|
 
 |
| REVIEW ARTICLE |
|
| Year : 2017 | Volume
: 1
| Issue : 4 | Page : 123-128 |
|
Takotsubo syndrome and heart transplantation: A reciprocate liaison?
Alfredo De Giorgi1, Fabio Fabbian2, Matteo Guarino2, Michele Domenico Spampinato2, Benedetta Boari1, Rosaria Cappadona2, Beatrice Zucchi2, Roberto De Giorgio2, Roberto Manfredini2
1 Department of Medicine, General Hospital of Ferrara, Ferrara, Italy
2 Department of Medical Sciences, Faculty of Medicine, Surgery and Prevention, University of Ferrara, Ferrara, Italy
| Date of Web Publication | 29-Oct-2018 |
Correspondence Address:
Dr. Alfredo De Giorgi
Department of Medicine, General Hospital of Ferrara, Via A. Moro 8, 44123 Cona (Ferrara)
Italy
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/hm.hm_8_18
Takotsubo syndrome (TTS) is a clinical syndrome characterized by transient left ventricular dysfunction, ischemic electrocardiographic changes, and minimal release of myocardial enzymes without obstructive coronary artery disease. This syndrome that mimics an acute myocardial infarction is prevalent among female patients and is regarded as a benign medical condition. The precise pathophysiological mechanism of TTS is complex and not completely understood, but specific emotional or physical events precipitate this syndrome that represents a typical condition characterized by interactions between cardiovascular and neuropsychological diseases. In addition, many different neurological disorders, such as stroke, subarachnoid bleeding, head injury, epilepsy, and bacterial meningitis, have directly or indirectly related to TTS; unfortunately, these acute neurological diseases represented the cause of death in patients nominated for organ donation and in particular for the heart donor. This article reviews the relationship between TTS and solid organ transplantation; in particular, this article highlights the possible mechanisms underlying the induction of TTS in pre- and post-transplantation phases and in heart-transplant patients. Keywords: Heart transplantation, reciprocate liaison, Takotsubo syndrome
How to cite this article:
De Giorgi A, Fabbian F, Guarino M, Spampinato MD, Boari B, Cappadona R, Zucchi B, De Giorgio R, Manfredini R. Takotsubo syndrome and heart transplantation: A reciprocate liaison?. Heart Mind 2017;1:123-8 |
How to cite this URL:
De Giorgi A, Fabbian F, Guarino M, Spampinato MD, Boari B, Cappadona R, Zucchi B, De Giorgio R, Manfredini R. Takotsubo syndrome and heart transplantation: A reciprocate liaison?. Heart Mind [serial online] 2017 [cited 2023 Jun 6];1:123-8. Available from: http://www.heartmindjournal.org/text.asp?2017/1/4/123/244376 |
| Introduction | |  |
Takotsubo syndrome (TTS), also defined as “stress-induced cardiomyopathy,” “broken heart syndrome,” or “transient left apical ballooning syndrome,” was first described by Dote et al. in the early 1990s.[1] TTS is a clinical syndrome mimicking an acute myocardial infarction and characterized by transient left ventricular dysfunction, ischemic electrocardiographic changes, and minimal release of myocardial enzymes without obstructive coronary artery disease.[2] This syndrome is poorly recognized and, even if it was initially regarded as a benign condition, it has been associated with severe clinical complications,[3] and outcome may be determined by risk factors, comorbidities, clinical presentation, and in-hospital or out-of-hospital occurrence.[4] Moreover, similarly with other acute cardiovascular events, it has shown that time of onset may exhibit a temporal preference.[3],[4],[5]
It is estimated to represent approximately 1%–3% of all and 5%–6% of female patients presenting with suspected ST-elevation myocardial infarction[6],[7] and represent about 1%–3% of all suspected cases of myocardial infarction; prevalence in female patients is higher. According to the available literature, about 90% of TTS patients are women with a mean age of 67–70 years, and around 80% are older than 50 years.[8],[9] Moreover, although TTS occurs mostly in women, male gender represents an independent predictor of adverse outcome.[4]
It is possible that the higher risk in postmenopausal women is related to the protective myocardial effects of estrogen-influencing vasomotor tone through endothelial nitric oxide synthesis, attenuating catecholamine-mediated vasoconstriction, and decreasing the sympathetic response to mental stress. Moreover, in women with acute subarachnoid hemorrhage, low levels of estradiol have been associated with an increased risk of ventricular wall motion abnormalities.[10]
TTS represents a typical condition characterized by interactions between cardiovascular and neuropsychological diseases, representing a new branch called “psycho-cardiology.”[11],[12] This clinical relationship, due to the high sensitivity of the autonomic nervous system, may be related to nervous system dysregulation, endothelial dysfunction, microcirculation dysfunction, and neurohormonal alterations,[13] which represents the basis of functional alterations leading to TTS.
