- Email: [email protected]
False tendons may be associated with the genesis of J-waves
International Journal of Cardiology 172 (2014) 428–433
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
False tendons may be associated with the genesis of J-waves Prospective study in young healthy male Mikiko Nakagawa ⁎, Kaori Ezaki, Hiroko Miyazaki, Yuki Ebata, Tetsuji Shinohara, Yasushi Teshima, Kunio Yufu, Naohiko Takahashi, Tetsunori Saikawa Department of Cardiology and Clinical Examination, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Yufu City, Oita 879–5593, Japan
a r t i c l e
i n f o
Article history: Received 29 October 2013 Received in revised form 20 December 2013 Accepted 19 January 2014 Available online 25 January 2014 Keywords: False tendon J-wave Electrocardiogram Echocardiogram
a b s t r a c t Background: Recent studies showed that J-waves are associated with vulnerability to ventricular fibrillation. Recently we reported the association between false tendons (FTs) and J-waves in a retrospective study. Methods and results: We prospectively studied 50 young healthy men (mean age 24.6 ± 2.7 years). FTs were detected echocardiographically and classified based on their points of attachment as type 1 (longitudinal type), type 2 (diagonal type), and type 3 (transverse type). J-waves were defined as terminal QRS notching or slurring with ≥0.1 mV. The filtered QRS duration (fQRSd), RMS40, and LAS40 were measured on signal-averaged ECGs. FTs were detected in 37 of the 50 subjects (74%). The incidence of J-waves was significantly higher in subjects with type 1 or type 2 FTs than those with no- or type 3 FTs (61% vs. 26%, p b 0.05). The leads with J-waves were closely associated with the location of the FT. While no late potential was recorded in any study subjects, fQRSd and LAS40 were significantly longer in subjects with type 1 or type 2 FTs (p b 0.05). Univariate and multivariate logistic regression analysis revealed that only the existence of FTs (type 1 or 2) was an independent predictor of the presence of J-waves. Conclusions: Our results suggest that FTs were related to the genesis of J-waves with conduction delay. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The J-wave is characterized by a slurring or notching at the termination of the QRS complex on electrocardiograms (ECG). The electrophysiological mechanisms underlying the manifestation of J-waves remain unclear. While J-waves, especially in the inferior or lateral leads, have been reported to be associated with vulnerability to ventricular fibrillation, they were present in the same leads in healthy individuals [1–9]. The false tendon (FT) is a discrete, fibromuscular structure that traverses the left ventricular (LV) cavity. As FTs may be arrhythmogenic, they are the target of radiofrequency ablation in patients with ventricular arrhythmias [10–13]. FTs are present in approximately 50% of human hearts [14–16]. Some FTs contain longitudinal conduction tissues [15–17] suggesting that some types of FT are a continuation of His bundle-like conduction tissues and that they contribute to the occurrence of ventricular arrhythmias. Under the hypothesis that FTs play a role in the genesis of J-waves, in an earlier retrospective study we investigated the relationship between FTs and J-waves [18]. We demonstrated that the incidence of J-waves was significantly higher in patients with than without FTs. Ours was ⁎ Corresponding author. Tel.: +81 97 586 5962; fax: +81 97 586 6059. E-mail address: [email protected] (M. Nakagawa). 0167-5273/$ – see front matter © 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijcard.2014.01.101
the first evidence for a possible association between FTs and the genesis of J-waves. However, that study was retrospective and the clinical background of the study population was not uniform. Therefore, to confirm our hypothesis we carried out a prospective study using the signalaveraged ECG (SAECG) values of only young healthy men. 2. Methods 2.1. Study population We enrolled 50 healthy male volunteers whose mean age was 24.6 ± 2.7 years. Their medical histories were unremarkable, none were on medications, and their physical examination, biochemical profiles, 12-lead ECGs, echocardiograms, and chest X-rays were normal. We included only subjects whose transthoracic echocardiographic visualization was adequate for the detection of FTs. Their basic characteristics including the body height and weight and the body mass index (weight/height2 (kg/m2)) were recorded. The subjects who regularly (more than 3 times/week) performed physical exercises were defined as the athletes. Our study was approved by the Ethics Committee of Oita University and all participants provided prior informed consent. 2.2. Echocardiographic study All echocardiograms were acquired on a Vivid 7 echocardiography system (GE Healthcare UK Ltd, Buckinghamshire, England) with an M3S probe. All studies included standard parasternal long and short axis, apical 2, 3, and 4 chamber, and subcostal views. To determine the FT orientation and insertion points we also recorded off-axis
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433 parasternal and apical views. All echocardiographic images were stored on digitally visualized disks and reviewed by 2 echocardiography experts (blinded to ECG findings). The presence of FTs and their type were independently recorded by the 2 experts and only if both reviewers achieved a consensus of the results, the subjects were enrolled in this study. The FTs were defined as linear cordlike fibromuscular structures that crossed the LV cavity without attachment to the mitral valve leaflets. The thickness of the FT was measured at the thickest portion on any views in each subject. The FTs were classified into 3 types based on the points of attachment (Fig. 1). Type 1 was connected at the basal septum and the posteromedial papillary muscle (PM) or the apical free wall (longitudinal type), type 2 was at the mid septum and anterolateral PM or apical free wall (diagonal type), and type 3 was located between the apical septum and the lateral free wall (transverse type). In cases with plural FTs, the thickest was used for the type-classification. The dimensions and ejection fraction of the LV were also measured on the parasternal long-axis view in each subject. Based on our earlier findings [18] we divided the study subjects into 2 groups according to the presence or absence of FTs and the FT type. Group 1 (n = 31) manifested type 1 or type 2 FTs. Group 2 (n = 19) had no or type 3 FTs. Between group 1 and group 2 there were no significant differences in the age (24.6 ± 2.9, 24.6 ± 2.5 years), body height (172.2 ± 5.9, 171.4 ± 4.8 cm), body weight (64.9 ± 6.9, 67.8 ± 12.3 kg), body mass index (21.9 ± 1.9, 23.0 ± 3.5 kg/m2), and the proportion of the athletes (51.6, 52.6%). There were no significant differences in all echocardiographic parameters except for the FTs between 2 groups.
429
Signal-averaged electrocardiographs (SAECG) were recorded using the modified bipolar leads (X, Y and Z) of Cardio Star (FCP-7541, Fukuda Denshi, Tokyo, Japan) and measured with a commercially available program (FP-705LP, Fukuda Denshi). Sampling frequency was 8000 Hz with 18 bit resolution. Signal averaging was performed on data obtained from 300 beats and filtered with a band-pass filter between 40 and 300 Hz. The filtered QRS duration (fQRSd), the root-mean-square voltage of the terminal 40 ms of the filtered QRS complex (RMS40), and the duration of low-amplitude signals (b40 μV) in the terminal filtered QRS complex (LAS40) were measured. The QRS onset and offset were determined by a computer algorithm. The computer-determined QRS offset point was confirmed visually and if it was incorrect, the actual QRS offset point was determined manually. Late potentials were considered positive when 2 of 3 criteria (fQRSd N 135 ms, RMS40 b 15.0 μV, LAS40 N 39 ms) were met.
