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T-Wave Microalternans in Hypertrophic Cardiomyopathy: The Complexity of an Inherited Cardiac Condition with Multiple Phenotypic Expressions

Cardiomiopatia Hipertrófica; Morte Súbita; Arritmias Cardíacas; Desfibriladores Implantáveis

The fact that ventricular tachyarrhythmia is the most frequent cause of sudden cardiac death (SCD) in cardiomyopathies (CM) does not mean that all CM exhibit similar structural and functional alterations that, identified in advance, for example, by analyzing changes in ventricular depolarization and repolarization, may collaborate in the primary prevention of SCD.

In the current edition of ABC Cardiol, Antunes et al.11. Antunes MO, Arteaga-Fernandes E, Samesima N, Pereira Filho HG, Matsumoto AY, Verner RL, et al. Avaliação Prognóstica da Microalternância da onda T na Cardiomiopatia Hipertrófica em um seguimento clínico de 9 anos. Arq Bras Cardiol.2023;120(8):20220833. doi:10.36660/abc/20220833
https://doi.org/10.36660/abc/20220833...
reveals that altered T-wave alternans (TWA) is not associated with SCD and/or malignant ventricular arrhythmias in hypertrophic cardiomyopathy (HCM) patients.11. Antunes MO, Arteaga-Fernandes E, Samesima N, Pereira Filho HG, Matsumoto AY, Verner RL, et al. Avaliação Prognóstica da Microalternância da onda T na Cardiomiopatia Hipertrófica em um seguimento clínico de 9 anos. Arq Bras Cardiol.2023;120(8):20220833. doi:10.36660/abc/20220833
https://doi.org/10.36660/abc/20220833...
This suggests that diagnostic methods used for non-ischemic cardiomyopathies (NICM). stratification may not universally apply across a heterogeneous set of pathologies.

Electrical alterations in ventricular repolarization have long been known to signal a high risk of malignant ventricular arrhythmias and could serve as a non-invasive risk marker for SCD.22. Rosenbaum DS, Jackson LE, Smith JM, Garan H, Ruskin JN, Cohen RJ. Electrical alternans and vulnerability to ventricular arrhythmias. N Engl J Med. 1994 Jan 27;330(4):235-41. doi: 10.1056/NEJM199401273300402. PMID: 8272084.
https://doi.org/10.1056/NEJM199401273300...
Pastore et al. were the first to establish a direct link between TWA and the onset of ventricular reentry,33. Pastore JM, Girouard SD, Laurita KR, Akar FG, Rosenbaum DS. Mechanism linking T-wave alternans to the genesis of cardiac fibrillation. Circulation. 1999 Mar 16;99(10):1385-94. doi: 10.1161/01.cir.99.10.1385. PMID: 10077525.
https://doi.org/10.1161/01.cir.99.10.138...
contributing to the FDA’s approval of TWA as a non-invasive method for evaluating ICD implantation needs in various cardiomyopathies.44. de Oliveira Antunes M, Samesima N, Pereira Filho HG, Matsumoto AY, Verrier RL, Pastore CA, et al. Exercise-induced quantitative microvolt T-wave alternans in hypertrophic cardiomyopathy. J Electrocardiol. 2017 Mar-Apr;50(2):184-90. doi: 10.1016/j.jelectrocard.2016.10.010.
https://doi.org/10.1016/j.jelectrocard.2...

The International Society for Holter and Non-invasive Electrocardiology (ISH-NIE) recommends TWA evaluation when suspected of vulnerability to lethal cardiac arrhythmias. However, none of the prospective studies they analyzed mentioned HCM specifically.55. Verrier RL, Klingenheben T, Malik M, El-Sherif N, Exner DV, Hohnloser SH, Ikeda T, et al. Microvolt T-wave alternans physiological basis, methods of measurement, and clinical utility--consensus guideline by International Society for Holter and Non-invasive Electrocardiology. J Am Coll Cardiol. 2011 Sep 20;58(13):1309-24. doi: 10.1016/j.jacc.2011.06.029.
https://doi.org/10.1016/j.jacc.2011.06.0...