Many theories for pathophysiological mechanisms of TTS have been described, such as transient coronary artery spasm, microvascular dysfunction, and aborted myocardial and catecholamine activation with direct myocardial injury. However, the precise pathophysiological mechanisms of TTS are complex and not completely understood; however, specific emotional or physical events precipitate the syndrome in many cases. The exact mechanism by which catecholamine excess, related to neurological stress, induces myocardial damage with regional ballooning patterns is unknown. Several hypotheses have been proposed such as the microcirculation dysfunction due to vasoconstrictor effects of catecholamines and endothelins in the coronary microvasculature that have a high density of α1-receptors and type A endothelin receptors.[14] These substances induce a reduction of microvascular blood flow leading to TTS. Furthermore, a direct effect of catecholamines on cardiomyocytes should be clarified; in fact, high levels of catecholamine, due to pheochromocytoma or subarachnoid hemorrhage, were related to myocyte damage with hypercontracted sarcomeres, eosinophilic infiltration, and interstitial mononuclear inflammation.[15] Moreover, catecholamine excess response is different depending on the density of the β-adrenergic receptors which is higher in the apex; these receptors were more sensitive to high levels of catecholamines with a reduction not only of coronary blood flow, but also with a negative inotropic effects and local inflammation, due to the production of nitric oxide that is potentially responsible for the extension of the initial myocardial lesion.[16]
Recently, the diagnostic criteria have been reviewed.[17] Compared to the previous Mayo Clinic criteria,[18] novel features have been added, including laboratory data (significant elevation of brain natriuretic peptide), gender (higher incidence in postmenopausal women), and trigger, where neurological disorders (e.g., subarachnoid hemorrhage, stroke/transient ischemic attack, or seizures) as well as pheochromocytoma may serve as triggers for TTS. Many medical conditions have been associated with TTS, i.e., infectious diseases,[19] respiratory diseases,[20] endocrine disorders,[21] allergic diseases,[22] sepsis,[23] and even suicidal behavior.[24] Furthermore, many different neurological disorders have directly or indirectly related to heart diseases with a condition defined as brain–heart disorders; the most well-known of these neurological disorders are stroke, subarachnoid bleeding, head injury, epilepsy, and bacterial meningitis.[25]
Many of these acute neurological diseases, such as stroke, subarachnoid bleeding, and head injury, represented the cause of death in patients nominated for organ donation and in particular for the heart donor; interestingly, among deceased organ donors, only 28% of hearts are recovered for transplantation because many potential donor hearts are refused due to systolic dysfunction.[26] This systolic dysfunction would seem to be related to the increasing serum levels of catecholamines which represent the link between acute brain injury and heart dysfunctions, including TTS. A structural brain damage due to cerebral bleeding, stroke, or transient ischemic attack, and subsequent increase of intracranial pressure induces an elevation in tissue and plasma of catecholamine levels; it has been reported that, within the first 48 h during subarachnoid hemorrhage, total body norepinephrine level increases by three folds. These levels that can still remain high for 1 week are responsible for myocyte calcium overload and cell death, causing cardiac dysfunction.[27] Furthermore, the acute brain injury may be related to dysfunction of the insular cortex that plays a crucial role in the autonomic nervous system function, inducing augmentation of sympathetic tone; this damage has been associated with electrocardiographic (ECG) changes, arrhythmias, and impaired cardiac wall motion,[28] promoting the development of TTS and increasing the risk of mortality at 3 months.
