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Reverse Takotsubo Stress Cardiomyopathy During Liver Transplantation

Published:December 12, 2022DOI:https://doi.org/10.1053/j.jvca.2022.12.008

      Key Words

      Takotsubo cardiomyopathy (TC), also known as stress-induced cardiomyopathy or “broken heart syndrome,” is characterized by an acute, reversible ventricular wall motion abnormality.
      • Prasad A
      • Lerman A
      • Rihal CS.
      Apical ballooning syndrome (Tako-tsubo or stress cardiomyopathy): A mimic of acute myocardial infarction.
      Typical TC involves apical hypokinesis/akinesis and basal hyperkinesis, but anatomic variants have been described, including a midventricular akinesis/hypokinesis and a basal wall motion abnormality, referred to as “reverse TC” (rTC).
      • Prasad A
      • Lerman A
      • Rihal CS.
      Apical ballooning syndrome (Tako-tsubo or stress cardiomyopathy): A mimic of acute myocardial infarction.
      This is a rare form of TC that has been reported to have distinct clinical and diagnostic criteria. Takotsubo cardiomyopathy has been reported in the perioperative period of major surgeries, including orthotopic liver transplantation (OLT).
      • Bedanova H
      • Ondrasek J
      • Filipensky P
      • et al.
      Inverted takotsubo cardiomyopathy as an early complication after liver transplantation.
      • Eagle SS
      • Thompson A
      • Fong PP
      • et al.
      Takotsubo cardiomyopathy and coronary vasospasm during orthotopic liver transplantation: Separate entities or common mechanism?.
      • Lee HR
      • Hurst RT
      • Vargas HE.
      Transient left ventricular apical ballooning syndrome (takotsubo cardiomyopathy) following orthotopic liver transplantation.
      • Mukhtar A
      • Moharam H
      • Sarhan K
      • et al.
      Liver transplantation using dexmedetomidine in a patient with a history of takotsubo cardiomyopathy.
      • Saner FH
      • Plicht B
      • Treckmann J
      • et al.
      Tako-tsubo syndrome as a rare cause of cardiac failure in liver transplantation.
      • Tachotti Pires LJ
      • Cardoso Curiati MN
      • Vissoci Reiche F
      • et al.
      Stress-induced cardiomyopathy (takotsubo cardiomyopathy) after liver transplantation-report of two cases.
      • Tiwari AK
      • D'Attellis N
      Intraoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy during orthotopic liver transplantation.
      • Vitin AA
      • Pennington MW
      • Bowdle TA
      • et al.
      Stress (takotsubo) cardiomyopathy during liver transplantation: Case study and literature review.
      • Bedanova H
      • Orban M
      • Nemec P.
      Postoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy following orthotopic liver transplantation.
      Timely intraoperative diagnosis of rTC via transesophageal echocardiography (TEE), in the setting of OLT, is challenging. New left ventricular dysfunction, hemodynamic changes, and an altered electrocardiogram can be potentially due to TC or its variants including rTC. The authors present a case of intraoperative rTC during OLT and detail the diagnostic and clinical management.

