A Comprehensive Excursus of the Roles of Echocardiography in Heart Transplantation Follow-Up

Current guidelines for the care of heart transplantation recipients recommend routine endomyocardial biopsy and invasive coronary angiography as the cornerstones in the surveillance for acute rejection (AR) and coronary allograft vasculopathy (CAV). Non-invasive tools, including coronary computed tomography angiography and cardiac magnetic resonance, have been introduced into guidelines without roles of their own as gold standards. These techniques also carry the risk of contrast-related kidney injury. There is a need to explore non-invasive approaches providing valuable information while minimizing risks and allowing their application independently of patient comorbidities. Echocardiographic examination can be performed at bedside, serially repeated, and does not carry the burden of contrast-related kidney injury and procedure-related risk. It provides comprehensive assessment of cardiac morphology and function. Advanced echocardiography techniques, including Doppler tissue imaging and strain imaging, may be sensitive tools for the detection of minor myocardial dysfunction, thus providing insight into early detection of AR and CAV. Stress echocardiography may offer a valuable tool in the detection of CAV, while the assessment of coronary flow reserve can unravel coronary microvascular impairment and add prognostic value to conventional stress echocardiography. The review highlights the role of Doppler echocardiography in heart transplantation follow-up, weighting advantages and limitations of the different techniques.

[1]  G. Gerosa,et al.  New Non-Invasive Imaging Technologies in Cardiac Transplant Follow-Up: Acquired Evidence and Future Options , 2023, Diagnostics.

[2]  A. Angelini,et al.  The International Society for Heart and Lung Transplantation (ISHLT) guidelines for the care of heart transplant recipients. , 2022, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[3]  A. Caixeta,et al.  Evaluation of the myocardial deformation in the diagnosis of rejection after heart transplantation , 2022, Frontiers in Cardiovascular Medicine.

[4]  S. Poulsen,et al.  Assessment of Acute Rejection by Global Longitudinal Strain and Cardiac Biomarkers in Heart-Transplanted Patients , 2022, Frontiers in Immunology.

[5]  W. Droogné,et al.  Speckle-tracking-based global longitudinal and circumferential strain detect early signs of antibody-mediated rejection in heart transplant patients. , 2021, European heart journal. Cardiovascular Imaging.

[6]  V. Salemi,et al.  Diagnostic Accuracy of Dobutamine Stress Echocardiography for Detection of Cardiac Allograft Vasculopathy in Orthotopic Heart Transplant Patients , 2021, Journal of the Saudi Heart Association.

[7]  E. Grove,et al.  CORONARY FLOW VELOCITY RESERVE AND MYOCARDIAL DEFORMATION PREDICT LONG-TERM OUTCOME IN HEART TRANSPLANT RECIPIENTS. , 2021, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[8]  M. Villavicencio,et al.  Primary graft dysfunction in heart transplantation: How to recognize it, when to institute extracorporeal membrane oxygenation, and outcomes , 2021, JTCVS open.

[9]  M. Cameli,et al.  Detection of cardiac allograft vasculopathy by multi-layer left ventricular longitudinal strain in heart transplant recipients , 2021, The International Journal of Cardiovascular Imaging.

[10]  J. Defraigne,et al.  Constrictive pericarditis after heart transplantation: a case report. , 2020, European heart journal. Case reports.

[11]  M. Pan,et al.  Tissue Doppler velocities for ruling out rejection in heart transplant recipients in the context of myocardial strain imaging: a multivariate, prospective, single-center study , 2020, The International Journal of Cardiovascular Imaging.

[12]  M. Xie,et al.  Diagnostic value of myocardial strain using two‐dimensional speckle‐tracking echocardiography in acute cardiac allograft rejection: A systematic review and meta‐analysis , 2020, Echocardiography.

[13]  R. Kerber,et al.  Pharmacological vs Exercise Stress Echocardiography for Detection of Cardiac Allograft Vasculopathy , 2020, Mayo Clinic proceedings. Innovations, quality & outcomes.

[14]  B. Meiser,et al.  The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: Thirty-sixth adult heart transplantation report - 2019; focus theme: Donor and recipient size match. , 2019, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[15]  N. Nanda,et al.  GLOBAL LONGITUDINAL STRAIN ASSESSMENT OF THE LEFT VENTRICLE BY SPECKLE TRACKING ECHOCARDIOGRAPHY DETECTS ACUTE CELLULAR REJECTION IN ORTHOTOPIC HEART TRANSPLANT RECIPIENTS: A SYSTEMATIC REVIEW AND META-ANALYSIS , 2019, Journal of the American College of Cardiology.