Treatment of choice for patients with end-stage solid organ damage is organ transplantation which is actually considered as the last resort therapy. However, different clinical complications mainly due to the recipient-mediated acute or chronic immune response need to be managed by transplant physicians in their everyday clinical work. Solid organ rejection is avoided by nonspecific suppression of host immune system, but lifelong immunosuppression is causing significant side effects such as infections, malignancies, chronic kidney disease, diabetes, and cardiovascular disease. Complications could be even more relevant in patients with a longer length of time with transplanted organ due to longer period of immunosuppressive treatment.[29] In 2017, the 50th anniversary of the first human heart transplant carried out by the South African surgeon, Christiaan (“Chris”) Barnard, was celebrated,[30] and, since then, the number of heart-transplanted patients has been increasing. In 2017, the International Society for Heart and Lung Transplantation Registry published the 34th heart transplant report on 135,387 heart transplants in recipients of all ages, including 120,991 adult heart transplants. Median survival was 10.7 years in adults and 16.1 years in pediatric recipients; however, adult recipient unadjusted survival was reported to improve over time.[31]
TTS is considered a benign disease due to a transient myocardial damage; however, if TTS is a reversible condition, hemodynamic and electrical instability during the acute phase exposes patients to the risk of serious adverse in-hospital events occurring in approximately one-fifth of TTS patients.[8] Conditions related to adverse in-hospital outcome include acute neurologic or psychiatric diseases, high troponin values, and admission systolic left dysfunction (left ventricular ejection fraction <45%). Females older than 55 years have a five-fold greater risk of TTS compared to women younger than 55 years and a 10-fold greater risk than men.[8] Furthermore, Sobue et al.[32] showed that male (hazard ratio [HR] 11.9) and physical trigger (HR 14.7) were related with in-hospital mortality in TTS patients. A Japanese study showed that both white blood cell count (odds ratio [OR] 2.52) and brain natriuretic peptide levels (OR 4.92) were independent predictors of in-hospital adverse cardiac complications.[33] No data were reported on long-term survival in TTS patients, probably it is similar to patients with acute myocardial infarction.[34]
| Takotsubo Syndrome Preheart Transplantation | | |
Acute brain injury is the most common cause of death in potential heart-transplant donors, but systolic heart dysfunction was present in about one-third of patients with major cerebral events, probably due to the production of catecholamines consequently to subarachnoid hemorrhage and brain death.[35] Pérez López et al.[36] reported that brain death induced hemodynamic and neuroendocrine alterations with increasing plasma levels of epinephrine, norepinephrine, and dopamine. Epinephrine and dopamine have a rapid release patterns after cerebral events, while norepinephrine peak happens 1 h later after an acute brain stress; the activation of hypothalamic-pituitary-adrenocortical and sympatho-adrenomedullary axes induces a neuroendocrine change with the increasing epinephrine and norepinephrine serum levels; these cerebral reactions to acute events are due to the activation of the right insular cortex and then augmentation of sympathetic tone.[37] Excessive catecholamine plasma levels and sympathetic stimulation could induce prolonged sarcomere contraction, resulting in a pathologic subendocardial pattern of necrosis.
After acute brain events, the following cardiac complications have been reported: ECG abnormalities, including prolonged QTc, T-wave, ST-segment abnormalities, elevated cardiac enzymes, and ECG ventricular dysfunction, such as hypokinesis of the ventricular apex,[38] and they appear to be similar to those reported in patients with TTS.
Therefore, both TTS and acute cerebral accident appear to share the same mechanism, sympathetic reflex activation and increase in serum catecholamine levels. Many authors suggest that if cardiac dysfunctions are detected at the time of initial heart donor evaluation, serial imaging assessment should be undertaken in order to precisely diagnose cardiac dysfunction; indeed, in a single clinical case reported by Redfors et al.,[39] a 34-year-old man received the heart transplant from a 50-year-old man donor with subarachnoid hemorrhage and subsequent TTS event. The transplanted heart, after 1-month posttransplantation, presented normal left ventricular function and absence of ECG signs of regional dysfunctions. Subsequently, Ravi et al.[40] reported a 61-year-old man who received a heart transplant from a 17-year-old girl suffering acute TTS consequently by a motor vehicle accident. No complications were reported during a 46-month follow-up period.