      Case Presentation

      A 57-year-old White woman with a history of cryptogenic cirrhosis, status post-OLT 25 years earlier, presented for retransplantation due to chronic rejection. She had a Model for End-Stage Liver Disease score of 35, and underwent transjugular intrahepatic portosystemic shunt 2 days prior to retransplantation. Her acute liver decompensation was complicated by mild encephalopathy, grade 2 esophageal varices requiring banding, and hepatorenal syndrome requiring hemodialysis. The past medical history was significant for hypertension and hypothyroidism. She had no known significant cardiac history and preoperative coronary angiography demonstrated nonobstructive coronary artery disease. Preoperative transthoracic echocardiography demonstrated normal left ventricular ejection fraction of 70%, with no regional wall motional abnormalities and no valvular pathology.
      On the day of surgery, the patient was brought to the operating room, standard American Society of Anesthesiologists monitors were placed, and the patient was induced with 2 mg of midazolam, 125 µg of fentanyl, 100 mg of propofol, and 8 mg of vecuronium. After endotracheal intubation with a single-lumen 8.0 endotracheal tube, a right radial arterial catheter was placed, and a TEE probe was inserted atraumatically. Anesthesia was maintained with sevoflurane. A 9-French introducer in the right internal jugular vein was inserted under ultrasound guidance, followed by a pulmonary artery catheter. Given this patient's retransplant status and anticipation of a complex surgery with a potentially prolonged anhepatic phase, and risks of significant blood loss, hemodynamic instability, and cardiac arrest, a venovenous bypass (VVB) was planned. An outflow cannula was placed percutaneously in the right internal jugular vein at the time of central line placement. An inflow cannula was placed by the surgical team via the right femoral vein. Portal vein cannulation was avoided due to intravascular thrombosis after transjugular intrahepatic portosystemic shunt placement.
      The VVB was initiated prior to hepatectomy. The circulation was supported with the use of vasoactive infusions of phenylephrine, vasopressin, and norepinephrine to maintain mean arterial pressures >65 mmHg. Immediately prior to reperfusion, the patient become acutely hypotensive and premature ventricular contractions were observed on the electrocardiogram. The TEE assessment demonstrated new severe depression of left ventricular ejection fraction of 20%, basal akinesis, and apical hyperkinesis. Additional inotropic support was implemented with intermittent boluses of epinephrine and ephedrine. Hemodynamics stabilized and portal vein reperfusion was tolerated well without further hemodynamic instability. The patient was weaned off VVB and the hepatic artery and biliary anastomoses were uneventful. The graft was reperfused within 7 hours from donor aortic cross-clamp. The intraoperative estimated blood loss was 5.3 liters, and the patient was transfused 10 units of packed red blood cells, 3 units of fresh frozen plasma, 1 pack of platelets, and 2 packs of cryoprecipitate.
      The patient was transferred to the intensive care unit while sedated and intubated. High-sensitivity troponin T assay peaked at 478 ng/L, and probrain natriuretic peptide was more than 50,000 pmol/L. Cardiac catheterization ruled out significant obstructive coronary artery disease, and laboratory testing was negative for viral infection. Postoperative transthoracic echocardiography (TTE) demonstrated severely reduced left ventricular ejection fraction of 13%, left ventricular dilatation, and severe mitral regurgitation. Given the clinical presentation, the patient was diagnosed with rTC. Diuretic therapy and a dobutamine infusion were initiated. Hemodynamics improved and the patient was extubated on postoperative day 2, and a follow-up TTE on postoperative day 12 demonstrated improved left ventricular function, with an ejection fraction of 43%, and resolution of mitral regurgitation. The patient was discharged home on postoperative day 25.