2.4. Statistical analysis Data are presented as the mean ± SD. We used two-way analysis of variance (ANOVA) followed by the Bonferroni post-hoc and unpaired t-test to evaluate differences between the groups for each parameter. Discrete variables were analyzed by the χ2 test. Univariate and multivariate logistic regression analysis was performed to identify independent predictors of the presence of J-waves. A p value of b0.05 was considered statistically significant.
2.3. Electrocardiographic study
3. Results
With the subject resting in supine position, standard 12-lead surface digital ECGs were recorded using Cardiofax (Nihon Kohden, Tokyo, Japan) with a 100 Hz low-pass filter. Signals were digitized with 1.25 μV resolution and a range of 16 bits. The PQ, QRS, QT, and JT intervals were automatically measured on each ECG using a commercially available program (ECAPS12C, Nihon Kohden). The rate-corrected QT and JT intervals (QTc, JTc) were calculated using the Fridericia formula [19] where QTc = QT/ RR1/3 and JTc = JT/RR1/3. J-waves were defined as either notching (a positive deflection) or slurring (a smooth transition from the QRS to the ST segment) with an amplitude of ≥0.1 mV on the terminal QRS portion in at least two of the inferior (II, III, aVF) or the lateral leads (I, aVL, and V4 through V6).
3.1. False tendons and J-waves We observed FTs in 37 of our 50 subjects (74%); 17 manifested type 1, 14 type 2, and 6 type 3. J-waves were present in 24 subjects (48%). The J-wave location was recorded as inferior lead only, lateral lead only, and both leads. Among the 24 subjects with J-waves, 15 (62.5%) had J-waves in the inferior lead only, in 3 (12.5%) they were observed in the lateral lead only, and in 6 (25%) they were seen in both leads.
Fig. 1. Echocardiographic types of false tendons. Type 1 (longitudinal type) is connected at the basal septum and the posteromedial papillary muscle (PM) or the apical free wall (A). Type 2 (diagonal type) is connected at the mid-septum and the anterolateral PM or the apical free wall (B). Type 3 (transverse type) is located between the apical septum and the lateral free wall (C). False tendons are the red lines in the illustration. On the echocardiogram they are identified by the arrowhead.
430
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
Figs. 2 and 3 show the 12-lead ECG recordings, the echocardiograms, and the SAECGs from a 23- and a 31-year-old man, respectively. The incidence and location of the J-waves based on the FT type were shown in Table 1 and Fig. 4. Both depended significantly on the FT type (p b 0.05). The incidence of J-waves in subjects with 1-, 2- and 3-type FTs (n = 37) was 64.7%, 57.1%, and 33.3%, respectively. When we classified the FTs as thick (≥2 mm) and thin (b 2 mm) we found that the incidence of J-waves was significantly higher (p b 0.05) in subjects with thick (n = 29, 65.5%) than thin FTs (n = 8, 25%).
3.2. Comparison of electrocardiographic findings In Table 2 we compare the electrocardiographic characteristics of the 2 subject groups (group 1 = type 1 or type 2 FTs, group 2 = type 3 or no FTs). There were no significant differences in the heart rate, PR interval, QRS duration, and the QTc and JTc intervals obtained from 12-lead ECGs. However, the incidence of J-waves was significantly higher in group 1
(61%) than group 2 (26%) (p b 0.05). On the other hand, fQRSd and LAS40 obtained from SAECG data were significantly longer in group 1 (p b 0.05). We did not record late potentials in any of the 50 subjects. Fig. 5 shows the fQRSd and LAS40 based on the FT type. Both fQRSd and LAS40 were significantly longer in subjects with type 1 and type 2 FTs (group 1) than in subjects with type 3 FTs (group 2).
3.3. Univariate and multivariate logistic regression analysis The results of univariate and multivariate logistic regression analyses for the presence of J-waves are shown in Table 3. Univariate analysis using the body height and weight, the body mass index, the exercise custum (athlete), and the presence of FTs of type 1 or type 2 revealed that only the presence of FTs was associated with J-waves. Subsequent multivariate analysis using the same factors showed that only the existence of FTs was an independent predictor of the presence of J-waves (odds ratio 6.286, 95% confidence interval 1.504–26.266, p = 0.012).
Fig. 2. ECGs and echocardiogram of a 23-year-old man. (A) Twelve-lead ECG recording, (B) echocardiogram, and (C) SAECG. J-waves are seen in the inferior leads (II, III, aVF) (red arrows, A). The echocardiogram shows a thick, type 1 false tendon measuring 4.2 mm in diameter (arrow heads, B). On SAECG there is a J-wave only in lead Y (red arrow, C) and late potential was not recorded.
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
431
Fig. 3. ECGs and echocardiogram of a 31-year-old man. (A) Twelve-lead ECG recording, (B) echocardiogram, and (C) SAECG (C). J-waves are seen in the lateral leads (I, aVL, and V4 through V6) (red arrows, A). The echocardiogram reveals 3 thick, type 2 false tendons measuring 4.6 mm in maximum diameter (arrow heads, B). On SAECG there is a J-wave only in lead X (red arrow, C) and late potential was not recorded.
The sensitivity and the specificity of the presence of FTs of type 1 or type 2 for the prediction of the genesis of J-waves were 79% and 54%, respectively.
Table 1 Relationship between types of false tendon and J-wave locations. False tendon
Type 1 Type 2 Type 3 No FT Total
Location of J-waves Inferior
Lateral
Both
10 2 2 1 15
0 3 0 0 3
1 3 0 2 6
Values are number of subjects. FT, false tendon.
