C 2009, Wiley Periodicals, Inc.
DOI: 10.1111/j.1540-8175.2009.01013.x
ECHO ROUNDS Section Editor: Edmund Kenneth Kerut, M.D.
Normal Anatomic Variants on Transthoracic Echocardiogram Anil George, M.D.,∗ Anoop Parameswaran, M.D., M.P.H.,† Raj Nekkanti, M.D.,∗ Karen Lurito, M.D.,∗ and Assad Movahed, M.D.∗ ∗
East Carolina Heart Institute, East Carolina University, Greenville, North Carolina; and †Heart and Vascular Institute, Department of Cardiology, Albert Einstein Medical Center, Philadelphia, Pennsylvania Apart from their existence as medical curiosities, anatomic variants also double as diagnostic dilemmas. In the heart, more than in any other location in the body, misinterpretation of normal anatomic variants as pathologic entities can have a profound impact on treatment decisions and clinical consequences. Echocardiography is an easily accessible tool these days and is used routinely in most cardiac evaluations. Thus it becomes imperative for the echocardiographer to be cognizant of normal anatomic variants. Furthermore, echocardiographic findings should always be evaluated in their proper clinical context and diagnoses should never be entertained in a clinical vacuum. The literature is replete with numerous case reports and vignettes on these fascinating structures but is lacking in a formal review of normal anatomic variants. In this article, we have attempted a systemic review of normal variants, their embryologic origins, echocardiographic characteristics, and common pitfalls encountered in their evaluation. (ECHOCARDIOGRAPHY, Volume 26, October 2009) normal variant, transthoracic echocardiogram, Chiari network, embryology Introduction Anatomic variants exist throughout the body, and the heart is no exception. However, in this location, they may be confused with pathologic structures related to cardiac or extra cardiac disease processes. Furthermore, the ability to distinguish normal anatomic variants from pathologic structures as an essential skill for the echocardiographer cannot be over emphasized, given the ramifications on treatment decisions. Quite often, normal anatomic variants in the heart are misinterpreted as tumors (masses) or thrombi, diagnoses that portend adverse prognoses. As newer imaging equipment offers higher resolution, such diagnostic ambiguities have become more frequent, and thus the need for the echocardiographer to be more aware of normal variants. The literature perNo potential conflict of interest relevant to this article is reported. Address for correspondence and reprint requests: Assad Movahed, M.D, F.A.C.P., F.A.C.C., East Carolina Heart Institute, East Carolina University, Room 1348, 115 Heart Drive, Greenville, NC 27834. Fax: 252-744-5884; E-mail:
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taining to normal anatomical variants is replete with numerous case reports and short descriptives. This review thus hopes to serve as a comprehensive narrative on the various commonly encountered anatomical variants, their embryologic origins, and their echocardiographic characteristics with pointers that might help in differentiating them from pathologic conditions. Definition of Anatomic Variant For the purpose of this discussion, a definition of anatomic normality is warranted. Studies pertaining to coronary artery anomalies have defined normality as that which is observed in at least 1% of unselected cases. Thus, normal variants (variations within normality) and less frequently encountered morphologies (anomalies) do not necessarily denote disease or pathology.1–3 The anatomic variants will be grouped by the cardiac chambers in which they are commonly encountered. A brief introduction is provided on the key anatomic, embryological, and echocardiographic features pertaining to each. We will then describe the transesophageal echocardigraphic (TEE) findings used to
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confirm some of these variants, since this has been demonstrated to be a superior modality to transthoracic echocardiography, especially for right atrial lesions or masses.4,5 The right atrium is the chamber that is the most common source of anatomic variants leading to misinterpretation on echocardiograms.6
compared to the Chiari network and lacks fenestrations.15 Confirmation of Chiari network can be done by transesophageal echocardiogram (TEE) in the right ventricular inflow view (Fig. 1) which renders images with much better quality and usually shows a broad based attachment with a filamentous and fenestrated appearance.16,17