[16]  N. Nanda,et al.  Diagnostic accuracy of dobutamine stress echocardiography in the detection of cardiac allograft vasculopathy in heart transplant recipients: A systematic review and meta‐analysis study , 2019, Echocardiography.

[17]  E. Zorn Effector B cells in cardiac allograft vasculopathy , 2019, Current opinion in organ transplantation.

[18]  M. Zembala,et al.  Speckle-Tracking Echocardiography for Monitoring Acute Rejection in Transplanted Heart. , 2018, Transplantation proceedings.

[19]  M. Zembala,et al.  Evaluation of the Graft Mechanical Function Using Speckle-Tracking Echocardiography During the First Year After Orthotropic Heart Transplantation , 2018, Annals of transplantation.

[20]  A. Kfoury,et al.  Microvascular Loss and Diastolic Dysfunction in Severe Symptomatic Cardiac Allograft Vasculopathy , 2018, Circulation. Heart failure.

[21]  M. Stagmo,et al.  Normal Reference Ranges for Transthoracic Echocardiography Following Heart Transplantation , 2017, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[22]  Z. Ali,et al.  Dobutamine stress echocardiography is inadequate to detect early cardiac allograft vasculopathy. , 2016, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[23]  L. Alonso Pulpón,et al.  Two‐Dimensional Speckle Tracking Echocardiography in Heart Transplant Patients: Two‐Year Follow‐Up of Right and Left Ventricular Function , 2016, Echocardiography.

[24]  P. Lancellotti,et al.  Can multiple previous treatment-requiring rejections affect biventricular myocardial function in heart transplant recipients? A two-dimensional speckle-tracking study. , 2016, International journal of cardiology.

[25]  A. Javaheri,et al.  How to Approach the Assessment of Cardiac Allograft Vasculopathy in the Modern Era: Review of Invasive Imaging Modalities , 2016, Current Heart Failure Reports.

[26]  I. García-Lunar,et al.  Usefulness of Two-Dimensional Strain Parameters to Diagnose Acute Rejection after Heart Transplantation. , 2015, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[27]  L. Badano,et al.  European Association of Cardiovascular Imaging/Cardiovascular Imaging Department of the Brazilian Society of Cardiology recommendations for the use of cardiac imaging to assess and follow patients after heart transplantation. , 2015, European heart journal cardiovascular Imaging.

[28]  J. Kobashigawa,et al.  Antibody-mediated rejection in cardiac transplantation: emerging knowledge in diagnosis and management: a scientific statement from the American Heart Association. , 2015, Circulation.

[29]  M. Desai,et al.  Dobutamine stress echocardiography during follow-up surveillance in heart transplant patients: Diagnostic accuracy and predictors of outcomes. , 2015, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[30]  J. Lindenfeld,et al.  Myocardial strain and strain rate from speckle-tracking echocardiography are unable to differentiate asymptomatic biopsy-proven cellular rejection in the first year after cardiac transplantation. , 2015, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[31]  S. Aggarwal,et al.  Strain and strain rate imaging using speckle tracking in acute allograft rejection in children with heart transplantation , 2015, Pediatric transplantation.

[32]  S. Poulsen,et al.  Changes in longitudinal myocardial deformation during acute cardiac rejection: the clinical role of two-dimensional speckle-tracking echocardiography. , 2015, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[33]  S. Poulsen,et al.  Evaluation of longitudinal myocardial deformation by 2-dimensional speckle-tracking echocardiography in heart transplant recipients: relation to coronary allograft vasculopathy. , 2015, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[34]  J. A. Vázquez de Prada,et al.  Chronic Renal Insufficiency in Heart Transplant Recipients: Risk Factors and Management Options , 2014, Drugs.

[35]  Stavros G Drakos,et al.  Coronary computed tomography angiography for the detection of cardiac allograft vasculopathy: a meta-analysis of prospective trials. , 2014, Journal of the American College of Cardiology.

[36]  Zhezhen Jin,et al.  Left ventricular longitudinal strain by speckle-tracking echocardiography is associated with treatment-requiring cardiac allograft rejection. , 2014, Journal of cardiac failure.

[37]  L. Sade,et al.  Follow-up of heart transplant recipients with serial echocardiographic coronary flow reserve and dobutamine stress echocardiography to detect cardiac allograft vasculopathy. , 2014, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[38]  S. Russell,et al.  Report from a consensus conference on primary graft dysfunction after cardiac transplantation. , 2014, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[39]  S. Cook,et al.  Quantitative myocardial contrast echocardiography: a new method for the non-invasive detection of chronic heart transplant rejection. , 2013, European heart journal cardiovascular Imaging.

[40]  S. Colan,et al.  Tissue Doppler imaging for rejection surveillance in pediatric heart transplant recipients. , 2013, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[41]  G. Di Salvo,et al.  Right heart morphology and function in heart transplantation recipients , 2013, Journal of cardiovascular medicine.

