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Prognostic value of right ventricular trabecular complexity in patients with arrhythmogenic cardiomyopathy

  • Cardiac
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Abstract

Objectives

The present study aimed to investigate the incremental prognostic value of the right ventricular fractal dimension (FD), a novel marker of myocardial trabecular complexity by cardiac magnetic resonance (CMR) in patients with arrhythmogenic cardiomyopathy (ACM).

Methods

Consecutive patients with ACM undergoing CMR were followed up for major cardiac events, including sudden cardiac death, aborted cardiac arrest, and appropriate implantable cardioverter defibrillator intervention. Prognosis prediction was compared by Cox regression analysis. We established a multivariable model supplemented with RV FD and evaluated its discrimination by Harrell’s C-statistic. We compared the category-free, continuous net reclassification improvement (cNRI) and integrated discrimination index (IDI) before and after the addition of FD.

Results

A total of 105 patients were prospectively included from three centers and followed up for a median of 60 (48, 66) months; experienced 36 major cardiac events were recorded. Trabecular FD displayed a strong unadjusted association with major cardiac events (p < 0.05). In the multivariable Cox regression analysis, RV maximal apical FD maintained an independent association with major cardiac events (hazard ratio, 1.31 (1.11–1.55), p < 0.002). The Hosmer–Lemeshow goodness of fit test displayed good fit (X2 = 0.68, p = 0.99). Diagnostic performance was significantly improved after the addition of RV maximal apical FD to the multivariable baseline model, and the continuous net reclassification improvement increased 21% (p = 0.001), and the integrated discrimination index improved 16% (p = 0.045).

Conclusions

In patients with ACM, CMR-assessed myocardial trabecular complexity was independently correlated with adverse cardiovascular events and provided incremental prognostic value.

Clinical relevance statement

The application of FD values for assessing RV myocardial trabeculae may become an accessible and promising parameter in monitoring and early diagnosis of risk factors for adverse cardiovascular events in patients with ACM.

Key Points

• Ventricular trabecular morphology, a novel quantitative marker by CMR, has been explored for the first time to determine the severity of ACM.

• Patients with higher maximal apical fractal dimension of RV displayed significantly higher cumulative incidence of major cardiac events.

• RV maximal apical FD was independently associated with major cardiac events and provided incremental prognostic value in patients with ACM.

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Abbreviations

ACM:

Arrhythmogenic cardiomyopathy

ALVC:

Arrhythmogenic left ventricular cardiomyopathy

ARVC:

Arrhythmogenic right ventricular cardiomyopathy

ARVD:

Arrhythmogenic right ventricular dysplasia

DSG2:

Desmoglein-2

DSP:

Desmoplakin

FD:

Fractal dimension

NSVT:

Non-sustained ventricular tachycardia

PKP2:

Plakophilin-2 gene

PVC:

Premature ventricular complex

TFC:

Task Force Criteria

TWI:

Inverted T-wave

References

  1. Towbin JA, McKenna WJ, Abrams DJ et al (2019) 2019 HRS expert consensus statement on evaluation, risk stratification, and management of arrhythmogenic cardiomyopathy. Heart Rhythm 16:e301–e372

    Article  PubMed  Google Scholar 

  2. Corrado D, Zorzi A, Cipriani A et al (2021) Evolving diagnostic criteria for arrhythmogenic cardiomyopathy. J Am Heart Assoc 10:e021987

    Article  PubMed  PubMed Central  Google Scholar 

  3. Aquaro GD, De Luca A, Cappelletto C et al (2020) Prognostic value of magnetic resonance phenotype in patients with arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol 75:2753–2765

    Article  PubMed  Google Scholar 

  4. Tandri H, Calkins H, Nasir K et al (2003) Magnetic resonance imaging findings in patients meeting Task Force Criteria for arrhythmogenic right ventricular dysplasia. J Cardiovasc Electrophysiol 14:476–482

    Article  PubMed  Google Scholar 

  5. Molinari G, Sardanelli F, Gaita F et al (1995) Right ventricular dysplasia as a generalized cardiomyopathy? Findings on magnetic resonance imaging. Eur Heart J 16:1619–1624

