Prognostic Value of Tpeak–Tend Interval in Early Diagnosis of Duchenne Muscular Dystrophy Cardiomyopathy
Abstract
:1. Introduction
2. Materials and Methods
Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- McNally, E.M.; Kaltman, J.R.; Benson, D.W.; Canter, C.E.; Cripe, L.H.; Duan, D.; Finder, J.D.; Groh, W.J.; Hoffman, E.P.; Judge, D.P.; et al. Working Group of the National Heart, Lung, and Blood Institute; Parent Project Muscular Dystrophy. Contemporary cardiac issues in Duchenne muscular dystrophy. Circulation 2015, 131, 1590–1598. [Google Scholar] [CrossRef] [Green Version]
- Romitti, P.A.; Zhu, Y.; Puzhankara, S.; James, K.A.; Nabukera, S.K.; Zamba, G.K.; Ciafaloni, E.; Cunniff, C.; Druschel, C.M.; Mathews, K.D.; et al. MD STARnet. Prevalence of Duchenne and Becker muscular dystrophies in the United States. Pediatrics 2015, 135, 513–521. [Google Scholar] [CrossRef] [Green Version]
- Ryder, S.; Leadley, R.M.; Armstrong, N.; Westwood, M.; de Kock, S.; Butt, T.; Jain, M.; Kleijnen, J. The burden, epidemiology, costs and treatment for Duchenne muscular dystrophy: An evidence review. Orphanet J. Rare Dis. 2017, 12, 79. [Google Scholar] [PubMed] [Green Version]
- Yiu, E.M.; Kornberg, A.J. Duchenne muscular dystrophy. J. Paediatr. Child. Health 2015, 51, 759–764. [Google Scholar] [PubMed] [Green Version]
- Earl, C.C.; Pyle, V.I.; Clark, S.Q.; Annamalai, K.; Torres, P.A.; Quintero, A.; Damen, F.W.; Hor, K.N.; Markham, L.W.; Soslow, J.H.; et al. Localized strain characterization of cardiomyopathy in Duchenne muscular dystrophy using novel 4D kinematic analysis of cine cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 2023, 25, 14. [Google Scholar] [PubMed]
- Maforo, N.G.; Magrath, P.; Moulin, K.; Shao, J.; Kim, G.H.; Prosper, A.; Renella, P.; Wu, H.H.; Halnon, N.; Ennis, D.B. T1-Mapping and extracellular volume estimates in pediatric subjects with Duchenne muscular dystrophy and healthy controls at 3T. J. Cardiovasc. Magn. Reson. 2020, 22, 85. [Google Scholar]
- Romfh, A.; McNally, E.M. Cardiac assessment in duchenne and becker muscular dystrophies. Curr. Heart Fail. Rep. 2010, 7, 212–218. [Google Scholar] [CrossRef]
- Chenard, A.A.; Becane, H.M.; Tertrain, F.; de Kermadec, J.M.; Weiss, Y.A. Ventricular arrhythmia in Duchenne muscular dystrophy: Prevalence, significance and prognosis. Neuromuscul. Disord. 1993, 3, 201–206. [Google Scholar]
- Yanagisawa, A.; Miyagawa, M.; Yotsukura, M.; Tsuya, T.; Shirato, C.; Ishihara, T.; Aoyagi, T.; Ishikawa, K. The prevalence and prognostic significance of arrhythmias in Duchenne type muscular dystrophy. Am. Heart J. 1992, 124, 1244–1250. [Google Scholar] [CrossRef]
- You, C.X.; Liu, C.F. Premature Ventricular Contractions and Cardiomyopathy. Cardiol. Rev. 2019, 27, 322–326. [Google Scholar] [CrossRef]