No J-wave
Total
6 6 4 10 26
17 14 6 13 50
4. Discussion Our earlier retrospective study [18] suggested an association between FTs and the genesis of J-waves. To our knowledge, the current investigation is the first prospective study of the association between FTs and J-waves using both 12-lead ECG and SAECG data. FTs are discrete, fibromuscular structures of varying length and thickness that traverse the LV cavity. Their morphologic appearance and location in the LV cavity have been documented in autopsy studies [14–16] where the incidence of FTs was higher in males than females [14]. The rate of FTs in our young healthy male subjects was 74% and higher than in autopsy studies that included both genders (55–62%) [14,16]. Recent advances in the quality of echocardiographic images facilitate the detection of very thin FTs. In our earlier study we divided FTs into 4 types [18]. Type 1 and type 2 FTs connect the basal- or mid-septum to the PMs or to the apical free wall and tend to be thick and long. Type
432
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
Fig. 4. Types of false tendon and J-wave locations. In subjects with type 1 false tendons the J-waves were located in the inferior leads only (58.8%) or in both leads (5.9%); 35.3% had no J-waves. In subjects with type 2 false tendons the J-waves were located in the inferior leads only (14.3%), the lateral leads only (21.4%), or in both leads (24.1%); 42.9% had no Jwaves. In subjects with type 3 false tendons J-waves were located in the inferior leads only (33.3%) and the other subjects (66.7%) manifested no J-waves. In subjects with no false tendons the J-waves were observed in the inferior leads only (7.7%) or in both leads (15.4%). The other subjects (76.9%) had no J-waves.
3 FTs that connect the apical free wall to the apical septum tend to be thin and short. None of our current subjects presented with the very rare web-like type 4 FTs. The incidence of J-waves was significantly different among subjects with different FT types and different FT thickness. J-waves were seen in 64.7% and 57.1% of subjects with type 1 and type 2 FTs, respectively, and in 33.3% of those with FTs of type 3. Thus, the incidence of J-waves was significantly higher in males whose FTs were ≥2 mm than in those with thinner FTs (b2 mm). The location of the J-waves also differed with the FT type; in subjects with type 1 FTs most were located in the inferior leads. On the other hand, in males with type 2 FTs, J-waves were observed in both inferior and lateral leads; they were more prevalent in the lateral leads than in the presence of type 1 FTs. These findings were consistent with our earlier retrospective study [18]. We compared the characteristics of ECGs obtained in our two study groups. On 12-lead ECGs there was no significant difference between them in any of the measurements taken. However, the incidence of Jwaves was significantly higher in group 1 and fQRSd and LAS40 values measured on SAECG were also significantly longer in this group. In neither group did we record late potentials. We also found that fQRSd and LAS40 were significantly longer in subjects with type 1 or type 2 FTs than in those with type 3 FTs. Our observations suggest that in subjects with type 1 or type 2 FTs there is some slowing of conduction especially
Table 2 Comparison of the electrocardiographic characteristics of group 1 and 2.
12-lead ECG Heart rate (bpm) PR interval (ms) QRS duration (ms) QTc interval (s) JTc interval (s) J wave (+) SAECG fQRSd (ms) RMS40 (μV) LAS40 (ms)
Group 1 (n = 31)
Group 2 (n = 19)
p
62.3 ± 10.7 156.9 ± 14.9 100.2 ± 7.1 0.409 ± 0.018 0.308 ± 0.019 19 (61%)
67.5 ± 11.7 160.4 ± 18.9 98.4 ± 12.4 0.412 ± 0.017 0.310 ± 0.016 5 (26%)
0.116 0.468 0.523 0.620 0.751 0.016⁎
140.8 ± 9.0 46.7 ± 24.0 26.8 ± 8.5
134.8 ± 9.7 55.2 ± 24.2 20.8 ± 8.3
0.036⁎ 0.232 0.019⁎
Values are mean ± SD or number (%). fQRSd, filtered QRS duration; RAS40, root-mean-square voltage of terminal 40 ms of filtered QRS complex; LAS40, the duration of low-amplitude signals (b40 μV) in the terminal filtered QRS complex. ⁎ p b 0.05.
Fig. 5. Comparison of SAECG measurements by the false tendon type. FQRSd, filtered QRS duration; LAS40, duration of low-amplitude signals (b40 μV) in the terminal filtered QRS complex.
in the terminal portion of ventricular excitation, and that delayed activation did not manifest as late potential. J-waves, usually defined as notching or slurring at the terminal QRS complex on ECG, are present in 5%–24% of healthy populations [4,5,7,9]. Their incidence is age- and sex-dependent and they are primarily found in young males. In addition, young male athletes had a higher incidence of J-waves [5]. The present study revealed that incidence of J-waves was higher than those in previous reports [4,5,7,9]. We consider that one of the reasons of high incidence of J-wave was that our study population was composed of only young males and more than half of them were athletes. We also think that the ECG filter setting is one of the important factors to explain the difference of the incidence of J-waves because the
Table 3 Univariate and multivariate logistic regression analysis for the presence of J-waves. Variables
Body height (cm) Body weight (kg) Body mass index (kg/m2) Athlete FT (group1)
Univariate
Multivariate
p
Odds ratio
95% CI
p
0.222 0.143 0.262 0.156 0.020⁎
0.492 2.228 0.087 2.806 6.286
0.138–1.753 0.435–11.423 0.001–11.796 0.747–10.539 1.504–26.266
0.274 0.337 0.330 0.127 0.012⁎
CI, confidence interval; FT, false tendon. ⁎ p b 0.05.
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
application of a low-pass filter with a low cutoff attenuates or eliminates J-waves [20]. The use of young healthy males as the only subjects to be examined enables us to exclude the influence of various factors including age, gender, and basic diseases on the QRS morphologies in the surface ECGs. We performed logistic regression analysis and found that the presence of FTs was the only independent predictor of the elicitation of J-waves. Histologically, some FTs contain conduction tissues, suggesting that they are intracavitary radiations of the His-bundle [15–17]. An autopsy study of Loukas et al. [16]. found that 60% of FTs included conduction tissue fibers that resembled the His-bundle. They identified 3 types of FT, those located between the posteromedial or the anterolateral PM and the septum, and the web-like type; they correspond to our FTs of type 1, 2, and 4. Another FT type consists of fibromuscular bands without conduction tissue. While the electrophysiological mechanisms responsible for the generation of J-waves remain unclear, clinical and experimental evidence suggests anomalies in delayed depolarization or early repolarization [8,21–26]. Our hypothesis for the role of FTs in the genesis of J-waves is as follows. If type 1 and type 2 FTs harbor longitudinal conduction tissue similar to the His-bundle, electrical activity is conducted through the FTs from the septum toward the inferior or the lateral free wall of the LV. However, conduction may be slower in these tissues and it may be directed anatomically in the inferolateral direction, resulting in the appearance of delayed activity in the terminal portion of the QRS complex in the inferior or lateral leads of surface ECGs. This hypothesis is supported by our finding that type 1 FTs that are attached in the posteroinferior region of the LV elicited J-waves in the inferior leads while type 2 FTs that are attached at the lateral region of the LV elicited J-waves in the lateral leads. Another hypothesis states that a local repolarization gradient due to stretching or to unknown effects of Purkinje fibers may be involved in the mechanisms that elicit J-waves. 5. Limitations Our study has some limitations. First, our study population was small and composed of only healthy young males without organic heart disease or clinical evidence of ventricular arrhythmias. The mechanisms eliciting J-waves in a healthy population may be different from those involved in the genesis of pathological J-waves. Further studies are needed to investigate the relevance of our findings to the manifestation of J-waves in patients with idiopathic ventricular fibrillation [1–7,27] or other organic heart diseases such as acute myocardial infarction [28,29]. Second, we used only 2D echocardiograms to detect the FTs. Although technical advances in echocardiography have improved the visualization of cavity structures inside the ventricles, intracardiac or 3D echocardiography and magnetic resonance imaging studies are needed to precisely identify the attachment site of FTs. Third, we did not subject the FTs to histological study. We are performing investigations on human cadaveric hearts and histological studies to test our hypothesis. 6. Conclusions Our prospective study reveals a high incidence of J-waves in healthy young male subjects with FTs and documents the close association between the J-wave location and the FT type. Our findings suggest that FTs are related to the genesis of J-waves.
