Left Ventricular False Tendons: Echocardiographic, Morphologic, and Histopathologic Studies and Review of the Literature

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ORIGINAL ARTICLE Left Ventricular False Tendons: Echocardiographic, Morphologic, and Histopathologic Studies and Review of the Literature

Saji Philip a,b,c, Kottureth Mammen Cherian a, Mei-Hwan Wu c, Hung-Chi Lue c,d,*

a Division of Pediatric Cardiology, St Gregorios Cardiovascular Center, Parumala, Mannar, Kerala, A Unit of Frontier Lifeline and Dr K.M. Cherian Heart Foundation, Chennai, India b Division of Biotechnology, Animal Technology Institute, Miaoli, Taiwan c Division of Pediatric Cardiology, Department of Pediatrics, National Taiwan University Children’s Hospital, Taipei, Taiwan d Department of Pediatrics, Saint Mary’s Hospital, Luodong, Taiwan

Received May 11, 2010; received in revised form Nov 17, 2010; accepted Nov 29, 2010

Key Words Background: Left ventricular false tendons (LVFTs) are fibrous or fibromuscular bands stretch- echocardiography; ing across the left ventricle (LV) from the ventricular septum to the papillary muscle or LV free histopathology; wall but not connecting, like the chordae tendinae, to the mitral leaflet. LVFTs have become human and piglet; the focus of studies and discussions since the advent of echocardiography. left ventricular false Materials and Methods: We prospectively studied the prevalence of LVFTs by two-dimensional tendons; echocardiography in 476 infants and children referred to our institute for cardiac evaluation morphology and cardiology workup. We also studied the morphology and histopathology of LVFTs in 68 congenital heart disease specimens and in 20 piglet hearts. The literature was reviewed and the clinical significance of LVFTs was discussed. Results: LVFTs of varying size and different location were detected in 371 (77.9%) of 476 infants and children studied, in 42 (61.8%) of 68 congenital heart disease specimens, and in 19 (95.0%) of 20 piglet hearts. Of the 75 LVFTs from the congenital heart disease specimens, 33 (44.4%) were fibrous type, measuring less than 1.4 mm; 38 (50.7%) were fibromuscular type, 1.5e2.4 mm; and 4 (5.3%) were muscular type, 2.5 mm or more in diameter. Of the 33 LVFTs from the piglet hearts, 23 (69.7%) and 10 (30.3%) were fibrous and fibromuscular, respectively, and none (0.0%) was muscular.

* Corresponding author. Division of Pediatric Cardiology, Department of Pediatrics, National Taiwan University Children’s Hospital, Taipei and Saint Mary’s Hospital, Luodong, Taiwan. E-mail address: [email protected] (H.-C. Lue).

Conclusions: LVFTs were detected partially or completely by modified two-dimensional echocardiography in both normal and abnormal hearts. LVFTs is a useful anatomical landmark of LV for the differentiation of morphological LV and right ventricle in segmental analysis of congenital heart disease. LVFTs are a cause of functional murmur. No pressure gradient was noted in the mid-LV or outflow tract. LVFTs could be a contributory factor in the generation of dysrhythmias during LV catheterization studies. LVFTs were more easily identifiable in neonates and young age patients because of a better delineation of images in echocardiography. Copyright ª 2011, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. All rights reserved.

1. Introduction 2.2. Echocardiographic studies

Filaments of the tissue crossing the left ventricular (LV) Echocardiographic studies were carried out with three cavity were first reported by Turner1,2 early in 1893. They different color Doppler 2-D echocardiographic machines, were fibrous or fibromuscular bands stretching from the General Electrical Logiqu 500-Pro series (New Jersey, NJ, ventricular septum to the papillary muscle, LV free wall, or USA), Multiscan G200, system Vivid 5 Vingmed Technology apex.1,2 LV false tendons (LVFTs) in early days were the (Stockton, CA, USA), and Acuson Cypress Siemens Medical incidental findings at autopsy but later became the common Solutions (Mountain View, CA, USA). The frequencies of the findings.1e4 The reported prevalence of LVFT in both human transducers used were 2.5e6 MHz, selected according to and animal studies varied from 0.4% to 95%.5e24 The asso- the age of patients. Parasternal long axis and apical four- or ciation of functional murmur, pre-excitation, repolarization five-chamber views were used with special attention in the electrocardiogram (ECG) abnormalities, and LV aneurysm delineation of the LV apex, papillary muscles, free walls, with LVFT in human has been reported.3,10,13,25e30 Based on and the ventricular septum. In addition to the above views, the literature, the clinical significance, effects, and mech- we also used apical two-chamber, substernal-four chamber, anism of LVFTs were discussed. and short-axis views in some cases. To define the LV tendons, all the examinations were performed by one 2. Materials and Methods pediatric cardiologist and confirmed by another cardiologist or echocardiographic technician. Doppler study was performed to see if any pressure gradient was produced in the 2.1. Study population mid-LV and LV outflow tract (LVOT) by the tendons, where the attachment was close to the aortic valve. Using the two-dimensional (2-D) echocardiography, we prospectively studied the presence of LVFT in 476 infants and children, aged 0e18 years, including 369 patients 2.3. Morphological studies referred to our cardiac clinic for evaluation of their cardiac murmur, chest pain, exertional dyspnea, and/or ECG We studied for the presence of LVFT in 20 piglet heart abnormalities, such as atrioventricular block, bundle specimens, of which the ages were 1e3 months with branch block, Wolff-Parkinson-White syndrome, and/or a mean of 2 months, weighing 20e32 kg.32 A series of 68 atrial/ventricular premature beat, and 107 patients with congenital heart disease specimens of ages, preterm known congenital heart disease referred to our service for (22e36 weeks gestation), neonate (0e30 days), and 2 cardiac workups. Those with difficulty in delineating monthse3 years were also studied. The LV tendons were ventricular chambers, such as single ventricle, and hypo- looked through the LV window, which was made for post- plastic LV were excluded from this study. mortem studies. All the LVFT specimens were perfused

