- ↑ 18.0 18.1 18.2 18.3 18.4 18.5 18.6 18.7 Bybee KA, Kara T, Prasad A, Lerman A, Barsness GW, Wright RS, Rihal CS (2004). "Systematic review: transient left ventricular apical ballooning: a syndrome that mimics ST-segment elevation myocardial infarction". Ann. Intern. Med. 141 (11): 858–65. PMID 15583228.
- ↑ 19.0 19.1 Tsuchihashi K, Ueshima K, Uchida T, Oh-mura N, Kimura K, Owa M, Yoshiyama M, Miyazaki S, Haze K, Ogawa H, Honda T, Hase M, Kai R, Morii I (2001). "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 (1): 11–8. PMID 11451258.
- ↑ 20.0 20.1 20.2 20.3 Sharkey SW, Lesser JR, Zenovich AG, Maron MS, Lindberg J, Longe TF, Maron BJ (2005). "Acute and reversible cardiomyopathy provoked by stress in women from the United States". Circulation. 111 (4): 472–9. doi:10.1161/01.CIR.0000153801.51470.EB. PMID 15687136.
- ↑ 21.0 21.1 Desmet WJ, Adriaenssens BF, Dens JA (2003). "Apical ballooning of the left ventricle: first series in white patients". Heart. 89 (9): 1027–31. PMC 1767823. PMID 12923018.
- ↑ Krishnamoorthy P, Garg J, Sharma A, Palaniswamy C, Shah N, Lanier G, Patel NC, Lavie CJ, Ahmad H (2015). "Gender Differences and Predictors of Mortality in Takotsubo Cardiomyopathy: Analysis from the National Inpatient Sample 2009-2010 Database". Cardiology. 132 (2): 131–136. doi:10.1159/000430782. PMID 26159108.
- ↑ 23.0 23.1 Templin C, Ghadri JR, Diekmann J, Napp LC, Bataiosu DR, Jaguszewski M, Cammann VL, Sarcon A, Geyer V, Neumann CA, Seifert B, Hellermann J, Schwyzer M, Eisenhardt K, Jenewein J, Franke J, Katus HA, Burgdorf C, Schunkert H, Moeller C, Thiele H, Bauersachs J, Tschöpe C, Schultheiss HP, Laney CA, Rajan L, Michels G, Pfister R, Ukena C, Böhm M, Erbel R, Cuneo A, Kuck KH, Jacobshagen C, Hasenfuss G, Karakas M, Koenig W, Rottbauer W, Said SM, Braun-Dullaeus RC, Cuculi F, Banning A, Fischer TA, Vasankari T, Airaksinen KE, Fijalkowski M, Rynkiewicz A, Pawlak M, Opolski G, Dworakowski R, MacCarthy P, Kaiser C, Osswald S, Galiuto L, Crea F, Dichtl W, Franz WM, Empen K, Felix SB, Delmas C, Lairez O, Erne P, Bax JJ, Ford I, Ruschitzka F, Prasad A, Lüscher TF (2015). "Clinical Features and Outcomes of Takotsubo (Stress) Cardiomyopathy". N. Engl. J. Med. 373 (10): 929–38. doi:10.1056/NEJMoa1406761. PMID 26332547.
- ↑ Y-Hassan S, Yamasaki K (2013). "History of takotsubo syndrome: is the syndrome really described as a disease entity first in 1990? Some inaccuracies". Int. J. Cardiol. 166 (3): 736–7. doi:10.1016/j.ijcard.2012.09.183. PMID 23073280.
- ↑ Sharkey SW, Lesser JR, Zenovich AG, Maron MS, Lindberg J, Longe TF, Maron BJ (2005). "Acute and reversible cardiomyopathy provoked by stress in women from the United States". Circulation. 111 (4): 472–9. doi:10.1161/01.CIR.0000153801.51470.EB. PMID 15687136.
- ↑ Krishnamoorthy P, Garg J, Sharma A, Palaniswamy C, Shah N, Lanier G, Patel NC, Lavie CJ, Ahmad H (2015). "Gender Differences and Predictors of Mortality in Takotsubo Cardiomyopathy: Analysis from the National Inpatient Sample 2009-2010 Database". Cardiology. 132 (2): 131–136. doi:10.1159/000430782. PMID 26159108.