433
References [1] Aizawa Y, Tamura M, Chinushi M, et al. Idiopathic ventricular fibrillation and bradycardia-dependent intraventricular block. Am Heart J 1993;126:1473–4. [2] Garg A, Finneran W, Feld GK. Familial sudden cardiac death associated with a terminal QRS abnormality on surface 12-lead electrocardiogram in the index case. J Cardiovasc Electrophysiol 1998;9:642–7. [3] Shinohara T, Takahashi N, Saikawa T, Yoshimatsu H. Characterization of J wave in a patient with idiopathic ventricular fibrillation. Heart Rhythm 2006;3:1082–4. [4] Haïssaguerre M, Derval N, Sacher F, et al. Sudden cardiac arrest associated with early repolarization. N Engl J Med 2008;358:2016–23. [5] Rosso R, Kogan E, Belhassen B, et al. J-point elevation in survivors of primary ventricular fibrillation and matched control subjects: incidence and clinical significance. J Am Coll Cardiol 2008;52:1231–8. [6] Haïssaguerre M, Sacher F, Nogami A, et al. Characteristics of recurrent ventricular fibrillation associated with inferolateral early repolarization. Role of drug therapy. J Am Coll Cardiol 2009;53:612–9. [7] Tikkanen JT, Anttonen O, Junttila MJ, et al. Long-term outcome associated with early repolarization on electrocardiography. N Engl J Med 2009;361:2529–37. [8] Abe A, Ikeda T, Tsukada T, et al. Circadian variation of late potentials in idiopathic ventricular fibrillation associated with J waves: insights into alternative pathophysiology and risk stratification. Heart Rhythm 2010;7:675–82. [9] Haruta D, Matsuo K, Tsuneto A, et al. Incidence and prognostic value of early repolarization pattern in the 12-lead electrocardiogram. Circulation 2011;123:2931–7. [10] Suwa M, Yoneda Y, Nagao H, et al. Surgical correction of idiopathic paroxysmal ventricular tachycardia possibly related to left ventricular false tendon. Am J Cardiol 1989;64:1217–20. [11] Thakur RK, Klein GJ, Sivaram CA, et al. Anatomic substrate for idiopathic left ventricular tachycardia. Circulation 1996;93:497–501. [12] Merliss AD, Seifert MJ, Collins RF, et al. Catheter ablation of idiopathic left ventricular tachycardia associated with a false tendon. PACE 1996;19(12 Pt 1):2144–6. [13] Abouezzeddine O, Suleiman M, Buescher T, et al. Relevance of endocavitary structures in ablation procedures for ventricular tachycardia. J Cardiovasc Electrophysiol 2010;21:245–54. [14] Luetmer PH, Edwards WD, Seward JB, Tajik AJ. Incidence and distribution of left ventricular false tendons: an autopsy study of 483 normal human hearts. J Am Coll Cardiol 1986;8:179–83. [15] Abdulla AK, Frustaci A, Martinez JE, Florio RA, Somerville J, Olsen EG. Echocardiography and pathology of left ventricular “false tendons”. Chest 1990;98:129–32. [16] Loukas M, Louis Jr RG, Black B, Pham D, Fudalej M, Sharkees M. False tendons: an endoscopic cadaveric approach. Clin Anat 2007;20:163–9. [17] Kervancioğlu M, Ozbağ D, Kervancioğlu P, et al. Echocardiographic and morphologic examination of left ventricular false tendons in human and animal hearts. Clin Anat 2003;16:389–95. [18] Nakagawa M, Ezaki K, Miyazaki H, et al. Electrocardiographic characteristics of patients with false tendon: possible association of false tendon with J waves. Heart Rhythm 2012;9:782–8. [19] Fridericia LS. Die Systolendauer in Elektrokardiogram bei normalen Menschen und bei Herzkranken. Acta Med Scand 1920;53:469–86. [20] García-Niebla J, Serra-Autonell G. Effects of inadequate low-pass filter application. J Electrocardiol 2009;42:303–4. [21] Antzelevitch C, Yan GX. J wave syndromes. Heart Rhythm 2010;7:549–58. [22] Boineau J. The early repolarization variant—normal or a marker of heart disease in certain subjects. J Electrocardiol 2007;40:3. [23] Borggrefe M, Schimpf R. J-wave syndromes caused by repolarization or depolarization mechanisms. A debated issue among experimental and clinical electrophysiologists. J Am Coll Cardiol 2010;55:798–800. [24] Rosso R, Adler A, Halkin A, Viskin S. Risk of sudden death among young individuals with J waves and early repolarization: putting the evidence into perspective. Heart Rhythm 2011;8:923–9. [25] Antzelevitch C. Genetic, molecular and cellular mechanisms underlying the J wave syndromes. Circ J 2012;76:1054–65. [26] Nam GB. Idiopathic ventricular fibrillation, early repolarization and other J waverelated ventricular fibrillation syndromes: from an electrocardiographic enigma to an electrophysiologic dogma. Circ J 2012;76:2723–31. [27] Miyazaki H, Nakagawa M, Shin Y, et al. Comparison of autonomic J-wave modulation in patients with idiopathic ventricular fibrillation and control subjects. Circ J 2013;77:330–7. [28] Naruse Y, Tada H, Harimura Y, et al. Early repolarization is an independent predictor of occurrences of ventricular fibrillation in the very early phase of acute myocardial infarction. Circ Arrhythm Electrophysiol 2012;5:506–13. [29] Tikkanen JT, Wichmann V, Junttila J, et al. Association of early repolarization and sudden cardiac death during an acute coronary event. Circ Arrhythm Electrophysiol 2012;5:714–8.