- Duffee, D.F.; Shen, W.K.; Smith, H.C. Suppression of frequent premature ventricular contractions and improvement of left ventricular function in patients with presumed idiopathic dilated cardiomyopathy. Mayo Clin. Proc. 1998, 73, 430–433. [Google Scholar] [CrossRef]
- Ruberman, W.; Weinblatt, E.; Goldberg, J.D.; Frank, C.W.; Chaudhary, B.S.; Shapiro, S. Ventricular premature complexes and sudden death after myocardial infarction. Circulation 1981, 64, 297–305. [Google Scholar] [CrossRef] [Green Version]
- Chua, K.C.; Nair, S.G.; Chugh, S.S. Risk markers of sudden death on the 12-lead ECG: Tpeak-Tend interval makes the cut. Heart Rhythm. 2015, 12, 1798–1799. [Google Scholar] [CrossRef] [PubMed]
- Panikkath, R.; Reinier, K.; Uy-Evanado, A.; Teodorescu, C.; Hattenhauer, J.; Mariani, R.; Gunson, K.; Jui, J.; Chugh, S.S. Prolonged Tpeak-to-tend interval on the resting ECG is associated with increased risk of sudden cardiac death. Circ. Arrhythm. Electrophysiol. 2011, 4, 441–447. [Google Scholar] [CrossRef] [Green Version]
- Tse, G.; Yan, B.P. Traditional and novel electrocardiographic conduction and repolarization markers of sudden cardiac death. Europace 2017, 19, 712–721. [Google Scholar] [PubMed]
- Castro Hevia, J.; Antzelevitch, C.; Tornés Bárzaga, F.; Dorantes Sánchez, M.; Dorticós Balea, F.; Zayas Molina, R.; Quiñones Pérez, M.A.; Fayad Rodríguez, Y. Tpeak-Tend and Tpeak-Tend dispersion as risk factors for ventricular tachycardia/ventricular fibrillation in patients with the Brugada syndrome. J. Am. Coll. Cardiol. 2006, 47, 1828–1834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kors, J.A.; Ritsema van Eck, H.J.; van Herpen, G. The meaning of the Tp-Te interval and its diagnostic value. J. Electrocardiol. 2008, 41, 575–580. [Google Scholar]
- Tse, G.; Chan, Y.W.F.; Keung, W.; Yan, B.P. Electrophysiological mechanisms of long and short QT syndromes. Int. J. Cardiol. Heart Vasc. 2016, 14, 8–13. [Google Scholar]
- Mitchell, C.; Rahko, P.S.; Blauwet, L.A.; Canaday, B.; Finstuen, J.A.; Foster, M.C.; Horton, K.; Ogunyankin, K.O.; Palma, R.A.; Velazquez, E.J. Guidelines for Performing a Comprehensive Transthoracic Echocardiographic Examination in Adults: Recommendations from the American Society of Echocardiography. J. Am. Soc. Echocardiogr. 2019, 32, 1–64. [Google Scholar]
- Barber, B.J.; Andrews, J.G.; Lu, Z.; West, N.A.; Meaney, F.J.; Price, E.T.; Gray, A.; Sheehan, D.W.; Pandya, S.; Yang, M.; et al. Oral corticosteroids and onset of cardiomyopathy in Duchenne muscular dystrophy. J. Pediatr. 2013, 163, 1080–1084. [Google Scholar]
- Shirokova, N.; Niggli, E. Cardiac phenotype of Duchenne Muscular Dystrophy: Insights from cellular studies. J. Mol. Cell Cardiol. 2013, 58, 217–224. [Google Scholar] [PubMed] [Green Version]