    Article  CAS  PubMed  Google Scholar 

  6. Petersen SE, Jensen B, Aung N et al (2023) Excessive trabeculation of the left ventricle: JACC: Cardiovascular Imaging Expert Panel Paper. JACC Cardiovasc Imaging 16:408–425

    Article  PubMed  PubMed Central  Google Scholar 

  7. Malik N, Mukherjee M, Wu KC et al (2022) Multimodality imaging in arrhythmogenic right ventricular cardiomyopathy. Circ Cardiovasc Imaging 15:e013725

    Article  PubMed  Google Scholar 

  8. Cipriani A, Mattesi G, Bariani R et al (2023) Cardiac magnetic resonance imaging of arrhythmogenic cardiomyopathy: evolving diagnostic perspectives. Eur Radiol 33:270–282

    Article  PubMed  Google Scholar 

  9. Corrado D, PerazzoloMarra M, Zorzi A et al (2020) Diagnosis of arrhythmogenic cardiomyopathy: the Padua criteria. Int J Cardiol 319:106–114

    Article  PubMed  Google Scholar 

  10. Dawes TJW, Cai J, Quinlan M et al (2018) Fractal analysis of right ventricular trabeculae in pulmonary hypertension. Radiology 288:386–395

    Article  PubMed  Google Scholar 

  11. Meyer HV, Dawes TJW, Serrani M et al (2020) Genetic and functional insights into the fractal structure of the heart. Nature 584:589–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Yu S, Chen X, Yang K et al (2022) Correlation between left ventricular fractal dimension and impaired strain assessed by cardiac MRI feature tracking in patients with left ventricular noncompaction and normal left ventricular ejection fraction. Eur Radiol 32:2594–2603

    Article  CAS  PubMed  Google Scholar 

  13. Captur G, Zemrak F, Muthurangu V et al (2015) Fractal analysis of myocardial trabeculations in 2547 study participants: multi-ethnic study of atherosclerosis. Radiology 277:707–715

    Article  PubMed  Google Scholar 

  14. Captur G, Muthurangu V, Cook C et al (2013) Quantification of left ventricular trabeculae using fractal analysis. J Cardiovasc Magn Reson 15:36

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wang J, Li Y, Yang F et al (2021) Fractal analysis: prognostic value of left ventricular trabecular complexity cardiovascular MRI in participants with hypertrophic cardiomyopathy. Radiology 298:71–79

    Article  PubMed  Google Scholar 

  16. Captur G, Lopes LR, Patel V et al (2014) Abnormal cardiac formation in hypertrophic cardiomyopathy: fractal analysis of trabeculae and preclinical gene expression. Circ Cardiovasc Genet 7:241–248

    Article  CAS  Google Scholar 

  17. Captur G, Lopes LR, Mohun TJ et al (2014) Prediction of sarcomere mutations in subclinical hypertrophic cardiomyopathy. Circ Cardiovasc Imaging 7:863–871

    Article  PubMed Central  Google Scholar 

  18. Kramer CM, Barkhausen J, Bucciarelli-Ducci C, Flamm SD, Kim RJ, Nagel E (2020) Standardized cardiovascular magnetic resonance imaging (CMR) protocols: 2020 update. J Cardiovasc Magn Reson 22:17

    Article  PubMed Central  Google Scholar 

  19. Zghaib T, Te Riele A, James CA et al (2021) Left ventricular fibro-fatty replacement in arrhythmogenic right ventricular dysplasia/cardiomyopathy: prevalence, patterns, and association with arrhythmias. J Cardiovasc Magn Reson 23:58

    Article  PubMed  PubMed Central  Google Scholar 

  20. Camporeale A, Moroni F, Lazzeroni D et al (2022) Trabecular complexity as an early marker of cardiac involvement in Fabry disease. Eur Heart J Cardiovasc Imaging 23:200–208

    Article  PubMed  Google Scholar 

  21. Li C, Huang R, Ding Z, Gatenby JC, Metaxas DN, Gore JC (2011) A level set method for image segmentation in the presence of intensity inhomogeneities with application to MRI. IEEE Trans Image Process 20:2007–2016