Studies carried out in patients with HCM, in general with small samples and a short clinical follow-up, signaled a correlation between the presence of TWA and a higher degree of myofibrillar disarrangement;66. Kon-No Y, Watanabe J, Koseki Y, Koyama J, Yamada A, Toda S, et al. Microvolt T wave alternans in human cardiac hypertrophy: electrical instability and abnormal myocardial arrangement. J Cardiovasc Electrophysiol. 2001 Jul;12(7):759-63. doi: 10.1046/j.1540-8167.2001.00759.x.
https://doi.org/10.1046/j.1540-8167.2001...
a greater association with echocardiographic findings and ventricular arrhythmia density and heterogeneity of fibrosis sites77. Puntmann VO, Yap YG, McKenna W, Camm J. T-wave alternans and left ventricular wall thickness in predicting arrhythmic risk in patients with hypertrophic cardiomyopathy. Circ J. 2010 Jun;74(6):1197-204. doi: 10.1253/circj.cj-09-1003.
https://doi.org/10.1253/circj.cj-09-1003...
and with the occurrence of nVT88. Trzos E, Kasprzak JD, Krzemińska-Pakuła M, Rechciński T, Wierzbowska-Drabik K, et al. The prevalence and the prognostic value of microvolt T-wave alternans in patients with hypertrophic cardiomyopathy. Ann Non-invasive Electrocardiol. 2011 Jul;16(3):276-86. doi: 10.1111/j.1542-474X.2011.00443.x.
https://doi.org/10.1111/j.1542-474X.2011...
but not being able to prove to be a predictor of serious arrhythmic events.

Even larger studies have had limited HCM patient numbers,99. Vandenberk B, Floré V, Röver C, Vos MA, Dunnink A, Leftheriotis D,et al. Repeating non-invasive risk stratification improves prediction of outcome in ICD patients. Ann Non-invasive Electrocardiol. 2020 Nov;25(6):e12794. doi: 10.1111/anec.12794.
https://doi.org/10.1111/anec.12794...
such as the ALPHA TRIAL, which primarily focused on idiopathic dilated cardiomyopathy.1010. Salerno-Uriarte JA, De Ferrari GM, Klersy C, Pedretti RF, Tritto M, Sallusti L, et al.; ALPHA Study Group Investigators. Prognostic value of T-wave alternans in patients with heart failure due to nonischemic cardiomyopathy: results of the ALPHA Study. J Am Coll Cardiol. 2007 Nov 6;50(19):1896-904. doi: 10.1016/j.jacc.2007.09.004.
https://doi.org/10.1016/j.jacc.2007.09.0...
Despite this, the authors follow the same simplistic and dichotomous approach and recommend incorporating TWA evaluation into the ICD therapy criteria for NYHA functional class II/III NICM.1010. Salerno-Uriarte JA, De Ferrari GM, Klersy C, Pedretti RF, Tritto M, Sallusti L, et al.; ALPHA Study Group Investigators. Prognostic value of T-wave alternans in patients with heart failure due to nonischemic cardiomyopathy: results of the ALPHA Study. J Am Coll Cardiol. 2007 Nov 6;50(19):1896-904. doi: 10.1016/j.jacc.2007.09.004.
https://doi.org/10.1016/j.jacc.2007.09.0...

However, the present study shows that TWA is not a reliable predictor of fatal events in HCM patients. This is primarily due to the disease’s low event rate and, principally, for being characterized by morphological, functional, clinical, and prognostic heterogeneity in which demonstrating new (and independent of conventional) risk markers is a challenging task.1111. Maron BJ, Rowin EJ, Maron MS. Evolution of risk stratification and sudden death prevention in hypertrophic cardiomyopathy: Twenty years with the implantable cardioverter-defibrillator. Heart Rhythm. 2021 Jun;18(6):1012-23. doi: 10.1016/j.hrthm.2021.01.019. Epub 2021 Jan 26.
https://doi.org/10.1016/j.hrthm.2021.01....

