Surg Radiol Anat (2008) 30:317–322 DOI 10.1007/s00276-008-0326-5
ORIGINAL PAPER
Right ventricular false tendons, a cadaveric approach Marios Loukas · Christopher T. Wartmann · R. Shane Tubbs · Nihal Apaydin · Robert G. Louis Jr · Brandie Black · Robert Jordan
Received: 22 May 2007 / Accepted: 7 February 2008 / Published online: 19 February 2008 © Springer-Verlag 2008
Abstract Left ventricular false tendons (LFTs) have been extensively described and recognized by gross anatomic studies. However, there is very little information available regarding right ventricular false tendons (RFTs). The aim of our study, therefore, was to explore and delineate the morphology, topography and morphometry of the RFTs, and provide a comprehensive picture of their anatomy across a broad range of specimens. We identiWed 35/100 heart specimens containing right ventricular RFTs and classiWed them into Wve types. In Type I (21, 47.7%) the RFTs, was located between the ventricular septum and the anterior papillary muscle; in Type II (11, 22.9%) between ventricu-
M. Loukas (&) · C. T. Wartmann · R. G. Louis Jr · B. Black · R. Jordan Department of Anatomical Sciences, School of Medicine, St George’s University, Grenada, West Indies e-mail:
[email protected] M. Loukas Department of Education and Development, Harvard Medical School, Boston, MA, USA C. T. Wartmann Department of Surgery, Northwestern University, Chicago, IL, USA R. S. Tubbs Department of Cell Biology, University of Alabama at Birmingham, Birmingham, AL, USA N. Apaydin Department of Anatomy, Ankara University School of Medicine, Ankara, Turkey R. G. Louis Jr Department of Neurosurgery, University of Virginia, Charlottesville, VA, USA
lar septum and the posterior papillary muscle; in Type III (7, 14.5%) between the anterior leaXet of the tricuspid valve and the right ventricular free wall; in Type IV (5, 10.4%) between the posterior papillary muscle and the ventricular free wall; and lastly, in Type V (4, 8.3%) between the anterior papillary muscle and ventricular free wall. The mean length of the RFTs was 18 § 7 mm with a mean diameter of 1.4 § 05 mm. Histologic examination with Masson trichrome and PAS revealed that 20 (41.6%) of the 48 RFTs carried conduction tissue Wbers. The presence of conduction tissue Wbers within the RFTs was limited to Types I, III, and IV. In Types II and V the RFTs resembled Wbrous structures in contrast with Type I, II and IV, which were composed more of muscular Wbers, including conduction tissue Wbers. RFTs containing conduction tissue Wbers were identiWed, which may implicate them in the appearance of arrhythmias. Keywords False tendons · Papillary muscle complex · Tricuspid valve · Ventricular septum · Membranous septum · Conduction tissue Wbers
Introduction Considering its current place as the organ implicated in the largest percentage of human mortality, it is easy to understand why the detailed anatomical structure of the heart has been extensively studied. Despite the multitude of studies investigating various aspects of cardiac anatomy, some structures of the heart still remain incompletely described. One area, which is particularly lacking in the literature, is that of right ventricular bands or false tendons (RFTs). Standard anatomical texts, in their topographical descriptions of the cardiac ventricles, give no mention of
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false tendons (FTs) [7, 19, 33]. It is only through probing the literature that one can begin to develop a working deWnition of a false tendon. As cited by Gerlis et al. FTs were Wrst described by Turner in 1893 and again by Keith and Flack in 1906, who reported that they were almost always present in both human and bovine hearts [11]. According to Kervancioglu et al. false tendons are single or multiple, thin, Wbrous, or Wbromuscular structures that traverse the cavity of the left ventricle and have no connections with the valvular cusps [12]. A series of studies, have extensively explored the anatomical features of the left false tendons (LFTs), macroscopically, histologically, endoscopically, and ultrasonographically [1, 6, 12, 16, 17, 25, 26, 29]. However, we have no data regarding the presence of RFTs in the right ventricle, other than the study of Armiger et al. in which only three human hearts were examined [5]. Similarly, the deWnition of a RFT is made for a single or multiple, thin, Wbrous, or Wbromuscular structures that traverse the cavity of the right ventricles and have no connections with the valvular cusps. Some authors describe the RFT atypical false chordae tendinae. However, in this study the RFT terminology has been adopted. Previous experience, by the present authors, with cadaveric exploration of the heart has led to the observation that great variation exists regarding the origin of the RFTs, their communication with the right ventricular free wall, papillary muscles and conduction tissue Wbers. The aim of our study was to explore and delineate the morphology, topography and morphometry of right ventricular RFTs and provide a comprehensive picture of their anatomy across a broad range of specimens.