- ↑ Paul NS, Roberts H, Butany J, Chung T, Gold W, Mehta S, Konen E, Rao A, Provost Y, Hong HH, Zelovitsky L, Weisbrod GL (2004). "Radiologic pattern of disease in patients with severe acute respiratory syndrome: the Toronto experience". Radiographics. 24 (2): 553–63. doi:10.1148/rg.242035193. PMID 15026600.
- ↑ Ajlan AM, Ahyad RA, Jamjoom LG, Alharthy A, Madani TA (October 2014). "Middle East respiratory syndrome coronavirus (MERS-CoV) infection: chest CT findings". AJR Am J Roentgenol. 203 (4): 782–7. doi:10.2214/AJR.14.13021. PMID 24918624.
- ↑ Chen, Nanshan; Zhou, Min; Dong, Xuan; Qu, Jieming; Gong, Fengyun; Han, Yang; Qiu, Yang; Wang, Jingli; Liu, Ying; Wei, Yuan; Xia, Jia'an; Yu, Ting; Zhang, Xinxin; Zhang, Li (2020). "Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study". The Lancet. doi:10.1016/S0140-6736(20)30211-7. ISSN 0140-6736.
- ↑ Haghi D, Fluechter S, Suselbeck T, Kaden JJ, Borggrefe M, Papavassiliu T (2007). "Cardiovascular magnetic resonance findings in typical versus atypical forms of the acute apical ballooning syndrome (Takotsubo cardiomyopathy)". Int. J. Cardiol. 120 (2): 205–11. doi:10.1016/j.ijcard.2006.09.019. PMID 17175045.
- ↑ 31.0 31.1 Mitchell JH, Hadden TB, Wilson JM, Achari A, Muthupillai R, Flamm SD (2007). "Clinical features and usefulness of cardiac magnetic resonance imaging in assessing myocardial viability and prognosis in Takotsubo cardiomyopathy (transient left ventricular apical ballooning syndrome)". Am. J. Cardiol. 100 (2): 296–301. doi:10.1016/j.amjcard.2007.02.091. PMID 17631086.
- ↑ Deetjen AG, Conradi G, Mollmann S, Rad A, Hamm CW, Dill T (2006). "Value of gadolinium-enhanced magnetic resonance imaging in patients with Tako-Tsubo-like left ventricular dysfunction". J Cardiovasc Magn Reson. 8 (2): 367–72. PMID 16669180.
- ↑ Abe Y, Kondo M, Matsuoka R, Araki M, Dohyama K, Tanio H (2003). "Assessment of clinical features in transient left ventricular apical ballooning". J. Am. Coll. Cardiol. 41 (5): 737–42. PMID 12628715.
- ↑ Dec GW (2005). "Recognition of the apical ballooning syndrome in the United States". Circulation. 111 (4): 388–90. doi:10.1161/01.CIR.0000155234.69439.E4. PMID 15687123.
- ↑ Handy AD, Prasad A, Olson TM (2009). "Investigating genetic variation of adrenergic receptors in familial stress cardiomyopathy (apical ballooning syndrome)". J Cardiol. 54 (3): 516–7. doi:10.1016/j.jjcc.2009.08.008. PMID 19944334.
- ↑ Eitel I, von Knobelsdorff-Brenkenhoff F, Bernhardt P, Carbone I, Muellerleile K, Aldrovandi A, Francone M, Desch S, Gutberlet M, Strohm O, Schuler G, Schulz-Menger J, Thiele H, Friedrich MG (2011). "Clinical characteristics and cardiovascular magnetic resonance findings in stress (takotsubo) cardiomyopathy". JAMA. 306 (3): 277–86. doi:10.1001/jama.2011.992. PMID 21771988.
- ↑ Eitel I, Behrendt F, Schindler K, Kivelitz D, Gutberlet M, Schuler G, Thiele H (2008). "Differential diagnosis of suspected apical ballooning syndrome using contrast-enhanced magnetic resonance imaging". Eur. Heart J. 29 (21): 2651–9. doi:10.1093/eurheartj/ehn433. PMID 18820322.
- ↑ Testa M, Feola M (2014). "Usefulness of myocardial positron emission tomography/nuclear imaging in Takotsubo cardiomyopathy". World J Radiol. 6 (7): 502–6. doi:10.4329/wjr.v6.i7.502. PMC 4109102. PMID 25071891.