Chiari Network Case: A 35-year-old female presents with complaints of chest pain. A TTE is obtained as part of the workup which reveals multiple filiform structures in the right atrium. Clinically the patient appears nontoxic and lacks stigmata of endocarditis. Chiari network is named after Hans Chiari (1851–1961), a Viennese physician, more famous for his contributions to neurosurgery.7 Chiari network refers to the presence of strands and reticula in an extensive network formation on the right side of the heart with attachments to the superior vena cava and to the tubercle of Lower (tuberculum intervenosum), a slight projection on the wall of the right atrium between the orifices of the vena cava.8,9 Right atrial strands have been named Chiari’s net, Chiari’s networks, Chiari network retinaculum, and Chiari remnant by various investigators. Bhatnagar et al. have suggested “right atrial net” as a more inclusive terminology for all these structures characterized by strands and fibers interconnecting the crista terminalis, the interatrial septum, inferior vena cava, and coronary sinus valves, or fenestrations of these valves.10 Embryologically, it is thought to represent one of the various forms of the eustachian valve (valve of the inferior vena cava) when it consists of interlacing fibers.9,11 It has a pathologic incidence of 2–3%.12 On TTE, Chiari network is characterized by discrete, highly mobile, highly reflective, curvilinear echoes located toward the posterior right atrium seen best usually in the longaxis parasternal view.13 Similar echo targets can be produced by right-heart vegetation, flail tricuspid leaflet, ruptured chordae tendinae to the tricuspid apparatus, a small right-heart thrombus, or a pedunculated right-heart tumor.13 Chiari network must also be differentiated from cor triatriatum dexter, a condition which occurs when there is persistence of the entire right sinus venosus valve.14 In this rare condition, a valve extends from the ostium of the inferior vena cava to the interatrial septum below the fossa ovalis. However, this is thicker 1110
Eustachian Valve Case: A mobile echo target is seen on a routine TTE obtained as part of workup for a 64-yearold male prior to initiation of chemotherapy for acute leukemia. The eustachian valve also known as valvula venae cavae inferioris is an embryologic remnant of the right valve of sinus venosus. In fetal life, it directs oxygenated blood from the inferior vena cava across the patent foramen ovale into the systemic circulation. Anatomically, it is a semilunar musculo-membraneous fold that extends posteriorly from the limbus fossa ovalis and anteriorly to the inferior vena caval orifice where it disappears.8,18 The eustachian valve is best identified in subcostal views imaging the inferior vena cava entering the right atrium. It appears as a linear partly mobile echo attached to the anterior rim of the inferior vena caval orifice (Fig. 2).19–21 Additionally, in the parasternal short-axis view, the eustachian valve can be visualized alongside the entry of the inferior vena cava into the right atrium. In the apical four-chamber view, the base of valve can be seen as a transverse fixed linear echo in the right atrium.22 A prominent eustachian valve on echo can be mistaken for a right atrial tumor, thrombus, renal cell carcinoma, or other cancers invading the inferior vena cava.22 Thrombus attached to the eustachian valve has also been described.23,24 Additionally, infective endocarditis involving the eustachian valve itself has been reported in injection drug users who are more prone, as the eustachian valve behaves as a nidus for vegetations.25–31 When TTE is inconclusive, a TEE should be performed with the caveat that although the eustachian valve should be considered a normal structure with significant variability in echocardiographic appearance, it is susceptible to pathological involvement. Because it is a right atrial structure, the eustachian valve is best visualized in the right ventricular inflow view.
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Figure 1. Chiari network seen on the bicaval view on TEEright ventricular inflow view.
Figure 4. Atrial septal aneurysm seen in a subcostal view on TEE. Notice bulging of the interatrial septum (IAS). LA = left atrium; LV = left ventricle; RA = right atrium; RV = right ventricle.
Thebesian Valve Case: A semicircular flap is visualized on TEE performed on a 32-year-old female as part of her workup for fever of unknown origin. The clinical concern is infective endocarditis. The coronary sinus, the main venous channel of the heart, empties into the right atrium through an opening that is partially guarded by an incompetent valve, the thebesian valve named after Adam Christian Thebesius.8,32 The valve, which always contains muscle fibers,
Figure 2. Eustachian valve on the right ventricular inflow view on TTE.
Figure 3. Thebesian valve (ThV) on TEE at the gastro– esophageal junction. RA = right atrium; RV = right ventricle; CS = coronary sinus.
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Figure 5. Arrows point to crista terminalis extending across the right atrium (RA) to the inferior vena cava (IVC) on the TTE subcostal view (Source: McKay T, et al. Eur J Echocardiogr 2007 8:288–291; doi:10.1016/j.euje.2006.03.006).