Another point of interest is whether or not to discontinue beta-blocker medication before TWA analysis. The ISH-NIE recommends performing TWA tests without altering medication regimens to ensure that test results reflect the effects of chronic drug therapy.55. Verrier RL, Klingenheben T, Malik M, El-Sherif N, Exner DV, Hohnloser SH, Ikeda T, et al. Microvolt T-wave alternans physiological basis, methods of measurement, and clinical utility--consensus guideline by International Society for Holter and Non-invasive Electrocardiology. J Am Coll Cardiol. 2011 Sep 20;58(13):1309-24. doi: 10.1016/j.jacc.2011.06.029.
https://doi.org/10.1016/j.jacc.2011.06.0...

It is important to note that studies on TWA have varied in their protocols regarding the suspension of beta-blocker therapy despite evidence that these drugs affect TWA amplitude and the presence of TWA during testing.1212. Chan PS, Gold MR, Nallamothu BK. Do Beta-blockers impact microvolt T-wave alternans testing in patients at risk for ventricular arrhythmias? A meta-analysis. J Cardiovasc Electrophysiol. 2010 Sep;21(9):1009-14. doi: 10.1111/j.1540-8167.2010.01757.x.
https://doi.org/10.1111/j.1540-8167.2010...

Heart rate is not the sole determinant of TWA because autonomic neurotransmitters and changes in myocardial substrate can lead to elevated levels of TWA during fixed rate pacing.55. Verrier RL, Klingenheben T, Malik M, El-Sherif N, Exner DV, Hohnloser SH, Ikeda T, et al. Microvolt T-wave alternans physiological basis, methods of measurement, and clinical utility--consensus guideline by International Society for Holter and Non-invasive Electrocardiology. J Am Coll Cardiol. 2011 Sep 20;58(13):1309-24. doi: 10.1016/j.jacc.2011.06.029.
https://doi.org/10.1016/j.jacc.2011.06.0...
Meta-analysis of 9 prospective studies in primary prevention patients with left ventricular dysfunction, the predictive power of TWA varied widely based on whether beta-blocker therapy was withheld prior to its assessment. The authors proposed that this observation may explain the inconsistent results of TWA studies in this population.1212. Chan PS, Gold MR, Nallamothu BK. Do Beta-blockers impact microvolt T-wave alternans testing in patients at risk for ventricular arrhythmias? A meta-analysis. J Cardiovasc Electrophysiol. 2010 Sep;21(9):1009-14. doi: 10.1111/j.1540-8167.2010.01757.x.
https://doi.org/10.1111/j.1540-8167.2010...

The significant finding of the present study was that altered TWA was associated with the AHA criteria considered high risk without this being reflected in the power to predict the primary outcome. The authors properly signaled that in HCM, other arrhythmogenic mechanisms, not adequately detectable by high TWA values, are involved in the origin of ventricular arrhythmias and SCD.11. Antunes MO, Arteaga-Fernandes E, Samesima N, Pereira Filho HG, Matsumoto AY, Verner RL, et al. Avaliação Prognóstica da Microalternância da onda T na Cardiomiopatia Hipertrófica em um seguimento clínico de 9 anos. Arq Bras Cardiol.2023;120(8):20220833. doi:10.36660/abc/20220833
https://doi.org/10.36660/abc/20220833...