    Article  PubMed  PubMed Central  Google Scholar 

  22. Captur G, Radenkovic D, Li C et al (2017) Community delivery of semiautomated fractal analysis tool in cardiac MR for trabecular phenotyping. J Magn Reson Imaging 46:1082–1088

    Article  PubMed  Google Scholar 

  23. Gasperetti A, Carrick RT, Costa S et al (2022) Programmed ventricular stimulation as an additional primary prevention risk stratification tool in arrhythmogenic right ventricular cardiomyopathy: a multinational study. Circulation. https://doi.org/10.1161/CIRCULATIONAHA.122.060866

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cadrin-Tourigny J, Bosman LP, Nozza A et al (2019) A new prediction model for ventricular arrhythmias in arrhythmogenic right ventricular cardiomyopathy. Eur Heart J 40:1850–1858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. McCullough J, Perera RG (2022) Arrhythmogenic right ventricular cardiomyopathy. N Engl J Med 387:e20

    Article  PubMed  Google Scholar 

  26. Vogel-Claussen J, Shehata ML, Lossnitzer D et al (2011) Increased right ventricular septomarginal trabeculation mass is a novel marker for pulmonary hypertension: comparison with ventricular mass index and right ventricular mass. Invest Radiol 46:567–575

    Article  PubMed  PubMed Central  Google Scholar 

  27. van de Veerdonk MC, Dusoswa SA, Marcus JT et al (2014) The importance of trabecular hypertrophy in right ventricular adaptation to chronic pressure overload. Int J Cardiovasc Imaging 30:357–365

    Article  PubMed  Google Scholar 

  28. Te Riele AS, James CA, Philips B et al (2013) Mutation-positive arrhythmogenic right ventricular dysplasia/cardiomyopathy: the triangle of dysplasia displaced. J Cardiovasc Electrophysiol 24:1311–1320

    Article  Google Scholar 

  29. Chun KH, Oh J, Hong YJ et al (2022) Prognostic cardiac magnetic resonance markers of left ventricular involvement in arrhythmogenic cardiomyopathy for predicting heart failure outcomes. J Am Heart Assoc 11:e023167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Dowd R, Dhanjal T, Schmucki M, Kanagala P, Khan JN (2021) Unique role of cardiovascular magnetic resonance imaging parametric mapping in the diagnosis of arrhythmogenic left ventricular cardiomyopathy. Eur Heart J Cardiovasc Imaging 22:e96

    Article  PubMed  Google Scholar 

  31. PerazzoloMarra M, Cipriani A, Rizzo S et al (2021) Myocardial tissue characterization in arrhythmogenic cardiomyopathy: comparison between endomyocardial biopsy and cardiac magnetic resonance. JACC Cardiovasc Imaging 14:1675–1678

    Article  Google Scholar 

Download references

Funding

Supported by the National Natural Science Foundation of China (No. 82171884); and Shanghai Jiao Tong University Medical Engineering Cross Project (No. YG2022QN016).

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Authors

Corresponding authors

Correspondence to Lei Zhao or Lian-Ming Wu.

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Guarantor

The scientific guarantor of this publication is Lian-Ming Wu.

Conflict of interest

The authors state that there neither exists a conflict of interest nor that there is financial information to disclose.

Statistics and biometry

Lian-Ming Wu kindly provided statistical advice for this manuscript.

Informed consent

Written informed consent was obtained from all participants in this study.

Ethical approval

Institutional Review Board approval was obtained. The CMR study protocol was approved by each of the institutional ethics committees (Shanghai Renji Hospital, Beijing Anzhen Hospital, and Fujian Longyan First Hospital) and was conducted according to the Declaration of Helsinki.

Study subjects or cohorts overlap

Study subjects or cohorts have not been previously reported.

Methodology

• prospective

• observational

• multicenter study

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Chen, BH., Jiang, WY., Zheng, JY. et al. Prognostic value of right ventricular trabecular complexity in patients with arrhythmogenic cardiomyopathy. Eur Radiol (2024). https://doi.org/10.1007/s00330-023-10561-y

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