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examined by three members of the team, independently ML, RGL, CW. Following preliminary examination, images from all dissected specimens were recorded with a Nikon digital camera (model: Coolpix S5) and studied using a computerassisted image analysis system (Lucia software 5.0 [2000, edition for Windows XP], made by Nikon [Laboratory Imaging Ltd]). The digital camera was connected to an image processor (Nvidia GeForce 6800 GT) and linked to a computer. Digitized images of the FTs were stored in the Lucia program (2,048 £ 1,536 pixels) and converted to intensity gray levels from 0 (darkest) to 32 bit (lightest). After applying a standard 1 mm scale to all pictures, the program was able to use this information to calculate pixel diVerences between two selected points, such as origin and termination of RFTs, as previously described [15]. SpeciWcally, the length was measured from the point of origin of the RFTs to its point of insertion. Access to the right ventricle was gained through the tricuspid and pulmonary valves. Results were analyzed with ANOVA test using Statistica software for Windows and values were considered statistically signiWcant when p < 0.05. Microscopic In all RFTs, we made serial transverse histological sections through the FT perpendicular to its long axis, cutting the sections at a thickness of 5 m. In order to analyze their structural composition, the RFTs sections were stained with Hematoxylin-Eosin, Van Gieson, Masson trichrome, and PAS methods.
Results Materials and methods Macroscopic The anatomy of the RFTs was examined in 100 Caucasian adult human hearts during gross anatomy courses at the St George’s University, during the years 2006–2007. The cadavers were derived from male (57) and female (43) subjects with an age range from 44 to 91 years and a mean age of 73 years. All the specimens were Wxed in formalin–phenol–alcohol solution and derived from US human body donated program. None of the specimens revealed any evidence of previous surgical procedures or traumatic lesions to the heart. Furthermore, the specimens collected were speciWcally derived from subjects in which no macroscopic pathological changes were visible (other than atherosclerosis) and the cause of death was non-cardiac related (carcinomas, brain aneurysm, etc). In order to correct for individual examiner variability, each specimen was
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During gross examination we were able to identify 35 heart specimens containing right ventricular RFTs. Of the 35 specimens, 12 (34.2%) contained multiple RFTs (seven specimens contained two RFTs and two specimens contained three RFTs and one specimen containing Wve RFTs), while the remaining specimens exhibited a single RFT. The total number of RFTs observed was 48, which were classiWed according to their location into Wve types. The classiWcation of Type I (21, 47.7%) was applied to RFTs, which were located between the ventricular septum and the anterior papillary muscle (Figs. 1, 2). Type II (11, 22.9%) was an RFT connection between ventricular septum and the posterior papillary muscle (Fig. 3). In Type III (seven, 14.5%) the RFTs were connecting the anterior leaXet of the tricuspid valve with the right ventricular free wall (Fig. 4). Type IV (Wve, 10.4%) describes an RFT, which connected the posterior papillary muscle to the ventricular free wall (Fig. 4). Lastly, Type V (four, 8.3%)
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Fig. 1 An example of Type I RFTs. The asterisks indicate the accessory false tendons arising distally from the ventricular septum to the anterior papillary muscle
Fig. 2 An example of Type I RFTs. The asterisks indicate the accessory false tendons arising distally from the ventricular septum to the anterior papillary muscle. In addition, the septal papillary muscles are also indicated in order to observe their diVerence with the right ventricular false tendons
designates RFTs, which were connecting the anterior papillary muscle to the ventricular free wall. Morphometric analysis showed that the mean length of the RFT was 18 § 7 mm with a range of 6–48 mm. The diameter of each RFT was also measured at the midpoint between its two connections and found to have a mean of 1.4 § 05 mm with a range of 1.1–2.0 mm. By using Masson trichrome and PAS staining techniques, we were able to determine that 20 (41.6%) of the 48 RFTs carried conduction tissue Wbers. The presence of conduction tissue Wbers within the RFTs was limited to Types I, III, and IV (Fig. 5). In Types II and V the RFTs resembled Wbrous structures (Fig. 6) in contrast with Type I, III