The result of the present study corroborates an observation that has become more relevant in recent years with a better understanding of the pathophysiology of NICM, findings from in-vivo and experimental studies, results of imaging tests (magnetic resonance imaging), and, finally, advances in genetic research.1313. Rizzo S, Carturan E, De Gaspari M, Pilichou K, Thiene G, Basso C. Update on cardiomyopathies and sudden cardiac death. Forensic Sci Res. 2019 Aug 19;4(3):202-10. doi: 10.1080/20961790.2019.1631957.
https://doi.org/10.1080/20961790.2019.16...
,1414. Ommen SR, Mital S, Burke MA, Day SM, Deswal A, Elliott P, et al. 2020 AHA/ACC Guideline for the Diagnosis and Treatment of Patients With Hypertrophic Cardiomyopathy: Executive Summary: A Report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol. 2020 Dec 22;76(25):3022-55. doi: 10.1016/j.jacc.2020.08.044.
https://doi.org/10.1016/j.jacc.2020.08.0...

The above observations are particularly applicable when dealing with HCM. The apical form of HCM is an example of this complexity, which is a classic phenotypic expression linked to a good clinical prognosis but which, in its so-called atypical forms (e.g., associated with apical aneurysm), presents a more reserved clinical prognosis.1313. Rizzo S, Carturan E, De Gaspari M, Pilichou K, Thiene G, Basso C. Update on cardiomyopathies and sudden cardiac death. Forensic Sci Res. 2019 Aug 19;4(3):202-10. doi: 10.1080/20961790.2019.1631957.
https://doi.org/10.1080/20961790.2019.16...

14. Ommen SR, Mital S, Burke MA, Day SM, Deswal A, Elliott P, et al. 2020 AHA/ACC Guideline for the Diagnosis and Treatment of Patients With Hypertrophic Cardiomyopathy: Executive Summary: A Report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol. 2020 Dec 22;76(25):3022-55. doi: 10.1016/j.jacc.2020.08.044.
https://doi.org/10.1016/j.jacc.2020.08.0...
-1515. Arbelo E, Protonotarios A, Gimeno JR, Arbustini E, Barriales-Villa PL, Basso C, et al. 2023 ESC Guidelines for the management of cardiomyopathies: Developed by the task force on the management of cardiomyopathies of the European Society of Cardiology (ESC) Eur Heart J.2023; ehad194. https://doi.org/10.1093/eurheartj/ehad194
https://doi.org/10.1093/eurheartj/ehad19...
Thus, although each subtype of HCM is defined by its main morphofunctional phenotype, a careful clinical evaluation demonstrates high phenotype variability with due prognostic and therapeutic implications.1414. Ommen SR, Mital S, Burke MA, Day SM, Deswal A, Elliott P, et al. 2020 AHA/ACC Guideline for the Diagnosis and Treatment of Patients With Hypertrophic Cardiomyopathy: Executive Summary: A Report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol. 2020 Dec 22;76(25):3022-55. doi: 10.1016/j.jacc.2020.08.044.
https://doi.org/10.1016/j.jacc.2020.08.0...
Another important aspect is that HCM is a disorder with variable phenotype expression that may progress and change in the same patient.1616. Wilde AAM, Semsarian C, Márquez MF, Shamloo AS, Ackerman MJ, Ashley EA, et al. Developed in partnership with and endorsed by the European Heart Rhythm Association (EHRA), a branch of the European Society of Cardiology (ESC), the Heart Rhythm Society (HRS), the Asia Pacific Heart Rhythm Society (APHRS), and the Latin American Heart Rhythm Society (LAHRS). European Heart Rhythm Association (EHRA)/Heart Rhythm Society (HRS)/Asia Pacific Heart Rhythm Society (APHRS)/Latin American Heart Rhythm Society (LAHRS) Expert Consensus Statement on the state of genetic testing for cardiac diseases. Europace. 2022 Sep 1;24(8):1307-67. doi: 10.1093/europace/euac030. Erratum in: Europace. 2022 Aug 30
https://doi.org/10.1093/europace/euac030...

