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Echocardiographic characteristics of the criss-cross heart
International Journal of Cardiology 140 (2010) 133–137
Contents lists available at ScienceDirect
International Journal of Cardiology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j c a r d
Editorial
Echocardiographic characteristics of the criss-cross heart Ya-Li Yang a, Xin-Fang Wang a, Tsung O. Cheng a,b,⁎, Ming-Xing Xie a, Qing Lü a, Lin He a, Xiao-Fang Lu a, Jing Wang a, Ling Li a, Robert H. Anderson c a Department of Ultrasonography, Union Hospital of Tongji Medical College, Huazhong University of Science and Technology, Hubei Provincial Key Laboratory of Molecular Imaging, Wuhan 430022, China b Department of Medicine, George Washington University Medical Center, 2150 Pennsylvania Avenue, N.W., Washington, D.C. 20037, USA c Cardiac Unit, Institute of Child Health, University College, London, UK
a r t i c l e
i n f o
Article history: Received 17 August 2009 Accepted 20 August 2009 Available online 16 September 2009 Keywords: Echocardiography Criss-cross heart Crossing atrioventricular connections Superoinferior ventricles Congenital heart disease
a b s t r a c t Objective: To assess the ultrasonic characteristics of the criss-cross heart, and explore the value of echocardiography in the diagnosis of this rare congenital cardiac defect. Methods: We reviewed the echocardiographic findings in 4 patients having criss-crossed atrioventricular connections at our hospital, and compared the findings with observations at surgery in 3 of the patients. Results: In all 4 patients, there was usual atrial arrangement, right hand ventricular topology, and concordant atrioventricular connections. The inlet components of the ventricular mass, however, crossed such that the apical component of the morphologically right ventricle was situated anteriorly and superiorly, and extended to the left relative to the apex of the morphologically left ventricle. The ventriculo-arterial connections were concordant in 1 patient, double outlet from the morphologically right ventricle in 2, and discordant in the other. In all 4 patients, it proved impossible to obtain the standard 4-chamber view showing simultaneously all four chambers and both atrioventricular valves. A series of apical 4-chamber or subcostal coronal views, obtained by tilting the transducer from posterior to anterior, demonstrate initially the connection of the leftsided left atrium and the right-sided left ventricle through the mitral valve. More anterior angulation of the transducer then showed the right-sided right atrium to be connected to the left-sided right ventricle through the tricuspid valve, confirming the presence of twisted atrioventricular connections. Color Doppler imaging displayed the crossing of the atrioventricular connections without mixing of the streams. Short-axis views across the ventricular mass confirmed that the right ventricle was superior, anterior, and to the left of the left ventricle, and demonstrated the horizontal position of the ventricular septum. When viewed subcostally, the distance between the tricuspid valve and the orifice of the inferior vena cava was significantly increased relative to normal findings. The echocardiographic findings were confirmed during surgical interventions in 3 patients, apart from the failure to diagnose one instance of persistent patency of the left superior vena cava. Conclusions: The failure to obtain a characteristic 4-chamber view in any cut was diagnostic for recognition of the criss-crossed atrioventricular junctions. Transthoracic echocardiography provides definitive images of this rare arrangement, and accurately defines the associated cardiac abnormalities. © 2009 Published by Elsevier Ireland Ltd.
1. Introduction Criss-cross heart, a term first coined in 1974 by Anderson et al. [1], and Ando et al. [2], is a rare arrangement in congenitally malformed hearts, the atrioventricular connections crossing at the level of the atrioventricular junctions such that the apical components of the ventricles occupy unexpected positions. Its frequency is no more than 8 per 1,000,000, and it is found in less than 0.1% of congenitally malformed hearts [3]. To date, nonetheless, at least 150 cases are described in the literature [4], and it has been shown that the essence
⁎ Corresponding author. The George Washington University Medical Center, 2150 Pennsylvania Avenue N.W., Washington, D.C. 20037, USA. Tel.: +1 202 741 2426; fax: +1 202 741 2324. E-mail address: [email protected] (T.O. Cheng). 0167-5273/$ – see front matter © 2009 Published by Elsevier Ireland Ltd. doi:10.1016/j.ijcard.2009.08.039
of the lesion is twisted atrioventricular connections [5]. Patients with the criss-cross arrangement usually have numerous coexisting cardiac defects, such that accurate diagnosis is a significant challenge. Most patients are usually described as case reports, and it is unusual to find series of patients in whom the echocardiographic findings have been analyzed in detail. We describe here the echocardiographic results of 4 patients found to have the criss-cross arrangement subsequent to admission to the Union Hospital. 2. Materials and methods 2.1. Patient population Between April, 2002, and June, 2009, we observed twisted atrioventricular connections in 3 male and 1 female patients admitted
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Y.-L. Yang et al. / International Journal of Cardiology 140 (2010) 133–137
Table 1 Echocardiographic results and operative findings in patients with criss-cross heart. Patients Sex Age 1 2
F M
3 4
M M
Cardiac location
6 years Levocardia 2 months Ectopia cordis 4 months Mesocardia 2 years Levocardia
Atrial Situs
Ventricular A-V loop connection
Solitus D-loop Solitus D-loop Solitus D-loop Solitus D-loop
V-A connection
Associated cardiac anomalies
Concordant DORV VSD, ASD, PS Concordant Concordant VSD, ASD, hypoplastic TV and RV, PS Concordant TGA VSD, multiple ASD, PS, DA Concordant DORV VSD, PFO, PS, DA
Surgery
Operative findings
Glenn anastomosis None
Same /
Switch operation Total cavopulmonary anastomosis
Same LSVC, the others same
A-V: atrio-ventricular; ASD: atrial septal defect; DA: dextroaortic arch; DORV: double-outlet right ventricle; LSVC: persistent left superior vena cava; PFO: patent foramen ovale; PS: pulmonary stenosis; RV: right ventricle; TGA: complete transposition of great arteries; TV: tricuspid valve; V-A: ventriculo-arterial; VSD: ventricular septal defect.