Table 1 Prevalence of LVFT and its correlation with heart murmur, chest pain, exertional dyspnea, and abnormal ECG among infants and children referred for cardiac evaluation and those with CHD for cardiac workup. Patients Patients studied Heart murmur Chest pain Exertional dyspnea Abnormal ECG Patients LVFT noted Patients LVFT noted Patients LVFT noted Patients LVFT noted Patients LVFT noted (n) (%) (n) (%) (n) (%) (n) (%) (n) (%) Referral 369 293 (79.4) 256 206 (80.5)* 30 21 (70.0) 13 10 (76.9) 30 11 (36.7)** patients CHD patients 107 78 (72.9) 107 70 (65.4)* 10 7 (70.0) 32 25 (78.1) 99 80 (80.8)** Total (%) 476 (100.0) 371 (77.9) 363 (76.3) 276 (76.0) 40 (8.4) 28 (70.0) 45 (9.5) 35 (77.8) 129 (27.1) 91 (70.5)

Figures in parenthesis denote percent LVFT noted or detected. *p Z 0.002, **p Z 0.001. CHD Z congenital heart disease; ECG Z electrocardiogram; LVFT Z left ventricular false tendon. Left ventricular false tendons 281 and put in 10% phosphate-buffered formaldehyde. All the 2.4. Statistical signiﬁcance tendons were serially sectioned into segments of 2e3mm thickness, and slides were prepared in hematoxylin and Statistical signiﬁcance was studied using SPSS analysis (IBM eosin stain for histopathological examinations. SPSS statistics, version 19; SPSS, Inc., Chicago, IL, USA) for

Figure 1 (AeF) Modified echocardiographic appearance of LV false tendons in normal and abnormal heart. (A) Apical four- chamber view showing LV fibrous tendon (*) measuring 0.3 mm in width connecting mid-IVS to the base of anteromedial papillary muscle. (B) Parasternal long-axis and M-mode view showing LV fibromuscular tendon (white small arrow) measuring 2.0 mm connecting from IVS perimembranous region to LV apex. (C) Modified subcostal RVOT view showing fibromuscular tendon (*) measuring 2.3 mm. (D) Parasternal long-axis view showing a muscular tendon (*) measuring 4.8 mm attaching perimembranous region of IVS to LV apex. (E) Parasternal long-axis view showing multiple tendons and a bifurcation near the apical portion (*). (F) Parasternal long-axis view showing a muscular tendon (*) in a morphological LV identified in a patient with D-TGA. AO Z aorta; APM Z anterior papillary muscle; BPM Z beats per minute; D-TGA Z D-transposition of the great arteries; FT Z fibrous tendon; IVS Z interventricular septum; LA Z left atrium; LV Z left ventricle; LVT Z left ventricle thrombus; PA Z pulmonary artery; PPM Z posterior papillary muscle; RPA Z right pulmonary artery; RV Z right ventricle; RVOT Z right ventricle outflow tract. 282 S. Philip et al

Figure 2 (AeC) Congenital heart disease specimens showing LV false tendons. (A) LV cut opened showing the bifurcating LV tendon connecting apex to mid-IVS to perimembranous in a case of TOF. (B) LV tendon (a probe inserted) connecting the perimembranous portion of interventricular septum to the LV free wall in a 1-year-old child with D-TGA and VSD. (C) A muscular tendon from the perimembranous portion of the ventricular septum to the apical free wall in a fetal specimen of 23 weeks’ gestation. D-TGA Z D-transposition of the great arteries; LV Z left ventricle; TOF Z Tetralogy of Fallot; VSD Z ventricular septal defect.