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Fig. 3 An example of Type II RFTs, in which the RFT is located between the ventricular septum and the posterior papillary muscle. In this case the RFT is passing posteriorly to the moderator band to Wnally attach to the base of the posterior papillary muscle. 1 Moderator band, 2 anterior papillary muscle, 3 posterior papillary muscle
Fig. 4 An example of Type III and Type IV RFTs in the same specimen. Arrow 1 demonstrates a Type III RFT which connects the anterior leaXet of the tricuspid valve with the right ventricular free wall. In contrast arrow 2 demonstrates a Type IV RFT, which connects the posterior papillary muscle to the ventricular free wall
and IV, which were composed more of muscular Wbers, including conduction tissue Wbers. Analysis revealed no statistically signiWcant diVerences in the prevalence of RFT type, with respect to age or gender (p > 0.1).
Discussion Although, the study of RFTs has historically been limited to gross dissections and echocardiography, several reports have provided excellent descriptions of their topography and relative positions; however, these reports have been
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Fig. 5 An example of a PAS stained histologic section revealing intense red stained areas that the conduction tissue resides. Asterisk indicates the core of the histologic section were the conduction tissue Wbers are present
Fig. 6 An example of a Masson trichrome stained histologic section revealing a uniform characteristic green color of collagen Wbers and absence of conduction tissue Wbers. Asterisk indicates the core of the histologic section
almost exclusively limited to the left ventricle [1, 6, 12, 16, 17, 25, 26, 29]. Several authors have observed that the papillary muscles and the tendinous cords of the right ventricle have shown endless variability in number, shape and location [8, 9, 24]. According to Gray’s anatomy [33], the chordae tendinae have been categorized as Wrst, second, and third order chordae according to the distance of their attachment from the margins of the atrioventricular leaXets; they can additionally be classiWed as single, free-edge, deep and basal chordae. False chordae tendinae (false tendons), however, are irregular in numbers and dimensions in the right ventricle [33]. In early embryonic development, the commissure between the anterior and septal leaXets of the tricuspid valve forms when the dextrodorsal conus swelling or right bulbar ridge fuses with the atrioventricular cushions or
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right tubercles of the atrioventricular cushions. If these fused mesenchymal structures remain closely associated with the membranous ventricular septum and become normally undermined during systole, the anteromedial commissure of the tricuspid valve becomes an uninterrupted expanse of valve tissue supported at the membranous ventricular septum by chordae and usually a raphe, and the annulus continues in a straight line across the center of the membranous ventricular septum. Interference with this developmental mechanism results in a spectrum of anatomic variations, including the formation of RFTs [5, 28]. Another theory largely stems from new insights to the development of the conduction tissue of the heart. According to Anderson et al. [2] cells that possess an unequivocally nodal phenotype, but are not part of the functioning conduction tissue may be present in the vestibule of the tricuspid valve and as a not of retroartic tissue [3]. More recently, it has been found that these cells are remnants of much more extensive area of cells to be found in the developing heart [4]. They were recognized as being special, nonetheless, long before the relationships to the developing primordiums of the conduction system was established [20, 21]. It is possible these cells will still be present in the postnatal heart and incorporated within the RFTs. Several reports exist partially commenting on the existence of abnormal muscular bands in the right ventricle, yet none provide a concrete description or full acknowledgement that these RFTs are present. For example, in a study of septal papillary muscles, Frick [10] identiWed unusual patterns of distribution of chordae tendinae, collectively naming them musculi transverse. In their morphologic study of the papillary muscles, Skwarek et al. [31, 32], as well as Nigri et al. [24] depicted RFTs in one of their Wgures, however, they failed to include this Wnding in their results. In another study by the same author [32] on the connection between the papillary muscle and the leaXets of the tricuspid valve, they identiWed atypical forms of distribution of RFTs in the right ventricle, yet their small