[42]  Z. Gertz,et al.  Marked changes in right ventricular contractile pattern after cardiothoracic surgery: implications for post-surgical assessment of right ventricular function. , 2013, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[43]  L. Held,et al.  Pericardial effusion unrelated to surgery is a predictor of mortality in heart transplant patients. , 2013, Cardiology journal.

[44]  S. Litwin,et al.  Noninvasive diagnosis of cardiac allograft rejection using echocardiography indices of systolic and diastolic function. , 2011, Transplantation proceedings.

[45]  S. Goland,et al.  Changes in left and right ventricular function of donor hearts during the first year after heart transplantation , 2011, Heart.

[46]  M. Colvin-adams,et al.  Cardiac allograft vasculopathy: current knowledge and future direction , 2011, Clinical transplantation.

[47]  R. Starling,et al.  International Society for Heart and Lung Transplantation working formulation of a standardized nomenclature for cardiac allograft vasculopathy-2010. , 2010, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[48]  G. Gerosa,et al.  Coronary Flow Reserve by Transthoracic Echocardiography Predicts Epicardial Intimal Thickening in Cardiac Allograft Vasculopathy , 2010, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[49]  N. Oda,et al.  Strain rate imaging would predict sub-clinical acute rejection in heart transplant recipients. , 2010, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[50]  E. Ingulli Mechanism of cellular rejection in transplantation , 2010, Pediatric Nephrology.

[51]  E. Caiani,et al.  Is right ventricular systolic function reduced after cardiac surgery? A two- and three-dimensional echocardiographic study. , 2009, European journal of echocardiography : the journal of the Working Group on Echocardiography of the European Society of Cardiology.

[52]  R. Hetzer,et al.  Echocardiographic strain and strain rate imaging--clinical applications. , 2009, International Journal of Cardiology.

[53]  R. Starling,et al.  Tricuspid regurgitation after cardiac transplantation: an old problem revisited. , 2008, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[54]  M. Galderisi,et al.  Usefulness and limitations of transthoracic echocardiography in heart transplantation recipients , 2008, Cardiovascular ultrasound.

[55]  F. Rademakers,et al.  Quantitative dobutamine stress echocardiography for the early detection of cardiac allograft vasculopathy in heart transplant recipients , 2007, Heart.

[56]  G. Sutherland,et al.  The potential clinical role of ultrasonic strain and strain rate imaging in diagnosing acute rejection after heart transplantation. , 2007, European journal of echocardiography : the journal of the Working Group on Echocardiography of the European Society of Cardiology.

[57]  Ó. Cano,et al.  Echocardiographic evaluation of the evolutionary changes after heart transplantation. , 2006, Transplantation proceedings.

[58]  Harlan M Krumholz,et al.  Detection of heart transplant rejection in adults by echocardiographic diastolic indices: a systematic review of the literature. , 2006, Journal of the American Society of Echocardiography : official publication of the American Society of Echocardiography.

[59]  C. Angermann,et al.  Assessment of cardiac allograft vasculopathy late after heart transplantation: when is coronary angiography necessary? , 2006, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[60]  G. Gerosa,et al.  Coronary Flow Reserve by Contrast‐Enhanced Echocardiography: A New Noninvasive Diagnostic Tool for Cardiac Allograft Vasculopathy , 2006, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[61]  Mario J. Garcia,et al.  Non-invasive evaluation of orthotopic heart transplant rejection by echocardiography. , 2005, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[62]  E. Bocchi,et al.  Dobutamine stress echocardiography predicts cardiac events or death in asymptomatic patients long-term after heart transplantation: 4-year prospective evaluation. , 2004, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[63]  S. Ray,et al.  Can the index of myocardial performance be used to detect acute cellular rejection after heart transplantation? , 2003, The American journal of cardiology.

[64]  A. Haverich,et al.  Heart transplantation: echocardiographic assessment of morphology and function after more than 10 years of follow-up. , 2002, The Annals of thoracic surgery.

[65]  R. Hetzer,et al.  Left ventricular dysfunction during cardiac allograft rejection: early diagnosis, relationship to the histological severity grade, and therapeutic implications. , 2002, Transplantation proceedings.

[66]  C. Lavie,et al.  Usefulness of the combined index of systolic and diastolic myocardial performance to identify cardiac allograft rejection. , 2002, The American journal of cardiology.

[67]  E. Wellnhofer,et al.  Reliability of Tissue Doppler Wall Motion Monitoring After Heart Transplantation for Replacement of Invasive Routine Screenings by Optimally Timed Cardiac Biopsies and Catheterizations , 2001, Circulation.