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
False tendons may be associated with the genesis of J-waves Prospective study in young healthy male Mikiko Nakagawa ⁎, Kaori Ezaki, Hiroko Miyazaki, Yuki Ebata, Tetsuji Shinohara, Yasushi Teshima, Kunio Yufu, Naohiko Takahashi, Tetsunori Saikawa Department of Cardiology and Clinical Examination, Faculty of Medicine, Oita University, 1-1 Idaigaoka, Yufu City, Oita 879–5593, Japan
a r t i c l e
i n f o
Article history: Received 29 October 2013 Received in revised form 20 December 2013 Accepted 19 January 2014 Available online 25 January 2014 Keywords: False tendon J-wave Electrocardiogram Echocardiogram
a b s t r a c t Background: Recent studies showed that J-waves are associated with vulnerability to ventricular fibrillation. Recently we reported the association between false tendons (FTs) and J-waves in a retrospective study. Methods and results: We prospectively studied 50 young healthy men (mean age 24.6 ± 2.7 years). FTs were detected echocardiographically and classified based on their points of attachment as type 1 (longitudinal type), type 2 (diagonal type), and type 3 (transverse type). J-waves were defined as terminal QRS notching or slurring with ≥0.1 mV. The filtered QRS duration (fQRSd), RMS40, and LAS40 were measured on signal-averaged ECGs. FTs were detected in 37 of the 50 subjects (74%). The incidence of J-waves was significantly higher in subjects with type 1 or type 2 FTs than those with no- or type 3 FTs (61% vs. 26%, p b 0.05). The leads with J-waves were closely associated with the location of the FT. While no late potential was recorded in any study subjects, fQRSd and LAS40 were significantly longer in subjects with type 1 or type 2 FTs (p b 0.05). Univariate and multivariate logistic regression analysis revealed that only the existence of FTs (type 1 or 2) was an independent predictor of the presence of J-waves. Conclusions: Our results suggest that FTs were related to the genesis of J-waves with conduction delay. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The J-wave is characterized by a slurring or notching at the termination of the QRS complex on electrocardiograms (ECG). The electrophysiological mechanisms underlying the manifestation of J-waves remain unclear. While J-waves, especially in the inferior or lateral leads, have been reported to be associated with vulnerability to ventricular fibrillation, they were present in the same leads in healthy individuals [1–9]. The false tendon (FT) is a discrete, fibromuscular structure that traverses the left ventricular (LV) cavity. As FTs may be arrhythmogenic, they are the target of radiofrequency ablation in patients with ventricular arrhythmias [10–13]. FTs are present in approximately 50% of human hearts [14–16]. Some FTs contain longitudinal conduction tissues [15–17] suggesting that some types of FT are a continuation of His bundle-like conduction tissues and that they contribute to the occurrence of ventricular arrhythmias. Under the hypothesis that FTs play a role in the genesis of J-waves, in an earlier retrospective study we investigated the relationship between FTs and J-waves [18]. We demonstrated that the incidence of J-waves was significantly higher in patients with than without FTs. Ours was ⁎ Corresponding author. Tel.: +81 97 586 5962; fax: +81 97 586 6059. E-mail address: [email protected] (M. Nakagawa). 0167-5273/$ – see front matter © 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijcard.2014.01.101
the first evidence for a possible association between FTs and the genesis of J-waves. However, that study was retrospective and the clinical background of the study population was not uniform. Therefore, to confirm our hypothesis we carried out a prospective study using the signalaveraged ECG (SAECG) values of only young healthy men. 2. Methods 2.1. Study population We enrolled 50 healthy male volunteers whose mean age was 24.6 ± 2.7 years. Their medical histories were unremarkable, none were on medications, and their physical examination, biochemical profiles, 12-lead ECGs, echocardiograms, and chest X-rays were normal. We included only subjects whose transthoracic echocardiographic visualization was adequate for the detection of FTs. Their basic characteristics including the body height and weight and the body mass index (weight/height2 (kg/m2)) were recorded. The subjects who regularly (more than 3 times/week) performed physical exercises were defined as the athletes. Our study was approved by the Ethics Committee of Oita University and all participants provided prior informed consent. 2.2. Echocardiographic study All echocardiograms were acquired on a Vivid 7 echocardiography system (GE Healthcare UK Ltd, Buckinghamshire, England) with an M3S probe. All studies included standard parasternal long and short axis, apical 2, 3, and 4 chamber, and subcostal views. To determine the FT orientation and insertion points we also recorded off-axis
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433 parasternal and apical views. All echocardiographic images were stored on digitally visualized disks and reviewed by 2 echocardiography experts (blinded to ECG findings). The presence of FTs and their type were independently recorded by the 2 experts and only if both reviewers achieved a consensus of the results, the subjects were enrolled in this study. The FTs were defined as linear cordlike fibromuscular structures that crossed the LV cavity without attachment to the mitral valve leaflets. The thickness of the FT was measured at the thickest portion on any views in each subject. The FTs were classified into 3 types based on the points of attachment (Fig. 1). Type 1 was connected at the basal septum and the posteromedial papillary muscle (PM) or the apical free wall (longitudinal type), type 2 was at the mid septum and anterolateral PM or apical free wall (diagonal type), and type 3 was located between the apical septum and the lateral free wall (transverse type). In cases with plural FTs, the thickest was used for the type-classification. The dimensions and ejection fraction of the LV were also measured on the parasternal long-axis view in each subject. Based on our earlier findings [18] we divided the study subjects into 2 groups according to the presence or absence of FTs and the FT type. Group 1 (n = 31) manifested type 1 or type 2 FTs. Group 2 (n = 19) had no or type 3 FTs. Between group 1 and group 2 there were no significant differences in the age (24.6 ± 2.9, 24.6 ± 2.5 years), body height (172.2 ± 5.9, 171.4 ± 4.8 cm), body weight (64.9 ± 6.9, 67.8 ± 12.3 kg), body mass index (21.9 ± 1.9, 23.0 ± 3.5 kg/m2), and the proportion of the athletes (51.6, 52.6%). There were no significant differences in all echocardiographic parameters except for the FTs between 2 groups.
429
Signal-averaged electrocardiographs (SAECG) were recorded using the modified bipolar leads (X, Y and Z) of Cardio Star (FCP-7541, Fukuda Denshi, Tokyo, Japan) and measured with a commercially available program (FP-705LP, Fukuda Denshi). Sampling frequency was 8000 Hz with 18 bit resolution. Signal averaging was performed on data obtained from 300 beats and filtered with a band-pass filter between 40 and 300 Hz. The filtered QRS duration (fQRSd), the root-mean-square voltage of the terminal 40 ms of the filtered QRS complex (RMS40), and the duration of low-amplitude signals (b40 μV) in the terminal filtered QRS complex (LAS40) were measured. The QRS onset and offset were determined by a computer algorithm. The computer-determined QRS offset point was confirmed visually and if it was incorrect, the actual QRS offset point was determined manually. Late potentials were considered positive when 2 of 3 criteria (fQRSd N 135 ms, RMS40 b 15.0 μV, LAS40 N 39 ms) were met.