      Discussion

      This report described intraoperative rTC in a patient undergoing OLT. Appropriate diagnosis and prompt clinical management resulted in a favorable outcome. Intraoperative findings of acute hemodynamic changes with acutely reduced left ventricular function in a patient with no history of coronary artery disease should alert the clinician to this potential diagnosis. Takotsubo cardiomyopathy is characterized by an acute, reversible ventricular wall motion abnormality not associated with a specific coronary artery distribution.
      • Prasad A
      • Lerman A
      • Rihal CS.
      Apical ballooning syndrome (Tako-tsubo or stress cardiomyopathy): A mimic of acute myocardial infarction.
      Although the pathophysiology of TC is poorly understood, it is associated with a sympathetic drive from physiologic or emotional stress, leading to a release of catecholamines and eventual microvascular dysfunction.
      • Guglin M
      • Nazif K.
      New onset nonischemic cardiomyopathy post liver transplantation.
      Takotsubo cardiomyopathy can lead to left ventricular thrombus formation, left ventricular outflow tract obstruction, and mitral regurgitation from systolic anterior movement of the anterior mitral valve leaflet. Takotsubo cardiomyopathy was previously described as a benign condition given its transient clinical course, though its reported mortality is comparable to mortality from acute coronary syndrome.
      • Prasad A
      • Lerman A
      • Rihal CS.
      Apical ballooning syndrome (Tako-tsubo or stress cardiomyopathy): A mimic of acute myocardial infarction.
      In the United States, hospitalizations with TC as a primary or secondary diagnosis have increased from 75 cases per million adults in 2007 to 259 per million in 2012, likely due to the improved understanding of this distinct entity.
      • Khera R
      • Light-McGroary K
      • Zahr F
      • et al.
      Trends in hospitalization for takotsubo cardiomyopathy in the United States.
      Typical TC involves apical hypokinesis/akinesis and basal hyperkinesis, also described as apical ballooning.
      • Prasad A
      • Lerman A
      • Rihal CS.
      Apical ballooning syndrome (Tako-tsubo or stress cardiomyopathy): A mimic of acute myocardial infarction.
      It was first reported in 1990 and named takotsubo, which is the term for “octopus trap” in Japanese, due to the distinct appearance of the ventricle. Reverse TC is the most common variant of TC, presenting with basal akinesis and apical hyperkinesis (Table 1).
      • Awad HH
      • McNeal AR
      • Goyal H.
      Reverse takotsubo cardiomyopathy: A comprehensive review.
      Wall motion abnormalities are transient, with rapid recovery in most patients; however, acute pulmonary edema and profound circulatory collapse have been reported. Intraoperative recognition of TC and rTC depends on a high degree of clinical suspicion and availability of TEE for timely evaluation and management. This cardiac complication may go unrecognized in OLT if TEE monitoring is not adopted or if there is a lack of familiarity with atypical forms of TC. Orthotopic liver transplantation is associated with large fluid shifts, hemodynamic perturbations, increased systemic inflammatory markers, and risk of intraoperative cardiac arrest.
      • Bezinover D
      • Mukhtar A
      • Wagener G
      • et al.
      Hemodynamic instability during liver transplantation in patients with end-stage liver disease: A consensus document from ILTS, LICAGE, and SATA.
      ,
      • Smith NK
      • Zerillo J
      • Kim SJ
      • et al.
      Intraoperative cardiac arrest during adult liver transplantation: Incidence and risk factor analysis from 7 academic centers in the United States.
      Intraoperative TEE is used in some centers to understand cardiac function and volume status during OLT. Routine use of TEE is controversial in OLT, as patients often present with esophageal varices, coagulopathy, and thrombocytopenia, thus increasing the risk of an adverse event (eg, esophageal injury, variceal tear, bleeding) with probe insertion. Additionally, the majority of patients have normal preoperative left ventricular function and invasive hemodynamic monitoring is standard. National societies, such as The American Society of Anesthesiologists, Society of Cardiovascular Anesthesiologists, and the American Society of Echocardiography, support the use of TEE in OLT for monitoring ventricular and valvular function.
      • Shanewise JS
      • Cheung AT
      • Aronson S
      • et al.
      ASE/SCA guidelines for performing a comprehensive intraoperative multiplane transesophageal echocardiography examination: Recommendations of the American Society of Echocardiography Council for Intraoperative Echocardiography and the Society of Cardiovascular Anesthesiologists Task Force for Certification in Perioperative Transesophageal Echocardiography.
      One of the first reports of the use of TEE in OLT was in 1992, in which the authors assessed the suprahepatic inferior vena cava anastomosis.
      • Bjerke RJ
      • Mieles LA
      • Borsky BJ
      • et al.
      The use of transesophageal ultrasonography for the diagnosis of inferior vena caval outflow obstruction during liver transplantation.
      In contemporary practice, TTE is used frequently during OLT. Survey data from high volume liver transplantation centers in the United States reported frequency of intraoperative TEE use in OLT of 87%.
      • Wax DB
      • Torres A
      • Scher C
      • et al.
      Transesophageal echocardiography utilization in high-volume liver transplantation centers in the United States.
      A recent position paper by the Society for Advancement of Transplant Anesthesia (SATA) states that the use of TEE during OLT is “an effective form of monitoring with a safety profile similar to cardiac surgery patients,” and that “it can improve outcomes in rare, but life-threatening conditions.”
      • De Marchi L
      • Wang CJ
      • Skubas NJ
      • et al.
      Safety and benefit of transesophageal echocardiography in liver transplant surgery: A position paper from the Society for the Advancement of Transplant Anesthesia (SATA).
      Currently, there are no standards for training and certification of liver transplant anesthesiologists performing intraoperative TEE. SATA recommends that “all anesthesiologists who use TEE during liver transplant surgery complete formal training pathways that lead to certification by the National Board of Echocardiography;” whereas other authors have proposed that a learning model based on TEE simulation may be more feasible and still enhance the acquisition of TEE skills in liver transplant anesthesiologists.
      • Christensen JM
      • Nelson JA
      • Klompas AM
      • et al.
      The success of a simulation-based transesophageal echocardiography course for liver transplant anesthesiologists.
      At any rate, it is evident that the use of TEE during OLT is being adopted by liver transplant anesthesiologists.
      Table 1Characteristics of Takotsubo Cardiomyopathy and Reverse Takotsubo Cardiomyopathy
      • Awad HH
      • McNeal AR
      • Goyal H.
      Reverse takotsubo cardiomyopathy: A comprehensive review.
      Takotsubo CardiomyopathyReverse Takotsubo Cardiomyopathy
      Proportion of all Takotsubo cases77-99%1-23%
      Echocardiographic FindingsTransient hypokinesis/akinesis/dyskinesis LV apical segment, basal hyperkinesis