This finding reflects that the complexity of the HCM arrhythmogenic substrate stems from a combination of alterations and arrangement of myocytes, microvascular abnormalities, interstitial/replacement fibrosis, autonomic modulation, and possibly pathogenic sarcomere gene mutations. However, the role of sarcomeric variants as a predictor of SCD remains to be demonstrated.1111. Maron BJ, Rowin EJ, Maron MS. Evolution of risk stratification and sudden death prevention in hypertrophic cardiomyopathy: Twenty years with the implantable cardioverter-defibrillator. Heart Rhythm. 2021 Jun;18(6):1012-23. doi: 10.1016/j.hrthm.2021.01.019. Epub 2021 Jan 26.
https://doi.org/10.1016/j.hrthm.2021.01....
,1616. Wilde AAM, Semsarian C, Márquez MF, Shamloo AS, Ackerman MJ, Ashley EA, et al. Developed in partnership with and endorsed by the European Heart Rhythm Association (EHRA), a branch of the European Society of Cardiology (ESC), the Heart Rhythm Society (HRS), the Asia Pacific Heart Rhythm Society (APHRS), and the Latin American Heart Rhythm Society (LAHRS). European Heart Rhythm Association (EHRA)/Heart Rhythm Society (HRS)/Asia Pacific Heart Rhythm Society (APHRS)/Latin American Heart Rhythm Society (LAHRS) Expert Consensus Statement on the state of genetic testing for cardiac diseases. Europace. 2022 Sep 1;24(8):1307-67. doi: 10.1093/europace/euac030. Erratum in: Europace. 2022 Aug 30
https://doi.org/10.1093/europace/euac030...
,1717. Maron BJ, Rowin EJ, Maron MS. Paradigm of Sudden Death Prevention in Hypertrophic Cardiomyopathy. Circ Res. 2019 Aug 2;125(4):370-8. doi: 10.1161/CIRCRESAHA.119.315159.
https://doi.org/10.1161/CIRCRESAHA.119.3...

In this era of precision medicine, the future holds great promise for improved risk stratification of cardiomyopathies. Possibly, we will move in the direction that, more than the analysis of changes in ventricular depolarization (e.g., fragmentation of the QRS) or ventricular repolarization (e.g., TWA), the answers will come from the detection of functional, structural, and morphological alterations, genetic biomarkers and analysis of potential epigenetic factors1515. Arbelo E, Protonotarios A, Gimeno JR, Arbustini E, Barriales-Villa PL, Basso C, et al. 2023 ESC Guidelines for the management of cardiomyopathies: Developed by the task force on the management of cardiomyopathies of the European Society of Cardiology (ESC) Eur Heart J.2023; ehad194. https://doi.org/10.1093/eurheartj/ehad194
https://doi.org/10.1093/eurheartj/ehad19...
,1818. Pagiatakis C, Di Mauro V. The emerging role of epigenetics in therapeutic targeting of cardiomyopathies. Int J Mol Sci. 2021 Aug 13;22(16):8721. doi: 10.3390/ijms22168721.
https://doi.org/10.3390/ijms22168721...
These data, combined with clinical markers, in a new space, that of the phenotype-genotype correlation, allowed individualizing the patient’s risk and shared decision-making regarding the need or not for an ICD implant for the primary prevention of SCD.