- Van Ruiten, H.J.; Marini Bettolo, C.; Cheetham, T.; Eagle, M.; Lochmuller, H.; Straub, V.; Bushby, K.; Guglieri, M. Why are some patients with Duchenne muscular dystrophy dying young: An analysis of causes of death in North East England. Eur. J. Paediatr. Neurol. 2016, 20, 904–909. [Google Scholar] [CrossRef] [PubMed]
- Schade van Westrum, S.M.; Hoogerwaard, E.M.; Dekker, L.; Standaar, T.S.; Bakker, E.; Ippel, P.F.; Oosterwijk, J.C.; Majoor-Krakauer, D.F.; van Essen, A.J.; Leschot, N.J.; et al. Cardiac abnormalities in a follow-up study on carriers of Duchenne and Becker muscular dystrophy. Neurology 2011, 77, 62–66. [Google Scholar] [CrossRef] [PubMed]
- Chiang, D.Y.; Allen, H.D.; Kim, J.J.; Valdes, S.O.; Wang, Y.; Pignatelli, R.H.; Lotze, T.E.; Miyake, C.Y. Relation of Cardiac Dysfunction to Rhythm Abnormalities in Patients With Duchenne or Becker Muscular Dystrophies. Am. J. Cardiol. 2016, 117, 1349–1354. [Google Scholar] [CrossRef] [PubMed]
- Perloff, J.K. Cardiac rhythm and conduction in Duchenne's muscular dystrophy: A prospective study of 20 patients. J. Am. Coll. Cardiol. 1984, 3, 1263–1268. [Google Scholar]
- Sanyal, S.K.; Johnson, W.W.; Thapar, M.K.; Pitner, S.E. An ultrastructural basis for electrocardiographic alterations associated with Duchenne's progressive muscular dystrophy. Circulation 1978, 57, 1122–1129. [Google Scholar] [CrossRef] [Green Version]
- Tang, L.; Shao, S.; Wang, C. Electrocardiographic features of children with Duchenne muscular dystrophy. Orphanet J. Rare Dis. 2022, 17, 320. [Google Scholar]
- Villa, C.R.; Czosek, R.J.; Ahmed, H.; Khoury, P.R.; Anderson, J.B.; Knilans, T.K.; Jefferies, J.L.; Wong, B.; Spar, D.S. Ambulatory Monitoring and Arrhythmic Outcomes in Pediatric and Adolescent Patients With Duchenne Muscular Dystrophy. J. Am. Heart Assoc. 2015, 5, e002620. [Google Scholar] [CrossRef] [Green Version]
- Cheeran, D.; Khan, S.; Khera, R.; Bhatt, A.; Garg, S.; Grodin, J.L.; Morlend, R.; Araj, F.G.; Amin, A.A.; Thibodeau, J.T.; et al. Predictors of Death in Adults With Duchenne Muscular Dystrophy-Associated Cardiomyopathy. J. Am. Heart Assoc. 2017, 6, e006340. [Google Scholar] [CrossRef] [Green Version]
- Menon, S.C.; Etheridge, S.P.; Liesemer, K.N.; Williams, R.V.; Bardsley, T.; Heywood, M.C.; Puchalski, M.D. Predictive value of myocardial delayed enhancement in Duchenne muscular dystrophy. Pediatr. Cardiol. 2014, 35, 1279–1285. [Google Scholar] [CrossRef]
- Karaman, K.; Altunkaş, F.; Çetin, M.; Karayakali, M.; Arısoy, A.; Akar, I.; Zencir, C.; Aygüç, B.; Çelik, A. New markers for ventricular repolarization in coronary slow flow: Tp-e interval, Tp-e/QT ratio, and Tp-e/QTc ratio. Ann. Noninvasive Electrocardiol. 2015, 20, 338–344. [Google Scholar] [CrossRef] [PubMed]