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varies in its extent from a flap that covers the ostium of the coronary sinus to a few strands of tissue.33 Numerous anatomical variations of the valve have been described.34 Embryologically, the thebesian valve represents the right valve of the sinus venosus.35 The thebesian valve can be seen as a semilunar or semicircular endocardial flap of variable length visualized best in the right heart inflow view.36 A fenestrated or trabeculated variant of the thebesian valve has been known to cause obstruction to the passage of the wires in retrograde coronary sinus access.37 On TEE, the thebesian valve is best seen with the TEE probe at the gastroesophageal junction where the coronary sinus can be seen draining into the RA (Fig. 3).
oventricular node. Embryologically, the crista terminalis develops from the regression of the septum spurium as the sinus venosus is incorporated into the right atrial wall.35 The process of regression varies in adults and if the crista terminalis is prominent superiorly it may be mistaken for a right atrial mass.46,47 However, the simultaneous visualization of the superior vena cava in the same image suggests that the “mass” is a prominent crista terminalis.46 Further confirmation can be obtained by TEE (bicaval view) as well as by magnetic resonance imaging/Cine magnetic resonance imaging.48,49 On TEE, the crista terminalis can be distinguished by its linear shape and location between the right sides of the two venacaval orifices (Fig. 5).50
Atrial Septal Aneurysm Case: A “mass” was seen bulging in and out of the left atrium in the parasternal long-axis view in a 65-year-old male patient admitted with hemorrhagic cerebrovascular accident. Atrial septal aneurysm, characterized by a bulging atrial septal shift, is an abnormality of uncertain clinical significance encountered in adults and is thought to be a risk factor for cardiogenic embolism especially when associated with shunts.38,39 Pearson et al. have suggested a septal excursion of >10 mm into either the left or right atrium or a sum of the total excursion into the left or right atrium of >10 mm, with a base width of >15 mm.40 TEE (subcostal view) is superior to TTE for diagnosing atrial septal aneurysm which needs to be distinguished from other right atrial lesions such as solid tumors (Fig. 4). Known associations with this condition include arrhythmias, mitral valve prolapse, Type II atrial septal defect, and patent foramen ovale.38,41–43
Moderator Band Case: A 24-year-old female who is an intravenous drug abuser undergoes a TTE as part of her evaluation for persistent bacteremia. Findings on echo suggest a right ventricular apical lesion. The moderator band is a prominent muscular band in the right ventricle that connects the septum to the base of the anterior papillary muscle and carries the right bundle branch within it.45 Morphologically, it varies from being a clearly evident muscle bundle to a prominent muscular ridge (crista septo-marginalis) to being completely absent.8 Embryologically, the moderator band forms as a result of right ventricular chamber expansion near the atrioventricular canal and dorsal interventricular muscular septum.35 On TTE, the moderator band can be visualized consistently in the apical four chamber view (Fig. 6).22
Crista Terminalis
Lipomatous Hypertrophy of the Interatrial Septum
Case: A 52-year-old man who has been recently diagnosed with lung cancer undergoes a TTE which shows a possible right atrial tumor. Anatomically the crista terminalis refers to the smooth fibro-muscular boundary that separates the trabeculated right atrium from the smooth walled sinus venarum.44,45 It extends superiorly from the junction of the superior vena cava and the right atrium and runs along the lateral right atrial wall to terminate inferiorly at the anterior edge of the inferior venacaval opening.8 It contains fibers that carry impulses from the sinoatrial node to the atri-
Case: A 65-year-old obese female with metastatic breast cancer undergoes a TTE prior to initiation of chemotherapy for her malignancy. A dumbbell-shaped lesion in the interatrial region raises concerns of cardiac involvement. Lipomatous hypertrophy of the atrial septum is a poorly understood condition which is defined as any deposit of fat in the atrial septum that exceeds 2 cm in thickness.51 Since the fossa ovalis itself is spared, fat deposition in the atrial septum results in a dumbbellshaped thickening of the postero-superior and
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Figure 6. Moderator band seen in the apical four-chamber view on TTE.
Figure 8. Coumadin ridge seen on the midesophageal view on TEE.
antero-inferior atrial septum.22,52 Fyke et al. have suggested an atrial septal thickness of 15 mm or more, hypertrophy resulting in bilobed appearance sparing the fossa ovalis and exclusion of other causes of atrial thickening as criteria for diagnosing Lipomatous hypertrophy of the atrial septum.53 This finding is best diagnosed in a subcostal four-chamber view (Fig. 7). Differential diagnosis consists of other causes of atrial septal thickening such as amyloid, atrial
Figure 9. Left ventricular chord is demonstrated on an offaxis apical four-chamber view on TTE.
Figure 7. Apical four-chambered view on TTE showing lipomatous hypertrophy of interatrial septum (arrows); LA = left atrium; LV = left ventricle; RA = right atrium; RV = right ventricle (Source: Nadra I, et al. Heart 2004;90:e66).
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Figure 10. Lambl’s excrescence seen on the midesophageal view on TEE.