      Lower LVEF than rTC
      Transient hypokinesis/akinesis/dyskinesis LV basal segments, apical hyperkinesis

      Low LVEF, but tend to be higher than TC
      Clinical CharacteristicsOlder age

      Less neurologic disease

      Acute psychiatric episode

      Chest pain, dyspnea, syncope, nausea, abdominal pain, diaphoresis, indigestion
      Younger age

      More neurologic disease (intracranial hemorrhage, multiple sclerosis)

      Administration of exogenous catecholamines

      Chest pain, dyspnea, syncope, nausea, abdominal pain, diaphoresis, indigestion

      More likely complicated by pulmonary edema/cardiogenic shock
      Diagnostic FindingsAbsence of obstructive coronary disease on CT or angiography

      Electrocardiogram changes (ST elevation and/or T-wave inversion), atrial fibrillation

      Elevation in cardiac troponin

      Higher levels of BNP and CRP than rTC
      Absence of obstructive coronary disease on CT or angiography

      Electrocardiogram changes (ST depression and/or T-wave inversion), new bundle-branch block, prolonged QT interval

      Elevation in cardiac troponin
      Proposed Pathophysiologic MechanismsSympathetic stimulation/catecholamine surge

      Unlikely due to coronary artery spasm

      Estrogen deficiency
      Sympathetic stimulation/catecholamine surge

      Coronary artery spasm

      Coronary microvascular impairment

      Estrogen deficiency
      ManagementSupportive

      Pharmacologic/hemodynamic support

      IABP

      Magnesium sulfate
      Supportive

      Pharmacologic/hemodynamic support

      Beta blockers for dynamic LV outflow tract obstruction

      IABP

      Magnesium sulfate
      Abbreviations: BNP, B-type natriuetic peptide; CRP, C-reactive protein; CT, computed tomography; IABP, intraaortic balloon pump; LV, left ventricle; LVEF, left ventricular ejection fraction; rTC, reverse takotsubo cardiomyopathy; TC, takotsubo cardiomyopathy.
      In a recent national database study of 38,740 patients undergoing OLT from 2015 to 2020, the incidence of TC was higher in OLT recipients (0.3%) versus the general population (0.04%).
      • Zmaili M
      • Alzubi J
      • Alkhayyat M
      • et al.
      Takotsubo cardiomyopathy in orthotopic liver transplant recipients: A cohort study using multi-center pooled electronic health record data.
      In another comprehensive analysis of individual cases reports of TC, 9% of >90 perioperative cases occurred in patients undergoing OLT.
      • Vitin AA
      • Azamfirei L
      • Tomescu D.
      Perioperative stress-induced (takotsubo) cardiomyopathy in liver transplant recipients.
      Of these, there are very few reports in the literature of intraoperative TC in OLT diagnosed via TEE (Table 2), the majority of described cases occurred postoperatively. Of intraoperative reports, all authors reported normal preoperative echocardiographic findings with no obstructive coronary disease (Table 2).
      • Eagle SS
      • Thompson A
      • Fong PP
      • et al.
      Takotsubo cardiomyopathy and coronary vasospasm during orthotopic liver transplantation: Separate entities or common mechanism?.
      ,
      • Mukhtar A
      • Moharam H
      • Sarhan K
      • et al.
      Liver transplantation using dexmedetomidine in a patient with a history of takotsubo cardiomyopathy.
      ,
      • Tiwari AK
      • D'Attellis N
      Intraoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy during orthotopic liver transplantation.
      ,
      • Vitin AA
      • Pennington MW
      • Bowdle TA
      • et al.
      Stress (takotsubo) cardiomyopathy during liver transplantation: Case study and literature review.
      ,
      • Elapavaluru S
      • Gologorsky A
      • Thai N
      • et al.