Change of cardiac transplantation indications could increase the quality of life of organ donor up to 25%, with a significant impact on the quality of life of many patients awaiting cardiac transplantation.[41]
| Takotsubo Syndrome Postsolid Organ Transplantation | | |
Similar neurological stress conditions present in patients with acute brain events may develop in patients after solid organ transplantation. We systematically explored case reports published in PubMed database, by using the following search keywords: “takotsubo cardiomyopathy” or “takotsubo syndrome” or “stress-induced cardiomyopathy” in combination with “transplantation.” For each case, we collected sex, age, type of transplanted organ, minutes or hours after operation, and outcome. The deadline for electronic search was May 31, 2018. Out of 3,742 articles, we selected 17 items relating TTS in solid organ transplantation, reporting 19 cases [Figure 1]. All these case reports are summarized in [Table 1]. The majority of patients were women (57.8%) with a median age of 54.7±9.8 (range 46 – 68) years. The outcome was unfavorable in one only patient. Time of TTS diagnosis was variable the onset could be very early, a few minutes or hours after operation, up to several days after operation; in one case, the acute myocardial event took place after many years. The mechanism responsible for TTS was ascribed to different causes; in peri-operative accidents the main cause could be anesthesia, in the later one immunosuppressive therapy. | Table 1: Review of available evidence on cases of solid organ transplantation complicated by onset of Takotsubo syndrome
Click here to view |
During the perioperative period, acute events could be related to tracheal intubation, induction of anesthesia with sympathetic reflex stimulation, anaphylaxis, and infusion of adrenergic drugs. Other cases of TTS were related to uncontrolled pain;[59],[60] however, TTS was due to increasing serum levels of catecholamines.
Gołębiewska et al.[43] reported that immunosuppressive therapy may be related to cardiotoxicity of renal calcineurin inhibitors which can induce direct damage of myocardium. Calcineurin inhibitors, in fact, were related to coronary epicardial endothelial dysfunction, impacting vasomotor function and progression of coronary microangiopathy negatively.[61] These microvascular cardiac modifications can partly explain the susceptibility to the development of TTS in transplanted patients, although the precise mechanisms have not yet been highlighted. Furthermore, optimal management of TTS in transplant recipients remains unclear; actual strategies include pharmacological treatment with beta-blockers, angiotensin-converting enzyme inhibitors, and diuretics,[62] aiming at reducing cardiovascular effects of catecholamines and myocardial remodeling.
Finally, we should underline that TTS should be differentiated from cardiac allograft vasculopathy (CAV). CAV is due to a diffuse immune-mediated pan-arteritis with concentric, longitudinal intimal thickening of the coronary arteries, representing a major cause of long-term morbidity and mortality after transplantation. Its incidence ranges from 42% at 5 years to 50% at 10 years, it has not significantly reduced and it occurs 1 year after transplantation, and it could appear also in an accelerated form of disease being more aggressive and associated with a worse prognosis. History of rejection, older age of the donor, the presence of donor-specific anti-HLA antibodies, ischemia-reperfusion injury, and traditional risk factors for coronary atherosclerosis are considered risk factors for CAV. Symptomatic CAV may present with dyspnea, angina pain, left ventricular dysfunction, restrictive physiology, or even sudden cardiac death could be symptoms due to CAV; however, the condition could remain asymptomatic due to denervation of the donor heart. Coronary angiography is the gold standard for diagnosis of CAV and when diagnosed it is associated with a poor prognosis. Prevention is an important strategy and re-transplantation is the definitive solution.[63]
| Is There Greater Risk of Takotsubo Syndrome in Transplanted Heart? | | |
Our review identified only two cases of TTS in heart-transplant recipients with two important clinical differences represented by the time of occurrence and the cause of the acute events. Gastwirth et al.[57] reported a TTS event in 55-year-old woman during dobutamine stress ECG 1 year after transplantation; instead, Behnes et al.[58] reported a 64-year-old hospitalized male without a definite cause of TTS. One of the mechanisms of TTS development in heart-transplant recipients was supposed to be the loss of inhibitory parasympathetic innervation of transplanted hearts, inducing more susceptibility to develop the action of catecholamines. Innervation of transplanted heart is a matter of debate; complete allograft denervation described soon after the operation is subsequently followed by re-innervation. In 1997, Uberfuhr et al.[64] reported sympathetic and parasympathetic re-innervations using spectral analysis of heart rate variability in 13 patients after 28 months' postheart transplantation. Similar data were reported by Cornelissen et al.[65] in 14 patients aged 59 years 10 years after transplantation. Partial autonomic re-innervation was confirmed with metaiodobenzylguanidine cardiac scintigraphy by Buendia-Fuentes et al.[66] reporting that sympathetic re-innervation occurred in 45 cardiac transplant recipients (32 males) 1 year after heart transplantation. On the other hand, autonomic cardiac re-innervation does not appear to be an additional cardiovascular risk as reported by Olmetti et al.[67] in solid organ transplantation.