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myxoma, true lipoma, and neoplastic processes (rare).54
TABLE I Differential Diagnosis of LVOT Echoes
Coumadin Ridge Case: An 80-year-old woman undergoes a TTE as part of her workup for new onset atrial fibrillation. A left atrial thrombus is suggested on the echo. Coumadin (warfarin) ridge is the term used to describe a distinct muscular ridge within the left atrium located between the left atrial appendage and the atrial insertion of the left superior pulmonary vein.55 This structure can extend into the left atrium and can be mistaken for a thrombus, thereby resulting in unnecessary anticoagulation and hence the name, Coumadin ridge.48,56 Careful evaluation of the structure with TEE in the midesophageal twochamber view at 90 degrees, comparing its relation to the surrounding landmarks, should confirm the diagnosis (Fig. 8). Administration of microbubble contrast agent can aid in differentiating left atrial masses from normal structures such as pectinate muscles by visualization of the filling defects which are present with masses.57 Left Ventricular Bands Case: A 12-year-old boy undergoes a TTE as part of a workup for persistent fever. Chord like structures in the left ventricle raise concerns of endocarditis. Normal chordae tendinae originate from one of the two left ventricular papillary muscles and insert on one of the two mitral leaflets.45 Left ventricular bands refer to fibro muscular bands that pass between papillary muscles, from papillary muscles to the ventricular septum, from free wall to free wall, or from free wall to ventricular septum.58 Other terms commonly used to describe these structures include anomalous left ventricular chordae tendinae, cords, tendinal cords, false chordae, false tendons, and moderator bands to name a few.59 Although originally observed over a century ago and considered, not clinically significant except as the cause of flow murmurs, they have assumed importance as they can be mistaken for pathologic lesions on TTE.60,61 Embryologically, left ventricular bands are thought to originate from the inner muscle layer of the primitive heart.62 The bands may be transverse, longitudinal, or sagittal, according to their orientation in the left ventricle.63 1114
Analysis of echoes Timing in cardiac cycle Appearance Attachments Corroborating echocardiographic signs Clinical presentation (e.g., fever with endocarditis) Modified from Choo, et al, Angiology 33:756, 1982
They appear as linear, string-like, filamentous, or thin bands on echo with characteristic behavior muscular bands become shorter and thicker; tendinous bands become loose and curved in systole, but taut and straight during diastole (Fig. 9).22,64 Manipulation of the transducer with rotation and angulation to obtain several views from the same position reveals echo-free space on both sides of the structure which helps confirm the diagnosis.65 The echocardiographer is often challenged to differentiate these bands from pathologic entities such as subaortic membrane, aortic or mitral vegetation, flail aortic or mitral valve leaflet, pedunculated tumors or thrombi, and aneurysm of sinus of Valsalva.22 To avoid mistakes Choo et al. have suggested a systematic approach (Table I) to left ventricular outflow tract echoes.66 Lambl’s Excrescences Case: An 80-year-old man undergoes a TEE as part of his workup for fever of unknown origin. Mobile strands are seen on the aortic valves which raise suspicion of endocarditis. Lambl’s excrescences are thin mobile filiform structures that occur most commonly on the ventricular side of the aortic valve and on the atrial side of the mitral valve usually along the valve closure line.67–69 Originally described by Vilem Dusan Lambl, they may occur as a single strand or in rows or clusters and have been known to involve other valves as well.67 They consist of a fibroelastic, avascular connective tissue core covered by a single layer of endothelial cells and range in thickness up to 1 mm and can be 1–5 mm long.67,69 Lambl’s excrescences can be best identified on TEE along the valve closure lines of the aortic and mitral valve as fine thread-like strands which are hyper mobile (Fig. 10).70 They have to be distinguished from fibroelastomas which are usually larger and pedunculated and may produce embolic symptoms.
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Conclusion Although echocardiography is a powerful tool, the presence of anatomical variants in the heart presents challenges in distinguishing the pathologic from what is normal but uncommon. Despite their rarity, misinterpretations of these structures on echo can lead to costly mistakes which translate into unnecessary and sometimes dangerous therapy or surgical intervention. Anticoagulation for misdiagnosed right atrial thrombi, valvular surgery for presumed vegetations, and cardiac surgery for misdiagnosed tumors are painful examples with potential legal ramifications for the medical team. In such circumstances, further confirmation of the diagnosis should be sought with alternate imaging techniques such as magnetic resonance imaging or computed tomography especially when tumor or malignancy is a consideration. The importance of interpreting imaging results with careful attention to the clinical scenario cannot be overemphasized. In many instances, TEE is able to provide a definitive diagnosis aided by the additional views afforded to the echocardiographer. The above discussion on normal variants can potentially help avoid diagnostic pitfalls especially by the novice echocardiographer by making them cognizant of these rather uncommon entities.
9. 10. 11. 12. 13.
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18. 19.
20. Acknowledgments: We thank Mr. Jerome Fuller for his invaluable help in the preparation of the images for this article.
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