      Perioperative stress cardiomyopathy in simultaneous liver and kidney transplantation: A call for early consideration of mechanical circulatory support.
      TC was associated with substantial hemodynamic derangements, with some necessitating use of an intraaortic balloon pump and cardiopulmonary resuscitation.
      • Eagle SS
      • Thompson A
      • Fong PP
      • et al.
      Takotsubo cardiomyopathy and coronary vasospasm during orthotopic liver transplantation: Separate entities or common mechanism?.
      ,
      • Tiwari AK
      • D'Attellis N
      Intraoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy during orthotopic liver transplantation.
      ,
      • Vitin AA
      • Pennington MW
      • Bowdle TA
      • et al.
      Stress (takotsubo) cardiomyopathy during liver transplantation: Case study and literature review.
      Tiwari, Eagle, and Mukhtar described decisions to abort the case to further stabilize the patient prior to transplantation, 2 patients prior to biliary anastomosis, and 1 patient prior to skin incision, with the authors further describing subsequent successful OLT in all 3 patients.
      • Eagle SS
      • Thompson A
      • Fong PP
      • et al.
      Takotsubo cardiomyopathy and coronary vasospasm during orthotopic liver transplantation: Separate entities or common mechanism?.
      ,
      • Mukhtar A
      • Moharam H
      • Sarhan K
      • et al.
      Liver transplantation using dexmedetomidine in a patient with a history of takotsubo cardiomyopathy.
      ,
      • Tiwari AK
      • D'Attellis N
      Intraoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy during orthotopic liver transplantation.
      Mukhtar et al. also noted use of dexmedetomidine infusion in the subsequent OLT, started prior to induction of anesthesia, with continued use throughout the case.
      • Mukhtar A
      • Moharam H
      • Sarhan K
      • et al.
      Liver transplantation using dexmedetomidine in a patient with a history of takotsubo cardiomyopathy.
      Dexmedetomidine was used to blunt sympathetic tone, and the surgery was successful without incident.
      Table 2Case Reports of Takotsubo Cardiomyopathy during Orthotopic Liver Transplantation
      AuthorSex/AgePhase of Surgery TC DetectedPresentationEchocardiographic FindingsIntraoperative ManagementPerioperative CourseComments
      Tiwari
      • Tiwari AK
      • D'Attellis N
      Intraoperative left ventricular apical ballooning: Transient takotsubo cardiomyopathy during orthotopic liver transplantation.


      2008
      F/45Post- reperfusionHypotension, peaked T waves, VT, asystoleTypical TC,

      TEE placed after hemodynamic instability
      Prolonged CPR,

      IABP,

      Epinephrine, vasopressin, dobutamine, dopamine, amiodarone
      OLT aborted prior to biliary anastomosis.

      POD 5: IABP discontinued

      POD12: EF 60%
      VVB in place

      POD 2: successful completion OLT

      Eventual death due to hemorrhage
      Eagle
      • Eagle SS
      • Thompson A
      • Fong PP
      • et al.
      Takotsubo cardiomyopathy and coronary vasospasm during orthotopic liver transplantation: Separate entities or common mechanism?.


      2010
      M/64Post-reperfusionHypotension, VT, bradycardia, ST segment elevationTypical TC,

      TEE placed after hemodynamic instability

      Severe hypokinesis
      CPR,

      Vasopressin, norepinephrine, cardioversion,

      Transvenous pacing
      OLT aborted prior to biliary anastomosis.

      Cardiac catheterization: severe RCA vasospasm.
      No VVB

      POD 1: successful completion OLT

      Survived to discharge
      Mukhtar
      • Mukhtar A
      • Moharam H
      • Sarhan K
      • et al.
      Liver transplantation using dexmedetomidine in a patient with a history of takotsubo cardiomyopathy.