| Conclusions | | |
The interaction between heart and brain is still an open matter and far to be quite disclosed due to high complexity. On the one hand, in most cases of deaths in the first 30 days after cardiac transplantation, the cause a failure of the donor heart, with a significant reduction in contractility and loss of contractile reserve before and soon after transplantation. Brain death in the donor, secondary to a “catecholamine storm,” and a rapidly rising intracranial pressure were hypothesized mechanisms. Just several years ago, the existence of at least three common features between stress cardiomyopathy and the heart of a brain-dead donor was observed as follows: (i) exposure to unusually high catecholamine levels, (ii) ventricular dysfunction, and (iii) prompt recovery.[68] On the other hand, cardiac transplantation is always limited by a paucity of donors, and acute brain injury is the most common cause of death in potential heart-transplant donors. Unfortunately, a left ventricle dysfunction is a well-reported abnormality in these patients.[69] Moreover, the mind is not strictly only anatomic brain. Psychiatric disorders are one of the most common comorbidities in TTS, and data from the InterTAK registry reported that approximately one-third of TTS patients had a chronic psychiatric disorder including affective, anxiety, and adjustment disorders.[8] Thus, TTS represents an ideal, although extremely complex, laboratory for studies on the mysterious and intriguing relationship between heart and mind.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | 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 1991;21:203-14.  |
| 2. | Bossone E, Savarese G, Ferrara F, Citro R, Mosca S, Musella F, et al. Takotsubo cardiomyopathy: Overview. Heart Fail Clin 2013;9:249-66, x. |
| 3. | Ghadri JR, Wittstein IS, Prasad A, Sharkey S, Dote K, Akashi YJ, et al. International expert consensus document on takotsubo syndrome (Part I): Clinical characteristics, diagnostic criteria, and pathophysiology. Eur Heart J 2018;39:2032-46. |
| 4. | Kato S, Gili S, Fabbian F, Manfredini R. Co-morbidities in takotsubo syndrome. In: Camm J, Luscher TF, Maurer G, Serruys PW, editors. Takotsubo Syndrome, ESC Textbook of Cardiovascular Medicine. 3 rd ed. 2018. DOI: 10.1093/med/9780198784906.001.0001. |
| 5. | Manfredini R, Manfredini F, Fabbian F, Salmi R, Gallerani M, Bossone E, et al. Chronobiology of takotsubo syndrome and myocardial infarction: Analogies and differences. Heart Fail Clin 2016;12:531-42. |
| 6. | Prasad A, Dangas G, Srinivasan M, Yu J, Gersh BJ, Mehran R, et al. Incidence and angiographic characteristics of patients with apical ballooning syndrome (takotsubo/stress cardiomyopathy) in the HORIZONS-AMI trial: An analysis from a multicenter, international study of ST-elevation myocardial infarction. Catheter Cardiovasc Interv 2014;83:343-8. |
| 7. | Bybee KA, Prasad A, Barsness GW, Lerman A, Jaffe AS, Murphy JG, et al. Clinical characteristics and thrombolysis in myocardial infarction frame counts in women with transient left ventricular apical ballooning syndrome. Am J Cardiol 2004;94:343-6. |
| 8. | 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. |
| 9. | Schneider B, Athanasiadis A, Stöllberger C, Pistner W, Schwab J, Gottwald U, et al. Gender differences in the manifestation of takotsubo cardiomyopathy. Int J Cardiol 2013;166:584-8. |
| 10. | Sugimoto K, Inamasu J, Hirose Y, Kato Y, Ito K, Iwase M, et al. The role of norepinephrine and estradiol in the pathogenesis of cardiac wall motion abnormality associated with subarachnoid hemorrhage. Stroke 2012;43:1897-903. |
| 11. | Yin H, Geng Q. Advances in discovering the interrelationship between mental disorders and heart diseases. Heart Mind 2017;1:71-7. [Full text] |