number of specimens prevented the authors from classifying them. Furthermore, atypical short, thickened chordae tendinae were also described in a post-mortem study by Kocak et al. notably found, in higher numbers in cardiac death cases [14]. More speciWcally, only one study in the literature describing the incidence of human RFTs exists, and was limited to three specimens [5]. Clinically, atypical chordae tendinae have been entertained as a possible etiology in several cardiac pathologic processes. One of the most important is that the RFT may be the origin of rhythm disturbances. For example, an important study by Suwa et al. described the clinical signiWcance of RFTs in association with premature ventricular contractions (PVCs) [34]. In their study of 1,117 patients, RFTs were observed to occur with an overall incidence of
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6.4%. However, among 62 patients with PVCs in the absence of underlying heart disease, the incidence of RFTs was found to be 56%. Although, a deWnitive etiologic role is diYcult to determine, the unexpectedly high incidence of coexistence suggests, that RFTs may be involved in the pathophysiology of PVCs [26, 34]. Imaging studies encountering the presence of RFTs have possibly been correlated with multiple cardiopathologic processes. Interestingly, a report by Sethuraman et al. reported detecting RFTs echocardiographically in only 4 (0.4%) of 1,012 patients studied [30]. Of the four patients with RFTs however, the authors concluded that there may have been a causal association between these abnormal bands and both an S3 gallop in one patient, and a systolic murmur in another. Furthermore, recent ultrasonographic studies suggest that aberrant tendinous chords of the right ventricle may serve as a pathologic congenital anomaly leading to severe tricuspid regurgitation in pediatric patients [13, 18]. From a histological point of view, only LFTs have been reported as Wbromuscular or muscular bands [1, 6, 12, 16, 25, 29]. Our previous study has shown that the LFTs often contain myocardial Wbers and conductive tissue [16]. Similarly, the present study has also shown the RFTs contain myocardial Wbers and conductive tissue. The conductive tissue of the RFTs is identical to that seen in the bundle of His and suggests that RFTs could be continuations of these tissues. The contribution of this conductive tissue in the ventricle may increase the clinical signiWcance of the RFTs in that it could oVer a possible explanation of the relationship between the RFTs and premature ventricular beats among other reentry arrhythmias. The possible pathogenicity of normal appearing RFTs may not be limited to electrical issues. A report by Mukai et al. provides an example of a hemodynamic complication where a ruptured LFT, secondary to dilated cardiomyopathy, served as a peduncle for a mobile left ventricular thrombus [23]. In another case, a LFT was identiWed as the cause of a transient, precordial murmur [27]. Multiple reports exist depicting complications involving entanglement within the chordae tendinae during right-sided cardiac catheterization. This may be one of the most important complications of RFTs. A case report from Winrow et al. depicts two cases in which a pigtail catheter was entrapped by the chordae tendinae of the tricuspid valve during pulmonary arteriography [35]. Additionally, Moreno et al. describe tricuspid valve chordae entanglement and subsequent rupture following pacemaker electrode replacement [22]. Intuitively, the existence of RFTs would serve as an additional obstacle, thus increasing the possibility of catheterization entanglement. Therefore, it is important for the interventional cardiologist to recognize the existence of these abnormal muscular bands in the right ventricle, not
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only as an additional possible cause of catheter entanglement, but also in order to develop potential techniques for dislodgement, as have already been implored for chordae tendinae, ultimately reducing the risk of rupturing a papillary muscle. Hypothetically speaking, one can only imagine the grave situation that would be encountered upon catheter entanglement during an emergent pulmonary arteriography in the attempt to diagnose an acute pulmonary embolism. With the increasingly recognized signiWcance of RFTs as relates to cardiovascular pathology (particularly arrhythmias), it remains important to continue searching for new and improved methods of detection and early diagnosis. We are still unaware to which degree a cardiac MRI, an ultrasound or an angioscopy are able to detect RFTs. We hope that future studies will aim to determine these facts.