Referências

  • 1
    Antunes MO, Arteaga-Fernandes E, Samesima N, Pereira Filho HG, Matsumoto AY, Verner RL, et al. Avaliação Prognóstica da Microalternância da onda T na Cardiomiopatia Hipertrófica em um seguimento clínico de 9 anos. Arq Bras Cardiol.2023;120(8):20220833. doi:10.36660/abc/20220833
    » https://doi.org/10.36660/abc/20220833
  • 2
    Rosenbaum DS, Jackson LE, Smith JM, Garan H, Ruskin JN, Cohen RJ. Electrical alternans and vulnerability to ventricular arrhythmias. N Engl J Med. 1994 Jan 27;330(4):235-41. doi: 10.1056/NEJM199401273300402. PMID: 8272084.
    » https://doi.org/10.1056/NEJM199401273300402
  • 3
    Pastore JM, Girouard SD, Laurita KR, Akar FG, Rosenbaum DS. Mechanism linking T-wave alternans to the genesis of cardiac fibrillation. Circulation. 1999 Mar 16;99(10):1385-94. doi: 10.1161/01.cir.99.10.1385. PMID: 10077525.
    » https://doi.org/10.1161/01.cir.99.10.1385
  • 4
    de Oliveira Antunes M, Samesima N, Pereira Filho HG, Matsumoto AY, Verrier RL, Pastore CA, et al. Exercise-induced quantitative microvolt T-wave alternans in hypertrophic cardiomyopathy. J Electrocardiol. 2017 Mar-Apr;50(2):184-90. doi: 10.1016/j.jelectrocard.2016.10.010.
    » https://doi.org/10.1016/j.jelectrocard.2016.10.010
  • 5
    Verrier RL, Klingenheben T, Malik M, El-Sherif N, Exner DV, Hohnloser SH, Ikeda T, et al. Microvolt T-wave alternans physiological basis, methods of measurement, and clinical utility--consensus guideline by International Society for Holter and Non-invasive Electrocardiology. J Am Coll Cardiol. 2011 Sep 20;58(13):1309-24. doi: 10.1016/j.jacc.2011.06.029.
    » https://doi.org/10.1016/j.jacc.2011.06.029
  • 6
    Kon-No Y, Watanabe J, Koseki Y, Koyama J, Yamada A, Toda S, et al. Microvolt T wave alternans in human cardiac hypertrophy: electrical instability and abnormal myocardial arrangement. J Cardiovasc Electrophysiol. 2001 Jul;12(7):759-63. doi: 10.1046/j.1540-8167.2001.00759.x.
    » https://doi.org/10.1046/j.1540-8167.2001.00759.x
  • 7
    Puntmann VO, Yap YG, McKenna W, Camm J. T-wave alternans and left ventricular wall thickness in predicting arrhythmic risk in patients with hypertrophic cardiomyopathy. Circ J. 2010 Jun;74(6):1197-204. doi: 10.1253/circj.cj-09-1003.
    » https://doi.org/10.1253/circj.cj-09-1003
  • 8
    Trzos E, Kasprzak JD, Krzemińska-Pakuła M, Rechciński T, Wierzbowska-Drabik K, et al. The prevalence and the prognostic value of microvolt T-wave alternans in patients with hypertrophic cardiomyopathy. Ann Non-invasive Electrocardiol. 2011 Jul;16(3):276-86. doi: 10.1111/j.1542-474X.2011.00443.x.
    » https://doi.org/10.1111/j.1542-474X.2011.00443.x
  • 9
    Vandenberk B, Floré V, Röver C, Vos MA, Dunnink A, Leftheriotis D,et al. Repeating non-invasive risk stratification improves prediction of outcome in ICD patients. Ann Non-invasive Electrocardiol. 2020 Nov;25(6):e12794. doi: 10.1111/anec.12794.
    » https://doi.org/10.1111/anec.12794
  • 10
    Salerno-Uriarte JA, De Ferrari GM, Klersy C, Pedretti RF, Tritto M, Sallusti L, et al.; ALPHA Study Group Investigators. Prognostic value of T-wave alternans in patients with heart failure due to nonischemic cardiomyopathy: results of the ALPHA Study. J Am Coll Cardiol. 2007 Nov 6;50(19):1896-904. doi: 10.1016/j.jacc.2007.09.004.
    » https://doi.org/10.1016/j.jacc.2007.09.004