Figure 3 (A and B) A piglet heart showing left ventricle (LV) false tendons. (A) Bifurcating ﬁbrous tendon (*), stretching between the perimembranous region of the ventricular septum to anteromedial papillary muscle in a 1-month-old piglet. (B) Fibromuscular tendon (*) attaching the midportion to the free wall of LV.

Table 2 The number and type of LVFT detected in congenital heart disease specimens and piglet hearts. Specimens (n) LVFT detected Number and type of LVFT n (%) I II III Total Congenital heart disease Preterms (12) 6 (2) 50.0 6 9 0 15 Neonates (36) 24 (10) 66.7 19 21 3 43 Children (20) 12 (3) 55.6 8 8 1 17 Total (68) 42 (15)* 61.8** 33 38 4 75 (%) (44.4) (50.7) (5.3) (100.0)*** Piglet hearts (20) 19 (9)* 95.0* 23 10 0 33 (%) (69.7) (30.3) (0.0) (100.0)***

Figures denote the number of specimens with more than one tendons. Type I: ﬁbrous <1.4 mm; Type II: ﬁbromuscular 1.5e2.4 mm; Type III: muscular >2.5 mm. *p Z 0.043, **p Z 0.003, ***p Z 0.018. LVFT Z left ventricular false tendons. Left ventricular false tendons 283 the prevalence of LVFT among patients and for the association of LVFT with heart murmur, chest pain, exertional dyspnea, and ECG abnormalities.

3. Results

There were LVFTs in 293 (79.4%) of 369 infants and children referred for cardiac evaluation and in 78 (72.8%) of 107 infants and children with known congenital heart diseases undergoing cardiology workup. The LVFT positive rate of the two groups of patients was not statistically significant (Table 1). Most LVFT were stretching from the lower third or middle region of the ventricular septum to the lower portion of the anterior or posterior free wall or to the papillary muscle. In only eight instances, the tendons were stretching from the perimembranous-trabecular portion of the ventricular septum to the LV free wall and in four, they were coursing from the ventricular septum, at the posterior wall of LVOT, near the atrioventricular valve, to the apical portion of the LV. There was no pressure gradient detected in the LV either in mid-LV or LVOT (Figures 1AeF). LVFT detected in patients referred for evaluation of the heart murmur, chest pain, exertional dyspnea, and abnormal ECG and in those with known congenital heart disease were compared, as seen in Table 1. A significantly higher percentage (80.5%) of patients referred with cardiac murmur had the LVFT than those (65.4%) with known congenital heart disease (p Z 0.002). Of those with abnormal ECG, a higher percentage (80.8%) of patients with congenital heart disease had the LVFT than those (36.7%) referred for cardiac evaluation (p Z 0.001). There was no significant difference in the prevalence of LVFT between the two groups of patients with chest pain and exertional dyspnea (Table 1).