2.4. Statistical analysis Data are presented as the mean ± SD. We used two-way analysis of variance (ANOVA) followed by the Bonferroni post-hoc and unpaired t-test to evaluate differences between the groups for each parameter. Discrete variables were analyzed by the χ2 test. Univariate and multivariate logistic regression analysis was performed to identify independent predictors of the presence of J-waves. A p value of b0.05 was considered statistically significant.
2.3. Electrocardiographic study
3. Results
With the subject resting in supine position, standard 12-lead surface digital ECGs were recorded using Cardiofax (Nihon Kohden, Tokyo, Japan) with a 100 Hz low-pass filter. Signals were digitized with 1.25 μV resolution and a range of 16 bits. The PQ, QRS, QT, and JT intervals were automatically measured on each ECG using a commercially available program (ECAPS12C, Nihon Kohden). The rate-corrected QT and JT intervals (QTc, JTc) were calculated using the Fridericia formula [19] where QTc = QT/ RR1/3 and JTc = JT/RR1/3. J-waves were defined as either notching (a positive deflection) or slurring (a smooth transition from the QRS to the ST segment) with an amplitude of ≥0.1 mV on the terminal QRS portion in at least two of the inferior (II, III, aVF) or the lateral leads (I, aVL, and V4 through V6).
3.1. False tendons and J-waves We observed FTs in 37 of our 50 subjects (74%); 17 manifested type 1, 14 type 2, and 6 type 3. J-waves were present in 24 subjects (48%). The J-wave location was recorded as inferior lead only, lateral lead only, and both leads. Among the 24 subjects with J-waves, 15 (62.5%) had J-waves in the inferior lead only, in 3 (12.5%) they were observed in the lateral lead only, and in 6 (25%) they were seen in both leads.
Fig. 1. Echocardiographic types of false tendons. Type 1 (longitudinal type) is connected at the basal septum and the posteromedial papillary muscle (PM) or the apical free wall (A). Type 2 (diagonal type) is connected at the mid-septum and the anterolateral PM or the apical free wall (B). Type 3 (transverse type) is located between the apical septum and the lateral free wall (C). False tendons are the red lines in the illustration. On the echocardiogram they are identified by the arrowhead.
430
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
Figs. 2 and 3 show the 12-lead ECG recordings, the echocardiograms, and the SAECGs from a 23- and a 31-year-old man, respectively. The incidence and location of the J-waves based on the FT type were shown in Table 1 and Fig. 4. Both depended significantly on the FT type (p b 0.05). The incidence of J-waves in subjects with 1-, 2- and 3-type FTs (n = 37) was 64.7%, 57.1%, and 33.3%, respectively. When we classified the FTs as thick (≥2 mm) and thin (b 2 mm) we found that the incidence of J-waves was significantly higher (p b 0.05) in subjects with thick (n = 29, 65.5%) than thin FTs (n = 8, 25%).
3.2. Comparison of electrocardiographic findings In Table 2 we compare the electrocardiographic characteristics of the 2 subject groups (group 1 = type 1 or type 2 FTs, group 2 = type 3 or no FTs). There were no significant differences in the heart rate, PR interval, QRS duration, and the QTc and JTc intervals obtained from 12-lead ECGs. However, the incidence of J-waves was significantly higher in group 1
(61%) than group 2 (26%) (p b 0.05). On the other hand, fQRSd and LAS40 obtained from SAECG data were significantly longer in group 1 (p b 0.05). We did not record late potentials in any of the 50 subjects. Fig. 5 shows the fQRSd and LAS40 based on the FT type. Both fQRSd and LAS40 were significantly longer in subjects with type 1 and type 2 FTs (group 1) than in subjects with type 3 FTs (group 2).
3.3. Univariate and multivariate logistic regression analysis The results of univariate and multivariate logistic regression analyses for the presence of J-waves are shown in Table 3. Univariate analysis using the body height and weight, the body mass index, the exercise custum (athlete), and the presence of FTs of type 1 or type 2 revealed that only the presence of FTs was associated with J-waves. Subsequent multivariate analysis using the same factors showed that only the existence of FTs was an independent predictor of the presence of J-waves (odds ratio 6.286, 95% confidence interval 1.504–26.266, p = 0.012).
Fig. 2. ECGs and echocardiogram of a 23-year-old man. (A) Twelve-lead ECG recording, (B) echocardiogram, and (C) SAECG. J-waves are seen in the inferior leads (II, III, aVF) (red arrows, A). The echocardiogram shows a thick, type 1 false tendon measuring 4.2 mm in diameter (arrow heads, B). On SAECG there is a J-wave only in lead Y (red arrow, C) and late potential was not recorded.
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
431
Fig. 3. ECGs and echocardiogram of a 31-year-old man. (A) Twelve-lead ECG recording, (B) echocardiogram, and (C) SAECG (C). J-waves are seen in the lateral leads (I, aVL, and V4 through V6) (red arrows, A). The echocardiogram reveals 3 thick, type 2 false tendons measuring 4.6 mm in maximum diameter (arrow heads, B). On SAECG there is a J-wave only in lead X (red arrow, C) and late potential was not recorded.
The sensitivity and the specificity of the presence of FTs of type 1 or type 2 for the prediction of the genesis of J-waves were 79% and 54%, respectively.
Table 1 Relationship between types of false tendon and J-wave locations. False tendon
Type 1 Type 2 Type 3 No FT Total
Location of J-waves Inferior
Lateral
Both
10 2 2 1 15
0 3 0 0 3
1 3 0 2 6
Values are number of subjects. FT, false tendon.