  • 11
    Maron BJ, Rowin EJ, Maron MS. Evolution of risk stratification and sudden death prevention in hypertrophic cardiomyopathy: Twenty years with the implantable cardioverter-defibrillator. Heart Rhythm. 2021 Jun;18(6):1012-23. doi: 10.1016/j.hrthm.2021.01.019. Epub 2021 Jan 26.
    » https://doi.org/10.1016/j.hrthm.2021.01.019
  • 12
    Chan PS, Gold MR, Nallamothu BK. Do Beta-blockers impact microvolt T-wave alternans testing in patients at risk for ventricular arrhythmias? A meta-analysis. J Cardiovasc Electrophysiol. 2010 Sep;21(9):1009-14. doi: 10.1111/j.1540-8167.2010.01757.x.
    » https://doi.org/10.1111/j.1540-8167.2010.01757.x
  • 13
    Rizzo S, Carturan E, De Gaspari M, Pilichou K, Thiene G, Basso C. Update on cardiomyopathies and sudden cardiac death. Forensic Sci Res. 2019 Aug 19;4(3):202-10. doi: 10.1080/20961790.2019.1631957.
    » https://doi.org/10.1080/20961790.2019.1631957
  • 14
    Ommen SR, Mital S, Burke MA, Day SM, Deswal A, Elliott P, et al. 2020 AHA/ACC Guideline for the Diagnosis and Treatment of Patients With Hypertrophic Cardiomyopathy: Executive Summary: A Report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J Am Coll Cardiol. 2020 Dec 22;76(25):3022-55. doi: 10.1016/j.jacc.2020.08.044.
    » https://doi.org/10.1016/j.jacc.2020.08.044
  • 15
    Arbelo E, Protonotarios A, Gimeno JR, Arbustini E, Barriales-Villa PL, Basso C, et al. 2023 ESC Guidelines for the management of cardiomyopathies: Developed by the task force on the management of cardiomyopathies of the European Society of Cardiology (ESC) Eur Heart J.2023; ehad194. https://doi.org/10.1093/eurheartj/ehad194
    » https://doi.org/10.1093/eurheartj/ehad194
  • 16
    Wilde AAM, Semsarian C, Márquez MF, Shamloo AS, Ackerman MJ, Ashley EA, et al. Developed in partnership with and endorsed by the European Heart Rhythm Association (EHRA), a branch of the European Society of Cardiology (ESC), the Heart Rhythm Society (HRS), the Asia Pacific Heart Rhythm Society (APHRS), and the Latin American Heart Rhythm Society (LAHRS). European Heart Rhythm Association (EHRA)/Heart Rhythm Society (HRS)/Asia Pacific Heart Rhythm Society (APHRS)/Latin American Heart Rhythm Society (LAHRS) Expert Consensus Statement on the state of genetic testing for cardiac diseases. Europace. 2022 Sep 1;24(8):1307-67. doi: 10.1093/europace/euac030. Erratum in: Europace. 2022 Aug 30
    » https://doi.org/10.1093/europace/euac030
  • 17
    Maron BJ, Rowin EJ, Maron MS. Paradigm of Sudden Death Prevention in Hypertrophic Cardiomyopathy. Circ Res. 2019 Aug 2;125(4):370-8. doi: 10.1161/CIRCRESAHA.119.315159.
    » https://doi.org/10.1161/CIRCRESAHA.119.315159
  • 18
    Pagiatakis C, Di Mauro V. The emerging role of epigenetics in therapeutic targeting of cardiomyopathies. Int J Mol Sci. 2021 Aug 13;22(16):8721. doi: 10.3390/ijms22168721.
    » https://doi.org/10.3390/ijms22168721
  • Short Editorial related to the article: Prognostic Evaluation of Microvolt T-Wave Alternans in Hypertrophic Cardiomyopathy: 9-year Clinical Follow-up

Publication Dates

  • Publication in this collection
    27 Oct 2023
  • Date of issue
    Oct 2023

History

  • Received
    30 Aug 2023
  • Reviewed
    06 Sept 2023
  • Accepted
    06 Sept 2023
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