[68]  S. Russell,et al.  Evaluation of early postoperative results after bicaval versus standard cardiac transplantation and review of the literature. , 2000, American heart journal.

[69]  H. Bittner,et al.  Right ventricular dysfunction after cardiac transplantation: primarily related to status of donor heart. , 1999, The Annals of thoracic surgery.

[70]  R L Kormos,et al.  Evaluation of the potential role of color-coded tissue Doppler echocardiography in the detection of allograft rejection in heart transplant recipients. , 1999, American heart journal.

[71]  U. Siebert,et al.  Diagnostic and prognostic value of serial dobutamine stress echocardiography for noninvasive assessment of cardiac allograft vasculopathy: a comparison with coronary angiography and intravascular ultrasound. , 1999, Circulation.

[72]  K. Akosah,et al.  Dobutamine stress echocardiography early after heart transplantation predicts development of allograft coronary artery disease and outcome. , 1998, Journal of the American College of Cardiology.

[73]  B. Reichart,et al.  Role of dobutamine stress echocardiography for diagnosis of cardiac allograft vasculopathy. , 1998, Transplantation proceedings.

[74]  K. Akosah,et al.  Role of dobutamine stress echocardiography in heart transplant patients. , 1998, Chest.

[75]  L. Martinelli,et al.  Echo-controlled endomyocardial biopsy in orthotopic heart transplantation with bicaval anastomosis. , 1997, Giornale italiano di cardiologia.

[76]  M. Yacoub,et al.  The prognostic significance of non-invasive cardiac tests in heart transplant recipients. , 1997, European heart journal.

[77]  J. Peteiro,et al.  Differences in heart transplant physiology according to surgical technique. , 1996, The Journal of thoracic and cardiovascular surgery.

[78]  R. Wilensky,et al.  Exercise echocardiography, angiography, and intracoronary ultrasound after cardiac transplantation. , 1996, The American journal of cardiology.

[79]  K. Akosah,et al.  Dobutamine stress echocardiography in orthotopic heart transplant recipients. , 1996, Journal of the American College of Cardiology.

[80]  M. Frigerio,et al.  Significance of pericardial effusion after heart transplantation. , 1995, The American journal of cardiology.

[81]  M. Kern,et al.  Superior accuracy of anatomic positioning with echocardiographic- over fluoroscopic-guided endomyocardial biopsy. , 1993, Catheterization and cardiovascular diagnosis.

[82]  D. Reich,et al.  The pericardium exerts constraint on the right ventricle during cardiac surgery , 1990, Acta anaesthesiologica Scandinavica.

[83]  R. Popp,et al.  Left ventricular diastolic function. Doppler echocardiographic changes soon after cardiac transplantation. , 1990, Circulation.

[84]  A. Pezzano,et al.  Echocardiographic assessment of cardiac allograft rejection. , 1989, European heart journal.

[85]  S. Hunt,et al.  Changes in Doppler echocardiographic indexes of left ventricular function as potential markers of acute cardiac rejection. , 1987, Circulation.

[86]  L. Cohn,et al.  Time course of resolution of pulmonary hypertension and right ventricular remodeling after orthotopic cardiac transplantation. , 1987, Circulation.

[87]  L. Stevenson,et al.  Mitral regurgitation after cardiac transplantation. , 1987, The American journal of cardiology.

[88]  N. Magid,et al.  Left ventricular function of heart allografts during acute rejection: an echocardiographic assessment. , 1985, The Journal of heart transplantation.

[89]  G. Gerosa,et al.  Endomyocardial biopsy under echocardiographic monitoring. , 2016, Multimedia manual of cardiothoracic surgery : MMCTS.

[90]  T. Mohanakumar,et al.  Mechanisms of chronic cardiac allograft rejection. , 2013, Texas Heart Institute journal.

[91]  E. Thorn,et al.  Echocardiography in the cardiac transplant recipient. , 2007, Heart failure clinics.

[92]  N. Giannetti,et al.  Tricuspid regurgitation after cardiac transplantation: how many biopsies are too many? , 2005, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[93]  J. Murgo,et al.  New developments in the diagnosis and management of cardiac allograft vasculopathy. , 1995, Texas Heart Institute journal.

[94]  G. Ciliberto,et al.  High-dose dipyridamole echocardiography test in coronary artery disease after heart transplantation. , 1993, European heart journal.

[95]  J. V. Nixon,et al.  Echocardiographic profile of the transplanted human heart in clinically well recipients. , 1992, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[96]  S. Hunt,et al.  A hemodynamic and Doppler echocardiographic study of ventricular function in long-term cardiac allograft recipients. Etiology and prognosis of restrictive-constrictive physiology. , 1989, Circulation.