- Gupta, P.; Patel, C.; Patel, H.; Narayanaswamy, S.; Malhotra, B.; Green, J.T.; Yan, G.X. T(p-e)/QT ratio as an index of arrhythmogenesis. J. Electrocardiol. 2008, 41, 567–574. [Google Scholar] [CrossRef] [PubMed]
- Erikssen, G.; Liestol, K.; Gullestad, L.; Haugaa, K.H.; Bendz, B.; Amlie, J.P. The terminal part of the QT interval (T peak to T end): A predictor of mortality after acute myocardial infarction. Ann. Noninvasive Electrocardiol. 2012, 17, 85–94. [Google Scholar] [CrossRef] [PubMed]
- Morin, D.P.; Saad, M.N.; Shams, O.F.; Owen, J.S.; Xue, J.Q.; Abi-Samra, F.M.; Khatib, S.; Nelson-Twakor, O.S.; Milani, R.V. Relationships between the T-peak to T-end interval, ventricular tachyarrhythmia, and death in left ventricular systolic dysfunction. Europace 2012, 14, 1172–1179. [Google Scholar] [PubMed]
- Rosenthal, T.M.; Stahls, P.F., 3rd; Abi Samra, F.M.; Bernard, M.L.; Khatib, S.; Polin, G.M.; Xue, J.Q.; Morin, D.P. T-peak to T-end interval for prediction of ventricular tachyarrhythmia and mortality in a primary prevention population with systolic cardiomyopathy. Heart Rhythm. 2015, 12, 1789–1797. [Google Scholar]
- Adali, M.K.; Davutoglu, Y.; Yilmaz, S. The relationship between premature ventricular complexes and index of cardiac-electrophysiological balance. Rev. Assoc. Med. Bras. 2023, 69, 142–146. [Google Scholar]
- Söylemez, N.; Yaman, B. Association between ventricular premature contraction burden and ventricular repolarization duration. Rev. Assoc. Med. Bras. 2022, 68, 1571–1575. [Google Scholar]
- Antzelevitch, C.; Sicouri, S.; Di Diego, J.M.; Burashnikov, A.; Viskin, S.; Shimizu, W.; Yan, G.X.; Kowey, P.; Zhang, L. Does Tpeak-Tend provide an index of transmural dispersion of repolarization? Heart Rhythm. 2007, 4, 1114–1116. [Google Scholar] [CrossRef] [Green Version]
- Tse, G.; Gong, M.; Wong, W.T.; Georgopoulos, S.; Letsas, K.P.; Vassiliou, V.S.; Chan, Y.S.; Yan, B.P.; Wong, S.H.; Wu, W.K.K.; et al. The Tpeak—Tend interval as an electrocardiographic risk marker of arrhythmic and mortality outcomes: A systematic review and meta-analysis. Heart Rhythm. 2017, 14, 1131–1137. [Google Scholar]
- Antzelevitch, C.; Di Diego, J.M. Tpeak-Tend interval as a marker of arrhythmic risk. Heart Rhythm. 2019, 16, 954–955. [Google Scholar]
- Jaromin, J.; Markiewicz-Łoskot, G.; Szydłowski, L.; Kulawik, A. Diagnostic Value of the TpTe Interval in Children with Ventricular Arrhythmias. Int. J. Environ. Res. Public. Health 2021, 18, 12194. [Google Scholar] [CrossRef]