No J-wave
Total
6 6 4 10 26
17 14 6 13 50
4. Discussion Our earlier retrospective study [18] suggested an association between FTs and the genesis of J-waves. To our knowledge, the current investigation is the first prospective study of the association between FTs and J-waves using both 12-lead ECG and SAECG data. FTs are discrete, fibromuscular structures of varying length and thickness that traverse the LV cavity. Their morphologic appearance and location in the LV cavity have been documented in autopsy studies [14–16] where the incidence of FTs was higher in males than females [14]. The rate of FTs in our young healthy male subjects was 74% and higher than in autopsy studies that included both genders (55–62%) [14,16]. Recent advances in the quality of echocardiographic images facilitate the detection of very thin FTs. In our earlier study we divided FTs into 4 types [18]. Type 1 and type 2 FTs connect the basal- or mid-septum to the PMs or to the apical free wall and tend to be thick and long. Type
432
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
Fig. 4. Types of false tendon and J-wave locations. In subjects with type 1 false tendons the J-waves were located in the inferior leads only (58.8%) or in both leads (5.9%); 35.3% had no J-waves. In subjects with type 2 false tendons the J-waves were located in the inferior leads only (14.3%), the lateral leads only (21.4%), or in both leads (24.1%); 42.9% had no Jwaves. In subjects with type 3 false tendons J-waves were located in the inferior leads only (33.3%) and the other subjects (66.7%) manifested no J-waves. In subjects with no false tendons the J-waves were observed in the inferior leads only (7.7%) or in both leads (15.4%). The other subjects (76.9%) had no J-waves.
3 FTs that connect the apical free wall to the apical septum tend to be thin and short. None of our current subjects presented with the very rare web-like type 4 FTs. The incidence of J-waves was significantly different among subjects with different FT types and different FT thickness. J-waves were seen in 64.7% and 57.1% of subjects with type 1 and type 2 FTs, respectively, and in 33.3% of those with FTs of type 3. Thus, the incidence of J-waves was significantly higher in males whose FTs were ≥2 mm than in those with thinner FTs (b2 mm). The location of the J-waves also differed with the FT type; in subjects with type 1 FTs most were located in the inferior leads. On the other hand, in males with type 2 FTs, J-waves were observed in both inferior and lateral leads; they were more prevalent in the lateral leads than in the presence of type 1 FTs. These findings were consistent with our earlier retrospective study [18]. We compared the characteristics of ECGs obtained in our two study groups. On 12-lead ECGs there was no significant difference between them in any of the measurements taken. However, the incidence of Jwaves was significantly higher in group 1 and fQRSd and LAS40 values measured on SAECG were also significantly longer in this group. In neither group did we record late potentials. We also found that fQRSd and LAS40 were significantly longer in subjects with type 1 or type 2 FTs than in those with type 3 FTs. Our observations suggest that in subjects with type 1 or type 2 FTs there is some slowing of conduction especially
Table 2 Comparison of the electrocardiographic characteristics of group 1 and 2.
12-lead ECG Heart rate (bpm) PR interval (ms) QRS duration (ms) QTc interval (s) JTc interval (s) J wave (+) SAECG fQRSd (ms) RMS40 (μV) LAS40 (ms)
Group 1 (n = 31)
Group 2 (n = 19)
p
62.3 ± 10.7 156.9 ± 14.9 100.2 ± 7.1 0.409 ± 0.018 0.308 ± 0.019 19 (61%)
67.5 ± 11.7 160.4 ± 18.9 98.4 ± 12.4 0.412 ± 0.017 0.310 ± 0.016 5 (26%)
0.116 0.468 0.523 0.620 0.751 0.016⁎
140.8 ± 9.0 46.7 ± 24.0 26.8 ± 8.5
134.8 ± 9.7 55.2 ± 24.2 20.8 ± 8.3
0.036⁎ 0.232 0.019⁎
Values are mean ± SD or number (%). fQRSd, filtered QRS duration; RAS40, root-mean-square voltage of terminal 40 ms of filtered QRS complex; LAS40, the duration of low-amplitude signals (b40 μV) in the terminal filtered QRS complex. ⁎ p b 0.05.
Fig. 5. Comparison of SAECG measurements by the false tendon type. FQRSd, filtered QRS duration; LAS40, duration of low-amplitude signals (b40 μV) in the terminal filtered QRS complex.
in the terminal portion of ventricular excitation, and that delayed activation did not manifest as late potential. J-waves, usually defined as notching or slurring at the terminal QRS complex on ECG, are present in 5%–24% of healthy populations [4,5,7,9]. Their incidence is age- and sex-dependent and they are primarily found in young males. In addition, young male athletes had a higher incidence of J-waves [5]. The present study revealed that incidence of J-waves was higher than those in previous reports [4,5,7,9]. We consider that one of the reasons of high incidence of J-wave was that our study population was composed of only young males and more than half of them were athletes. We also think that the ECG filter setting is one of the important factors to explain the difference of the incidence of J-waves because the
Table 3 Univariate and multivariate logistic regression analysis for the presence of J-waves. Variables
Body height (cm) Body weight (kg) Body mass index (kg/m2) Athlete FT (group1)
Univariate
Multivariate
p
Odds ratio
95% CI
p
0.222 0.143 0.262 0.156 0.020⁎
0.492 2.228 0.087 2.806 6.286
0.138–1.753 0.435–11.423 0.001–11.796 0.747–10.539 1.504–26.266
0.274 0.337 0.330 0.127 0.012⁎
CI, confidence interval; FT, false tendon. ⁎ p b 0.05.
M. Nakagawa et al. / International Journal of Cardiology 172 (2014) 428–433
application of a low-pass filter with a low cutoff attenuates or eliminates J-waves [20]. The use of young healthy males as the only subjects to be examined enables us to exclude the influence of various factors including age, gender, and basic diseases on the QRS morphologies in the surface ECGs. We performed logistic regression analysis and found that the presence of FTs was the only independent predictor of the elicitation of J-waves. Histologically, some FTs contain conduction tissues, suggesting that they are intracavitary radiations of the His-bundle [15–17]. An autopsy study of Loukas et al. [16]. found that 60% of FTs included conduction tissue fibers that resembled the His-bundle. They identified 3 types of FT, those located between the posteromedial or the anterolateral PM and the septum, and the web-like type; they correspond to our FTs of type 1, 2, and 4. Another FT type consists of fibromuscular bands without conduction tissue. While the electrophysiological mechanisms responsible for the generation of J-waves remain unclear, clinical and experimental evidence suggests anomalies in delayed depolarization or early repolarization [8,21–26]. Our hypothesis for the role of FTs in the genesis of J-waves is as follows. If type 1 and type 2 FTs harbor longitudinal conduction tissue similar to the His-bundle, electrical activity is conducted through the FTs from the septum toward the inferior or the lateral free wall of the LV. However, conduction may be slower in these tissues and it may be directed anatomically in the inferolateral direction, resulting in the appearance of delayed activity in the terminal portion of the QRS complex in the inferior or lateral leads of surface ECGs. This hypothesis is supported by our finding that type 1 FTs that are attached in the posteroinferior region of the LV elicited J-waves in the inferior leads while type 2 FTs that are attached at the lateral region of the LV elicited J-waves in the lateral leads. Another hypothesis states that a local repolarization gradient due to stretching or to unknown effects of Purkinje fibers may be involved in the mechanisms that elicit J-waves. 5. Limitations Our study has some limitations. First, our study population was small and composed of only healthy young males without organic heart disease or clinical evidence of ventricular arrhythmias. The mechanisms eliciting J-waves in a healthy population may be different from those involved in the genesis of pathological J-waves. Further studies are needed to investigate the relevance of our findings to the manifestation of J-waves in patients with idiopathic ventricular fibrillation [1–7,27] or other organic heart diseases such as acute myocardial infarction [28,29]. Second, we used only 2D echocardiograms to detect the FTs. Although technical advances in echocardiography have improved the visualization of cavity structures inside the ventricles, intracardiac or 3D echocardiography and magnetic resonance imaging studies are needed to precisely identify the attachment site of FTs. Third, we did not subject the FTs to histological study. We are performing investigations on human cadaveric hearts and histological studies to test our hypothesis. 6. Conclusions Our prospective study reveals a high incidence of J-waves in healthy young male subjects with FTs and documents the close association between the J-wave location and the FT type. Our findings suggest that FTs are related to the genesis of J-waves.