| 12. | Ma H, Liu G, Guo L, Geng Q. The link between brain and heart in mental stress-induced myocardial ischemia. Heart Mind 2017;1:93-6. [Full text] |
| 13. | Jiang W. Neuropsychocardiology – Evolution and advancement of the heart-mind field. Heart Mind 2017;1:59-64. [Full text] |
| 14. | Jaguszewski M, Osipova J, Ghadri JR, Napp LC, Widera C, Franke J, et al. Asignature of circulating microRNAs differentiates takotsubo cardiomyopathy from acute myocardial infarction. Eur Heart J 2014;35:999-1006. |
| 15. | Wittstein IS. Stress cardiomyopathy: A syndrome of catecholamine-mediated myocardial stunning? Cell Mol Neurobiol 2012;32:847-57. |
| 16. | Nguyen TH, Neil CJ, Sverdlov AL, Ngo DT, Chan WP, Heresztyn T, et al. Enhanced NO signaling in patients with takotsubo cardiomyopathy: Short-term pain, long-term gain? Cardiovasc Drugs Ther 2013;27:541-7. |
| 17. | Ghadri JR, Wittstein IS, Prasad A, Sharkey S, Dote K, Akashi YJ, et al. International expert consensus document on takotsubo syndrome (Part II): Diagnostic workup, outcome, and management. Eur Heart J 2018;39:2047-62. |
| 18. | Prasad A, Lerman A, Rihal CS. Apical ballooning syndrome (Takotsubo or stress cardiomyopathy): A mimic of acute myocardial infarction. Am Heart J 2008;155:408-17. |
| 19. | De Giorgi A, Fabbian F, Pala M, Parisi C, Misurati E, Molino C, et al. Takotsubo cardiomyopathy and acute infectious diseases: A mini-review of case reports. Angiology 2015;66:257-61. |
| 20. | Manfredini R, Fabbian F, Giorgi AD, Pala M, Menegatti AM, Parisi C, et al. Heart and lung, a dangerous liaison-takotsubo cardiomyopathy and respiratory diseases: A systematic review. World J Cardiol 2014;6:338-44. |
| 21. | De Giorgi A, Fabbian F, Tiseo R, Parisi C, Misurati E, Molino C, et al. Takotsubo cardiomyopathy and endocrine disorders: A mini-review of case reports. Am J Emerg Med 2014;32:1413-7. |
| 22. | Boccafogli A, De Giorgi A, Parisi C, Tiseo R, Misurati E, Molino C, et al. May allergic syndrome represent valid trigger for Takotsubo cardiomyopathy? A systematic review of reported cases. Exp Clin Cardiol 2014;20:5074-87. |
| 23. | Fabbian F, De Giorgi A, Tiseo R, Boari B, Salmi R, Signani F, et al. Takotsubo cardiomyopathy, sepsis and clinical outcome: Does gender matter? Am J Emerg Med 2015;33:1525-7. |
| 24. | Manfredini R, Fabbian F, Cappadona R, Zucchi B, Lopez-Soto PJ, Rodriguez-Borrego MA, et al. Attempted suicide as a trigger of takotsubo syndrome: A minireview of available case reports. Intern Emerg Med 2018;13:629-31. |
| 25. | Finsterer J, Wahbi K. CNS-disease affecting the heart: Brain-heart disorders. J Neurol Sci 2014;345:8-14. |
| 26. | Zaroff JG, Babcock WD, Shiboski SC. The impact of left ventricular dysfunction on cardiac donor transplant rates. J Heart Lung Transplant 2003;22:334-7. |
| 27. | Naredi S, Lambert G, Edén E, Zäll S, Runnerstam M, Rydenhag B, et al. Increased sympathetic nervous activity in patients with nontraumatic subarachnoid hemorrhage. Stroke 2000;31:901-6. |
| 28. | Cho HJ, Kim HY, Han SH, Kim HJ, Moon YS, Oh J, et al. Takotsubo cardiomyopathy following cerebral infarction involving the insular cortex. J Clin Neurol 2010;6:152-5. |
| 29. | Saidi RF, Hejazii Kenari SK. Clinical transplantation and tolerance: Are we there yet? Int J Organ Transplant Med 2014;5:137-45. |
| 30. | Cooper DK. Christiaan Barnard-the surgeon who dared: The story of the first human-to-human heart transplant. Glob Cardiol Sci Pract 2018;2018:11. |
| 31. | Lund LH, Khush KK, Cherikh WS, Goldfarb S, Kucheryavaya AY, Levvey BJ, et al. The registry of the International Society for Heart and Lung Transplantation: Thirty-fourth adult heart transplantation report-2017; focus theme: Allograft ischemic time. J Heart Lung Transplant 2017;36:1037-46. |