      2016
      M/48After induction before skin incisionHypotension, VTTypical TC,

      TTE placed after hemodynamic instability

      EF 15%
      NorepinephrineOLT abortedNo VVB

      Successful OLT 40 days later with dexmedetomidine
      Elapavaluru
      • Elapavaluru S
      • Gologorsky A
      • Thai N
      • et al.
      Perioperative stress cardiomyopathy in simultaneous liver and kidney transplantation: A call for early consideration of mechanical circulatory support.


      2017
      F/70AnhepaticPVCTypical TC,

      EF 25%

      TEE placed after induction

      mitral regurgitation
      Vasopressin, norepinephrineStable through graft reperfusion

      IABP in ICU

      POD 15: tracheostomy
      VVB in place

      Prolonged hospital course

      POD 38: survived to discharge

      POD 60: EF 50%
      Vitin
      • Vitin AA
      • Pennington MW
      • Bowdle TA
      • et al.
      Stress (takotsubo) cardiomyopathy during liver transplantation: Case study and literature review.


      2018
      M/65AnhepaticVT, VF, bradycardiaTypical TC,

      Severe LV dysfunction

      TEE placed after hemodynamic instability
      CPR,

      Cardioversion,

      Vasopressin, norepinephrine
      POD 18: normal EFVVB was started after CPR

      Survived to discharge
      Abbreviations: CPR, cardiopulmonary resuscitation; EF, ejection fraction; IABP, intraaortic balloon pump; ICU, intensive care unit; LV, left ventricle; OLT, orthotopic liver transplantation; POD, postoperative day; PVC, premature ventricular contraction; RCA, right coronary artery; TC, takotsubo cardiomyopathy; TEE, transesophageal echocardiography, VF, ventricular fibrillation; VT, ventricular tachycardia; VVB, venovenous bypass.
      No cases of intraoperative rTC in OLT have been described, and there are several key findings the authors would like to share. Invasive monitoring tools (ie, arterial line, pulmonary artery catheter, central venous catheter) cannot replace intraoperative TEE for assessing cardiac function at points of substantial hemodynamic instability. There is no other definitive intraoperative method of diagnosing TC or atypical TC. There are several variants of TC, and liver transplant clinicians should be aware of the atypical variety, particularly rTC. Clinical management consists of supportive measures, with escalation of care from pharmacologic to mechanical support. The VVB can be implemented at any point to maintain venous return and provide hemodynamic support, particularly if the consensus plan is to continue with the transplant surgery. Although the liver transplant community seems uncertain about the overall value and indications of VVB, it is a powerful tool in supporting hemodynamics in patients with compromised cardiac function.
      • Rangrass G
      • Vannucci A.
      Veno-venous bypass in liver transplantation: A commonly used technique with elusive outcome benefits.
      The literature does not support the use of any specific prophylactic agents, such as beta-blockers or dexmedetomidine, to prevent TC. Pharmacotherapy to decrease sympathetic stimulation should be given in the context of hemodynamic goals.

      Conflict of Interest

      None.

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      Linked Article

      • Reverse Takotsubo Cardiomyopathy During Liver Transplantation: Expert Commentary
        Journal of Cardiothoracic and Vascular Anesthesia
        • Preview
          TAKOTSUBO CARDIOMYOPATHY (TC), otherwise known as “broken-heart syndrome,” is a condition of which most anesthesiologists are aware; however, the Case Conference by Vannucci et al.1 points to a variation that is less familiar. Reverse Takotsubo cardiomyopathy (rTC) differs from traditional TC in that hypokinesis and/or akinesis is observed in the basilar portion of the left ventricle (LV) in contrast to the apical hypokinesis seen in the traditional form. In this case report, a patient with no prior cardiac history became acutely hypotensive and had severe depression of her LV function just prior to reperfusion during liver transplantation.
        • Full-Text
        • PDF
      • Reverse Takotsubo Stress Cardiomyopathy During Liver Transplantation
        Journal of Cardiothoracic and Vascular Anesthesia
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          The Case Conference by Vannucci et al. described an interesting case of reverse Takotsubo cardiomyopathy (rTC) during orthotopic liver transplantation (OLT) and the authors should be congratulated for successfully managing such a challenging case.1
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