- Salles, G.F.; Cardoso, C.R.; Xavier, S.S.; Sousa, A.S.; Hasslocher-Moreno, A. Electrocardiographic ventricular repolarization parameters in chronic Chagas' disease as predictors of asymptomatic left ventricular systolic dysfunction. Pacing Clin. Electrophysiol. 2003, 26, 1326–1335. [Google Scholar] [CrossRef] [PubMed]
- Sicouri, S.; Antzelevitch, C. A subpopulation of cells with unique electrophysiological properties in the deep subepicardium of the canine ventricle. The M cell. Circ. Res. 1991, 68, 1729–1741. [Google Scholar] [CrossRef] [PubMed]
- Jimenez-Vazquez, E.N.; Arad, M.; Macías, Á.; Vera-Pedrosa, M.L.; Cruz, F.M.; Gutierrez, L.K.; Cuttita, A.J.; Monteiro da Rocha, A.; Herron, T.J.; Ponce-Balbuena, D.; et al. SNTA1 gene rescues ion channel function and is antiarrhythmic in cardiomyocytes derived from induced pluripotent stem cells from muscular dystrophy patients. Elife 2022, 11, e76576. [Google Scholar] [CrossRef] [PubMed]
- Petitprez, S.; Zmoos, A.F.; Ogrodnik, J.; Balse, E.; Raad, N.; El-Haou, S.; Albesa, M.; Bittihn, P.; Luther, S.; Lehnart, S.E.; et al. SAP97 and dystrophin macromolecular complexes determine two pools of cardiac sodium channels Nav1.5 in cardiomyocytes. Circ. Res. 2011, 108, 294–304. [Google Scholar] [CrossRef] [PubMed]
- Koenig, X.; Rubi, L.; Obermair, G.J.; Cervenka, R.; Dang, X.B.; Lukacs, P.; Kummer, S.; Bittner, R.E.; Kubista, H.; Todt, H.; et al. Enhanced currents through L-type calcium channels in cardiomyocytes disturb the electrophysiology of the dystrophic heart. Am. J. Physiol. Heart Circ. Physiol. 2014, 306, H564–H573. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miyoshi, K. Echocardiographic evaluation of fibrous replacement in the myocardium of patients with Duchenne muscular dystrophy. Br. Heart J. 1991, 66, 452–455. [Google Scholar] [CrossRef]
Control Group (n = 27) | DMD, PVC < 1% Group 1 (n = 15) | DMD, PVC > 1% Group 2 (n = 10) | p-Value | |
---|---|---|---|---|
Age (years) | 13.2 ± 5 | 11.7 ± 4.5 | 14.6 ± 4.08 | 0.214 K |
BMI (kg/m2) | 25.7 ± 3.3 | 26.3 ± 6.6 | 26.9 ± 6.8 | 0.427 K |
Echocardiography | ||||
LVEF (%) | 67.6 ± 2.7 x,y | 59.9 ± 8.9 x,z | 50.5 ± 14.4 y,z | <0.001 A |
LVEDD (mm) | 41.0 ± 6.3 y | 43.7 ± 6.2 z | 50.4 ± 8.9 y,z | 0.005 A |
IVSd (mm) | 8.5 ± 1.2 x,y | 6.8 ± 0.8 x | 6.5 ± 0.6 y | <0.001 K |
PWd (mm) | 8.6 ± 1.1 x,y | 6.7 ± 0.7 x | 6.8 ± 0.5 y | <0.001 K |
Cardiac biomarkers | ||||
Pro-BNP (pg/mL) | 449 ± 18.3 x,y | 197.3 ± 235.1 x | 437.3 ± 574.8 y | 0.001 K |
Hs-Troponin (pg/mL) | 3.1 ± 1 x,y | 62.9 ± 51.2 x | 98.2 ± 32.1 y | <0.001 K |
Electrocardiography | ||||
PR interval (ms) | 140.9 ± 17.6 x,y | 117.5 ± 14.7 x | 124.2 ± 19.4 y | <0.001 K |
QRS duration (ms) | 95.3 ± 12.7 | 87.3 ± 5.7 | 94.4 ± 7.1 | 0.067 K |
QTc interval (ms) | 396.2 ± 14.9 x,y | 415.0 ± 19.9 x | 431.0 ± 20.4 y | <0.001 K |