References 1. Abdulla A, Frustaci A, Martinez J et al (1990) Echocardiography and pathology of left ventricular false tendons. Chest 98:129–132 2. Anderson RH, Webb S, Brown NA, Lamers W, Moorman A (2003) Development of the heart: (2) septation of the atriums and ventricles. Heart 89:949–958 3. Anderson RH, Taylor IM (1972) Development of atrioventricular specialized tissue in human heart. Br Heart J 34:1205–1214 4. Anderson RH, Ho SY (2003) The morphology of the cardiac conduction system. In: Chawdick DJ, Goode J (eds) Development of the cardiac conduction system. Wiley, New York, pp 6–17 5. Armiger LC, Urthaler F, James TN (1979) Morphological changes in the right ventricular septomarginal trabecula (false tendon) during maturation and ageing in the dog heart. J Anat 129:805–817 6. Casta A, Wolf W (1986) Left ventricular bands (false tendons): echocardiographic and angiocardiographic delineation in children. Am Heart J 111:321–324 7. Clemente CD (ed) (1985) Gray’s anatomy, 30th edn. Lea & Febiger, Philadelphia, pp 631–635 8. Frater RWM (1994) The right-sided atrioventricular valve. J Heart Valve Dis 3:25–26 9. Frater RWM (1995) Is right-sided atrioventricular valve trileaXet? J Heart Valve Dis 4:568–570 10. Frick H (1960) Das Herz der Primaten. In: Hofer H, Schultz AH, Starck D (eds) Primatologia. Vol. I, 4th edn. Basel, New York 11. Gerlis L, Wright H, Wilson N, Erzengin F, Dickinson DF (1984) Left venticular bands. A normal anatomical feature. Br Heart J 52:641–647 12. Kervancioglu M, Ozbag D, Kervancioglu P, Hatipoglu ES, Kilinc M, Yilmaz F, Deniz M (2003) Echocardiographic and morphologic examination of left ventricular false tendons in human and animal hearts. Clin Anat 16:389–395 13. Kobza R, Kurz DJ, Oechslin EN, Pretre R, Zuber M, Vogt P, Jenni R (2004) Aberrant tendinous chords with tethering of the tricuspid leaXets: a congenital anomaly causing severe tricuspid regurgitation. Heart 90:319–323 14. Kocak A, Govsa F, Aktas EO, Boydak B, Yavuz IC (2004) Structure of the human tricuspid valve leaXets and its chordae tendineae in unexpected death. A forensic autopsy study of 400 cases. Saudi Med J 25:1051–1059 15. Loukas M, Louis RG Jr, Hullett J, Loiacano M, Skidd P, Wagner T (2005) An anatomical classiWcation of the variations of the inferior phrenic vein. Surg Radiol Anat 27:566–574
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322 16. Loukas M, Louis RG Jr, Black B, Pham D, Fudalej M, Sharkees M (2007) False tendons: an endoscopic cadaveric approach. Clin Anat 20:163–169 17. Luetmer P, Edwards W, Seward J, Tajik AJ (1986) Incidence and distribution of left ventricular false tendons: an autopsy study of 483 normal human hearts. J Am Coll Cardiol 8:179–183 18. McElhinney DB, Silverman NH, Brook MM, Hanley FL, Stanger P (1999) Asymmetrically short tendinous cords causing congenital tricuspid regurgitation: improved understanding of tricuspid valvar dysplasia in the era of color Xow echocardiography. Cardiol Young 9:300–304 19. Moore KL, Dalley AF II (eds) (2006) Clinically oriented anatomy, 5th Edn. Lippincott Williams & Wilkins, Baltimore, pp 147–156 20. Moorman AFM, ChristoVels VM (2003) Development of the cardiac conduction system: a matter of chamber development. In: Chawdick DJ, Goode J (eds) Development of the cardiac conduction system. Wiley, New York, pp 25–34 21. Moorman AFM, ChristoVels VM (2003) Cardiac chamber formation: development, genes, and evolution. Physiol Rev 83:1223– 1267 22. Moreno R, Zamorano J, Ortega A, Villate A, Almeria C, Herrera D, Rodrigo JL, Morales R, Sanchez-Harguindey L (2003) Tricuspid valve chordae rupture following pacemaker electrode replacement. Int J Cardiol 87:291–292 23. Mukai S, Fuseno H, Nakamura M, Yoshikawa J, Shomura T (1991) Dilated cardiomyopathy complicated by a pedunculated and mobile left ventricular thrombus on a ruptured false tendon. Chest 99:1042–1043 24. Nigri GR, Di Dio LJ, Baptista CA (2001) Papillary muscles and tendinous cords of the right ventricle of the human heart: morphological characteristics. Surg Radiol Anat 23:45–49 25. Nishimura T, Kondo M, Umadome H, Shimono Y (1981) Echocardiographic features of false tendons in the left ventricle. Am J Cardiol 48:177–183
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Surg Radiol Anat (2008) 30:317–322 26. Perry LW, Ruckman RN, Shapiro SR, Kuehl KS, Galioto FM, Ruckman RN, Shapiro SR (1983) Left ventricular false tendons in children: prevalence as detected by 2 dimensional echocardiography and clinical signiWcance. Am J Cardiol 52:1264–1266 27. Roberts W (1969) Anomalous left ventricular band: an unemphasized cause of a precordial murmur. Am J Cardiol 23:735–738 28. Rosenquist GC, Sweeney LJ (1975) Normal variations in tricuspid valve attachments to the membranous ventricular septum: a clue to the etiology of left ventricle-to-right atrial communication. Am Heart J 89:186–188 29. Ryssing E, Egeblad H, Berning J (1984) False tendons in the left ventricular outXow tract. Clinical and echocardiograhpic manifestations. Dan Med Bull 31:59–62 30. Sethuraman K, Sriram R, Balachandar J (1984) Left ventricular false tendons: echocardiographic incidence in India and clinical importance. Int J Cardiol 6:385–387 31. Skwarek M, Hreczecha J, Grzybiak M, Kosinski A (2005) Remarks on the morphology of the papillary muscles of the right ventricle. Folia Morphol 64:176–182 32. Skwarek M, Hreczecha J, Dudziak M Grzybiak M (2006) The morphology of the right atrioventricular valve in the adult human heart. Folia Morphol 65:200–208 33. Standring S (ed) (2005) Gray’s anatomy, 39th edn. Elsevier, Edinburgh, pp 1001–1008 34. Suwa M, Hirota Y, Nagao H, Kino M, Kawamura K (1984) Incidence of the coexistence of left ventricular false tendons and premature ventricular contractions in apparently healthy subjects. Circulation 70:793–798 35. Winrow D, Beckmann CF, Lacomis JM, Dedrick CG (1996) Entanglement of a pigtail catheter by the chordae tendineae of the tricuspid valve during pulmonary angiography. Cardiovasc Intervent Radiol 19:275–277