| 32. | Sobue Y, Watanabe E, Ichikawa T, Koshikawa M, Yamamoto M, Harada M, et al. Physically triggered takotsubo cardiomyopathy has a higher in-hospital mortality rate. Int J Cardiol 2017;235:87-93. |
| 33. | Murakami T, Yoshikawa T, Maekawa Y, Ueda T, Isogai T, Konishi Y, et al. Characterization of predictors of in-hospital cardiac complications of takotsubo cardiomyopathy: Multi-center registry from Tokyo CCU network. J Cardiol 2014;63:269-73. |
| 34. | Tornvall P, Collste O, Ehrenborg E, Järnbert-Petterson H. A case-control study of risk markers and mortality in takotsubo stress cardiomyopathy. J Am Coll Cardiol 2016;67:1931-6. |
| 35. | Banki NM, Kopelnik A, Dae MW, Miss J, Tung P, Lawton MT, et al. Acute neurocardiogenic injury after subarachnoid hemorrhage. Circulation 2005;112:3314-9. |
| 36. | Pérez López S, Otero Hernández J, Vázquez Moreno N, Escudero Augusto D, Alvarez Menéndez F, Astudillo González A, et al. Brain death effects on catecholamine levels and subsequent cardiac damage assessed in organ donors. J Heart Lung Transplant 2009;28:815-20. |
| 37. | Steptoe A, Kivimäki M. Stress and cardiovascular disease. Nat Rev Cardiol 2012;9:360-70. |
| 38. | Hravnak M, Frangiskakis JM, Crago EA, Chang Y, Tanabe M, Gorcsan J 3 rd, et al. Elevated cardiac troponin I and relationship to persistence of electrocardiographic and echocardiographic abnormalities after aneurysmal subarachnoid hemorrhage. Stroke 2009;40:3478-84. |
| 39. | Redfors B, Råmunddal T, Oras J, Karason K, Ricksten SE, Dellgren G, et al. Successful heart transplantation from a donor with takotsubo syndrome. Int J Cardiol 2015;195:82-4. |
| 40. | Ravi Y, Campagna R, Rosas PC, Essa E, Hasan AK, Higgins RS, et al. Successful heart transplantation using a donor heart afflicted by takotsubo cardiomyopathy. Proc (Bayl Univ Med Cent) 2016;29:73-4. |
| 41. | Boudaa C, Lalot JM, Perrier JF, Voltz C, Strub P, Claudon O, et al. Evaluation of donor cardiac function for heart transplantation: Experience of a French academic hospital. Ann Transplant 2000;5:51-3. |
| 42. | Chrapko BE, Tomaszewski A, Jaroszyński AJ, Furmaga J, Wysokiński A, Rudzki S, et al. Takotsubo syndrome in a patient after renal transplantation. Med Sci Monit 2012;18:CS26-30. |
| 43. | Gołębiewska J, Stopczyńska I, Dębska-Ślizień A, Bohdan M, Gruchała M, Rutkowski B, et al. Tako-tsubo cardiomyopathy on the first day after renal transplantation – Case report and literature review. Transplant Proc 2014;46:2920-2. |
| 44. | Vailas MG, Vernadakis S, Kakavia K, Paizis I, Bokos J, Boletis J, et al. Aheartbreaking renal transplantation: Is norepinephrine the culprit to blame? Transplant Proc 2016;48:3088-91. |
| 45. | Lee HR, Hurst RT, Vargas HE. Transient left ventricular apical ballooning syndrome (Takotsubo cardiomyopathy) following orthotopic liver transplantation. Liver Transpl 2007;13:1343-5. |
| 46. | Tiwari AK, D'Attellis N. Intraoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy during orthotopic liver transplantation. J Cardiothorac Vasc Anesth 2008;22:442-5. |
| 47. | Saner FH, Plicht B, Treckmann J, Mathe Z, Sotiropoulos GC, Radtke A, et al. Tako-tsubo syndrome as a rare cause of cardiac failure in liver transplantation. Liver Int 2010;30:159-60. |
| 48. | Phillips MS, Pruett TL, Berg CL, Hagspiel KD, Sawyer RG, Bonatti HJ, et al. Takotsubo cardiomyopathy in a liver transplant recipient: A diagnosis of exclusion? J Cardiothorac Vasc Anesth 2009;23:268-9. |
| 49. | Eagle SS, Thompson A, Fong PP, Pretorius M, Deegan RJ, Hairr JW, et al. Takotsubo cardiomyopathy and coronary vasospasm during orthotopic liver transplantation: Separate entities or common mechanism? J Cardiothorac Vasc Anesth 2010;24:629-32. |