Tp-e interval (ms) | 62.7 ± 2.8 y | 68.8 ± 7.8 z | 80.7 ± 18.9 y,z | <0.001 K |
24 h Holter monitoring | ||||
Max HR (bpm) | 159.0 ± 21.2 | 156.5 ± 12.7 | 149.0 ± 21.8 | 0.516 K |
Min HR (bpm) | 51.3 ± 12.8 | 56.9 ± 6.5 | 55.4 ± 6.9 | 0.222 A |
Average HR (bpm) | 84.3 ± 16.6 x,y | 91.9 ± 12.4 x | 92.9 ± 12.9 y | 0.016 K |
PVC per 24 h | 87.7 (0–1213) y | 218.2 (0–917) z | 5166.8 (1050–19,500) y,z | <0.001 K |
Couplets per 24 h | 0 ± 0 y | 0 ± 0 z | 5.4 ± 8.8 y,z | <0.001 K |
Triplets per 24 h | 0 ± 0 | 0 ± 0 | 1 ± 1 |
Variables | Tpeak–Tend | PVC | ||
---|---|---|---|---|
r | p-Value | r | p-Value | |
LVEF % | −0.312 | 0.024 * | −0.346 | 0.012 * |
LVEDD (mm) | 0.115 | 0.415 | 0.407 | 0.003 * |
Pro-BNP | 0.571 | <0.001 * | 0.353 | 0.038 * |
Hs-Troponin | 0.446 | 0.007 * | 0.623 | <0.001 * |
PR interval (ms) | −0.247 | 0.077 | –0.083 | 0.561 |
QRS duration (ms) | −0.224 | 0.110 | 0.106 | 0.453 |
QTc interval (ms) | 0.432 | 0.001 * | 0.459 | <0.001 * |
Tp-Te | — | — | 0.400 | 0.003 * |
PVC | 0.400 | 0.003 * | — | — |
Maximum HR | 0.002 | 0.990 | –0.102 | 0.471 |
Minimum HR | 0.266 | 0.057 | 0.170 | 0.229 |
Average HR | 0.267 | 0.056 | 0.245 | 0.080 |
Univariate Regression | Multivariate Regression | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
OR | %95 CI | p-Value | OR | %95 CI | p-Value | |||||
LVEF % | 0.879 | 0.812 | - | 0.953 | 0.002 * | 0.879 | 0.812 | - | 0.953 | 0.002 * |
Tp-e | 1.195 | 1.068 | - | 1.336 | 0.002 * | 1.181 | 1.047 | - | 1.332 | 0.007 * |
QTc | 1.088 | 1.027 | - | 1.153 | 0.004 * | |||||
LVEDD | 1.210 | 1.040 | - | 1.408 | 0.014 * | |||||
Pro-BNP | 1.002 | 1.000 | - | 1.005 | 0.074 | |||||
Hs-Troponin | 1.025 | 1.006 | - | 1.044 | 0.010 * | |||||
PR interval | 0.977 | 0.939 | - | 1.016 | 0.240 | |||||
QRS duration | 1.017 | 0.954 | - | 1.085 | 0.603 |
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Baskan, S.; Karaca Ozer, P.; Orta, H.; Ozbingol, D.; Yavuz, M.L.; Ayduk Govdeli, E.; Nisli, K.; Oztarhan, K. Prognostic Value of Tpeak–Tend Interval in Early Diagnosis of Duchenne Muscular Dystrophy Cardiomyopathy. Diagnostics 2023, 13, 2381. https://doi.org/10.3390/diagnostics13142381
Baskan S, Karaca Ozer P, Orta H, Ozbingol D, Yavuz ML, Ayduk Govdeli E, Nisli K, Oztarhan K. Prognostic Value of Tpeak–Tend Interval in Early Diagnosis of Duchenne Muscular Dystrophy Cardiomyopathy. Diagnostics. 2023; 13(14):2381. https://doi.org/10.3390/diagnostics13142381
Chicago/Turabian StyleBaskan, Serra, Pelin Karaca Ozer, Huseyin Orta, Doruk Ozbingol, Mustafa Lutfi Yavuz, Elif Ayduk Govdeli, Kemal Nisli, and Kazim Oztarhan. 2023. "Prognostic Value of Tpeak–Tend Interval in Early Diagnosis of Duchenne Muscular Dystrophy Cardiomyopathy" Diagnostics 13, no. 14: 2381. https://doi.org/10.3390/diagnostics13142381