433
References [1] Aizawa Y, Tamura M, Chinushi M, et al. Idiopathic ventricular fibrillation and bradycardia-dependent intraventricular block. Am Heart J 1993;126:1473–4. [2] Garg A, Finneran W, Feld GK. Familial sudden cardiac death associated with a terminal QRS abnormality on surface 12-lead electrocardiogram in the index case. J Cardiovasc Electrophysiol 1998;9:642–7. [3] Shinohara T, Takahashi N, Saikawa T, Yoshimatsu H. Characterization of J wave in a patient with idiopathic ventricular fibrillation. Heart Rhythm 2006;3:1082–4. [4] Haïssaguerre M, Derval N, Sacher F, et al. Sudden cardiac arrest associated with early repolarization. N Engl J Med 2008;358:2016–23. [5] Rosso R, Kogan E, Belhassen B, et al. J-point elevation in survivors of primary ventricular fibrillation and matched control subjects: incidence and clinical significance. J Am Coll Cardiol 2008;52:1231–8. [6] Haïssaguerre M, Sacher F, Nogami A, et al. Characteristics of recurrent ventricular fibrillation associated with inferolateral early repolarization. Role of drug therapy. J Am Coll Cardiol 2009;53:612–9. [7] Tikkanen JT, Anttonen O, Junttila MJ, et al. Long-term outcome associated with early repolarization on electrocardiography. N Engl J Med 2009;361:2529–37. [8] Abe A, Ikeda T, Tsukada T, et al. Circadian variation of late potentials in idiopathic ventricular fibrillation associated with J waves: insights into alternative pathophysiology and risk stratification. Heart Rhythm 2010;7:675–82. [9] Haruta D, Matsuo K, Tsuneto A, et al. Incidence and prognostic value of early repolarization pattern in the 12-lead electrocardiogram. Circulation 2011;123:2931–7. [10] Suwa M, Yoneda Y, Nagao H, et al. Surgical correction of idiopathic paroxysmal ventricular tachycardia possibly related to left ventricular false tendon. Am J Cardiol 1989;64:1217–20. [11] Thakur RK, Klein GJ, Sivaram CA, et al. Anatomic substrate for idiopathic left ventricular tachycardia. Circulation 1996;93:497–501. [12] Merliss AD, Seifert MJ, Collins RF, et al. Catheter ablation of idiopathic left ventricular tachycardia associated with a false tendon. PACE 1996;19(12 Pt 1):2144–6. [13] Abouezzeddine O, Suleiman M, Buescher T, et al. Relevance of endocavitary structures in ablation procedures for ventricular tachycardia. J Cardiovasc Electrophysiol 2010;21:245–54. [14] Luetmer PH, Edwards WD, Seward JB, Tajik AJ. Incidence and distribution of left ventricular false tendons: an autopsy study of 483 normal human hearts. J Am Coll Cardiol 1986;8:179–83. [15] Abdulla AK, Frustaci A, Martinez JE, Florio RA, Somerville J, Olsen EG. Echocardiography and pathology of left ventricular “false tendons”. Chest 1990;98:129–32. [16] Loukas M, Louis Jr RG, Black B, Pham D, Fudalej M, Sharkees M. False tendons: an endoscopic cadaveric approach. Clin Anat 2007;20:163–9. [17] Kervancioğlu M, Ozbağ D, Kervancioğlu P, et al. Echocardiographic and morphologic examination of left ventricular false tendons in human and animal hearts. Clin Anat 2003;16:389–95. [18] Nakagawa M, Ezaki K, Miyazaki H, et al. Electrocardiographic characteristics of patients with false tendon: possible association of false tendon with J waves. Heart Rhythm 2012;9:782–8. [19] Fridericia LS. Die Systolendauer in Elektrokardiogram bei normalen Menschen und bei Herzkranken. Acta Med Scand 1920;53:469–86. [20] García-Niebla J, Serra-Autonell G. Effects of inadequate low-pass filter application. J Electrocardiol 2009;42:303–4. [21] Antzelevitch C, Yan GX. J wave syndromes. Heart Rhythm 2010;7:549–58. [22] Boineau J. The early repolarization variant—normal or a marker of heart disease in certain subjects. J Electrocardiol 2007;40:3. [23] Borggrefe M, Schimpf R. J-wave syndromes caused by repolarization or depolarization mechanisms. A debated issue among experimental and clinical electrophysiologists. J Am Coll Cardiol 2010;55:798–800. [24] Rosso R, Adler A, Halkin A, Viskin S. Risk of sudden death among young individuals with J waves and early repolarization: putting the evidence into perspective. Heart Rhythm 2011;8:923–9. [25] Antzelevitch C. Genetic, molecular and cellular mechanisms underlying the J wave syndromes. Circ J 2012;76:1054–65. [26] Nam GB. Idiopathic ventricular fibrillation, early repolarization and other J waverelated ventricular fibrillation syndromes: from an electrocardiographic enigma to an electrophysiologic dogma. Circ J 2012;76:2723–31. [27] Miyazaki H, Nakagawa M, Shin Y, et al. Comparison of autonomic J-wave modulation in patients with idiopathic ventricular fibrillation and control subjects. Circ J 2013;77:330–7. [28] Naruse Y, Tada H, Harimura Y, et al. Early repolarization is an independent predictor of occurrences of ventricular fibrillation in the very early phase of acute myocardial infarction. Circ Arrhythm Electrophysiol 2012;5:506–13. [29] Tikkanen JT, Wichmann V, Junttila J, et al. Association of early repolarization and sudden cardiac death during an acute coronary event. Circ Arrhythm Electrophysiol 2012;5:714–8.