| 50. | Anders MM, Comignani PD, Couce R, Prini N, Zerega AR, Santopinto M, et al. Takotsubo cardiomyopathy: A cardiac syndrome mimicking acute myocardial infarction in a liver transplant recipient. Cardiol Res 2011;2:82-5. |
| 51. | Tachotti Pires LJ, Cardoso Curiati MN, Vissoci Reiche F, Silvestre OM, Mangini S, Carballo Afonso R, et al. Stress-induced cardiomyopathy (takotsubo cardiomyopathy) after liver transplantation-report of two cases. Transplant Proc 2012;44:2497-500. |
| 52. | Bedanova H, Orban M, Nemec P. Postoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy following orthotopic liver transplantation. Am J Case Rep 2013;14:494-7. |
| 53. | Harika R, Bermas K, Hughes C, Al-Khafaji A, Iyer M, Wallace DJ, et al. Cardiac arrest after liver transplantation in a patient with takotsubo cardiomyopathy. Br J Anaesth 2014;112:594-5. |
| 54. | Vachiat A, McCutcheon K, Mahomed A, Schleicher G, Brand L, Botha J, et al. Takotsubo cardiomyopathy post liver transplantation. Cardiovasc J Afr 2016;27:e1-e3. |
| 55. | Michel-Cherqui M, Felten ML, Liu N, Sage E, Devaquet J, Grenet D, et al. Management of takotsubo cardiomyopathy in a lung transplant recipient. Transplantation 2010;90:692-4. |
| 56. | Ghadri JR, Bataisou RD, Diekmann J, Lüscher TF, Templin C. First case of atypical takotsubo cardiomyopathy in a bilateral lung-transplanted patient due to acute respiratory failure. Eur Heart J Acute Cardiovasc Care 2015;4:482-5. |
| 57. | Gastwirth VG, Yang HS, Steidley DE, Scott RL, Chandrasekaran K. Dobutamine stress-induced cardiomyopathy in an orthotopic heart transplant patient. J Heart Lung Transplant 2009;28:968-70. |
| 58. | Behnes M, Baumann S, Borggrefe M, Haghi D. Biventricular takotsubo cardiomyopathy in a heart transplant recipient. Circulation 2013;128:e62-3. |
| 59. | Goonewardene M, Aziz S. Takotsubo cardiomyopathy during elective general anaesthetic induction. BMJ Case Rep 2012;2012. pii: bcr2012006373. |
| 60. | Jabaudon M, Bonnin M, Bolandard F, Chanseaume S, Dauphin C, Bazin JE, et al. Takotsubo syndrome during induction of general anaesthesia. Anaesthesia 2007;62:519-23. |
| 61. | Keogh A. Calcineurin inhibitors in heart transplantation. J Heart Lung Transplant 2004;23:S202-6. |
| 62. | Akashi YJ, Goldstein DS, Barbaro G, Ueyama T. Takotsubo cardiomyopathy: A new form of acute, reversible heart failure. Circulation 2008;118:2754-62. |
| 63. | Kim IC, Youn JC, Kobashigawa JA. The past, present and future of heart transplantation. Korean Circ J 2018;48:565-90. |
| 64. | Uberfuhr P, Frey AW, Fuchs A, Paniara C, Roskamm H, Schwaiger M, et al. Signs of vagal reinnervation 4 years after heart transplantation in spectra of heart rate variability. Eur J Cardiothorac Surg 1997;12:907-12. |
| 65. | Cornelissen VA, Vanhaecke J, Aubert AE, Fagard RH. Heart rate variability after heart transplantation: A 10-year longitudinal follow-up study. J Cardiol 2012;59:220-4. |
| 66. | Buendia-Fuentes F, Almenar L, Ruiz C, Vercher JL, Sánchez-Lázaro I, Martínez-Dolz L, et al. Sympathetic reinnervation 1 year after heart transplantation, assessed using iodine-123 metaiodobenzylguanidine imaging. Transplant Proc 2011;43:2247-8. |
| 67. | Olmetti F, Pinna GD, Maestri R, D'Armini A, Pellegrini C, Viganò M, et al. Heart rate and cardiac allograft vasculopathy in heart transplant recipients. J Heart Lung Transplant 2011;30:1368-73. |
| 68. | Berman M, Ali A, Ashley E, Freed D, Clarke K, Tsui S, et al. Is stress cardiomyopathy the underlying cause of ventricular dysfunction associated with brain death? J Heart Lung Transplant 2010;29:957-65. |
| 69. | Mohamedali B, Bhat G, Tatooles A, Zelinger A. Neurogenic stress cardiomyopathy in heart donors. J Card Fail 2014;20:207-11. |
[Figure 1]
[Table 1]
|
Search Pubmed for