3.1. Morphological and histopathological examinations

The morphology of LVFT of congenital heart disease specimens is shown in Figures 2AeC and of piglet hearts in Figures 3A and 3B. LVFTs were found in 42 (61.8%) of 68 congenital heart disease specimens and more frequently (p Z 0.003) in 19 (95.0%) of 20 piglet hearts (Table 2)In 15 (35.7%) congenital heart disease specimens and in 9 (45.0%) of piglet hearts, more than one false tendons were found (Table 2). Of the 75 LVFT from the congenital heart specimens, 33 (44.4%) were fibrous type, measuring less than 1.4 mm in diameter; 38 (50.7%) fibromuscular type, 1.5e2.4 mm; and 4 (5.3.%) muscular type, larger than 2.5 mm (Figures 4AeC). Of the 33 LVFT specimens from the piglet hearts, 23 (69.7%) and 10 (30.3%) were fibrous and fibro-muscular type, respectively, and none (0.0%) was muscular type (Table 2 and Figures 3A and 3B). The distribution of LVFT types of congenital heart disease specimens and of piglet hearts was significantly different Figure 4 (AeC): Hematoxylin and eosin staining of left (p Z 0.018). ventricle (LV) false tendons (LVFT). (A) Fibrous type of LVFT (40Â). (B) Fibromuscular type of tendons (200Â) showing 4. Discussion predominantly muscular and fibrous tissues and small branches of coronary arteries. (C) Cross-section of a muscular type Â Various terms were used in the literature to call the LVFT tendon (100 ) showing Purkinje fibers, coronary arteries, stretching between the ventricular septum to the LV free fibrous (F), and predominantly myocardial fibers (M). 284 S. Philip et al wall or papillary muscle (Table 3).1,2,17,18,27e31,42e44 These Table 4 Prevalence of left ventricular false tendons tendons are not the chordae tendinae connecting the (LVFTs) reported in the literature. papillary muscle to the mitral valve leaflet. It is the reason, therefore, “false tendon” has become increasingly more Year Authors Studied (n) LVFT found, popular.29,30 n (%) The prevalence of LVFT reported in the literature varied 1981 Nishimura et al5 1000 Humana 5 (0.5) widely ranging from 0.4% to 68%, mainly because of the 1981 Okamoto et al6 132 61 (46) 5e22 different methodologies used (Table 4). Since the 1983 Perry et al7 3847 31 (0.8) advent of 2-D echocardiography, which could be one of the 1984 Vered et al8 2079 42 (2) most powerful tools in imaging tissues in the heart, LVFT 1984 Beattie et al9 2004 84 (4) have become the subjects of attention and studies. 1984 Sethuraman et al10 1012b 4 (0.4) We correlated the clinical symptoms and signs of 1984 Gerlis LM et al11 686 Humana 329 (48) patients with LVFT in our two groups of patients. Signifi- 159 Animala 151 (95) cantly higher percentage (80.5%) of patients with cardiac 1984 Brenner et al12 100 61 (61) murmurs, of which most were functional murmur, had the 1984 Suwa et al13 1117 71 (6) LVFT than those patients (65.4%) with congenital heart 1986 Luetmer et al14 483 Humana 265 (55) disease, indicating that LVFT might have a role precipi- 1986 Casta et al15 203 31 (14) tating the functional murmur. Higher percentage (80.8%) of 1986 Malouf et al16 488 123 (25) patients with congenital heart disease had the LVFT than 1987 Boyd et al17 474 Humana 322 (68) those (36.6%) of patients referred for ECG abnormalities 1988 Martins et al18 883b d indicating that LVFT might play only a role in causing ECG 1990 Abdulla et al19 100 Humana 34 (34) abnormalities (Table 1). Correlations of the various kinds of 1992 Cocchieri and Bardelli20 273 80 (29) ECG abnormalities and the locations and histopathology of 1996 Grzybiak et al21 180 d LVFT were not analyzed. 2003 Kervancioglu et al22 368 97 (26) Embryologically false tendons were thought to have 2010 Present study 476 371 (78) been derived from the inner muscle layer of the primitive 68 Humana 42 (62) 2,7 heart. The present study showed that LVFT were con- 20 Pigleta 19 (95) necting invariably from the ventricular septum to either the a Autopsy cases. papillary muscle or ventricular free wall. b Adult cases. Histopathologically, LVFT contain fibrous tissues, myocardial fibers, elastic fibers, and blood vessels.11,22 Thick bands are composed of thickened endocardium with discrete subaortic stenosis,34,35 vegetations,36 flail aortic myocardial tissues that have all the features attributable to valve,37 parachute accessory anterior mitral leaflet,38 and myogenic conducting tissues identical to that seen in the right sinus valsalva aneurysm.39 bundle of His.19 Purkinje cells were not observed in the LVFT have been shown to be a cause of functional, so- specimens studied.11,19,22 called innocent murmur.40,41 The cause of functional The presence of myocardial fibers and conducting tissues murmur may be multifactorial, including dimensions of the in LVFT might be a cause of premature ventricular ascending aorta, LVOT, and the location of tendons. In the contractions, ECG repolarization abnormalities (giant T present study, there was no pressure gradient, however, wave inversion), and pre-excitation reported in apparently detected in the mid-LV or LVOT, irrespective of the course, e healthy individuals.13,25 27 Some of the abnormal echo attachment, or thickness of the LV tendons. At the surgical shadows may simulate LV tendon, such as thrombus,33 closure of ventricular septal defect, surgeons should be careful to avoid suturing these tendons, in view of the possible presence of conduction system and coronary artery branches in the LVFT. LV tendons could be a contributory Table 3 Various terms used for left ventricular (LV) false factor in the generation of dysrhythmias during LV cathe- tendons in the literature. terization studies. Authors Year Terms used LVFT detectable by modified 2-D echocardiography in Turner1,2 1893 Moderate band in left ventricle both normal and abnormal heart is a useful anatomic Millar42 1964 Muscular strands landmark for differentiation of the ventricular chambers in Grzybiak et al21 1966 Fibromuscular ribbons segmental analysis of congenital heart disease. We found Roberts3 1969 Anomalous LV strands that LVFTs were more easily identifiable in neonates and Gueron 1972 Anomalous LV chordae tendinae young age patients because of a better delineation of and Cohen27 images by echocardiography. Pomerance43 1975 False tendons Goshal44 1975 Septomarginal trabeculae 31 Acknowledgments Choo et al 1982 Anomalous LV chordae tendinae Boyd et al17 1987 Prominent LV trabeculations Martins et al18 1994 Muscular false tendons The authors are grateful to Dr C. 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