to the Union Hospital, Wuhan. Their age at presentation ranged from 2 months to 6 years, with a median of 2.1 years. Their chief complaints were cyanosis when crying or exercising in 3 cases, palpitation and chest distress in 2 cases, and an extrathoracic location of the heart in one case. The routine physical examination revealed systolic cardiac murmurs at the left upper sternal border and/or cardiac apex. All patients underwent chest X-rays examination, electrocardiography, and echocardiography. The diagnosis was confirmed by intraoperative findings in 3 patients, while the patient with the ectopic heart was discharged from the hospital without operation, in accordance with the wishes of the family. 2.2. Echocardiography All 4 patients underwent a complete transthoracic cross-sectional and Doppler echocardiographic examination using a cardiac ultrasound system (GE Vivid 7, Vingmed, Horten, Norway/GE Vivid 7 Dimension, Vingmed, Horten, Norway/Philips IE 33, Andover, MA, USA) with a 3.5–7.5 MHz probe. The anatomical and haemodynamic abnormalities were observed by following the strict sequential segmental approach. The key planes included parasternal long-axis and short-axis views of the ventricles, apical 4-chamber views, apical 5-chamber views, subcostal coronal views, and some modified, nonstandard views showing the relative positions of the atrioventricular junctions. All cardiac segments, their arrangement, relations, and connections were thoroughly identified and reviewed. In particular, we documented the spatial arrangement of the atrioventricular connections, the relative location of the atrial and ventricular chambers in space, the orientation of the ventricular septum, the ventricular morphology, and the attachments and morphology of the atrioventricular valves. All associated malformations were recorded. The
echocardiographic characteristics were compared with the results obtained at surgery in the 3 patients undergoing surgical intervention. 3. Results We have summarized the echocardiographic and surgical findings in Table 1. All 4 patients had usual atrial arrangement and right hand ventricular topology (D ventricular loop) with concordant atrioventricular connections. In each case, however, the atrioventricular junctions crossed such that the apical component of the morphologically right ventricle was situated anteriorly, superiorly, and in part to the left of the apical component of the morphologically left ventricle. The ventriculo-arterial connections were concordant in 1 patient with an overriding aortic valve, double outlet from the morphologically right ventricle with an anterior aorta in 2, and discordant in the other. All 4 patients had interatrial communications within the oval fossa or probe patency of the oval foramen, ventricular septal defects, and pulmonary stenosis. In 2 patients, the aortic arch was right-sided, while individual patients had hypoplasia of the tricuspid valve and right ventricle, thoraco-abdominal exteriorization of the heart, and persistent patency of the left superior vena cava, respectively. The echocardiographic diagnosis of the criss-cross arrangement, and the associated cardiac abnormalities, were confirmed during surgical intervention in 3 patients, apart from the persistent left superior caval vein, which had not been noted preoperatively. We observed several characteristic echocardiographic findings. First, in no patients were we able to obtain a standard 4-chamber view by either subxiphoid or apical scanning. It proved impossible to find a plane showing the four chambers and both atrioventricular valves simultaneously (Fig. 1A). Second, we were unable to show any connection between the atrium and the ventricle on the same side,
Fig. 1. Subcostal coronal sections by echocardiography. A shows 4 chambers, and it seems that the atrioventricular connections are discordant. Note, however, that the two atrioventricular valves are not imaged clearly, and the two ventricular apexes are separate. B demonstrates the connection of the left-sided left atrium (LA) and the right-sided left ventricle (LV) through mitral valve. With anterior tilting from B, C demonstrates the connection of the right-sided right atrium (RA) and the left-sided right ventricle (RV) through the tricuspid valve. The atrioventricular connections are concordant. The arrows in B and C indicate the openings of the two valves, which cross each other.
Y.-L. Yang et al. / International Journal of Cardiology 140 (2010) 133–137
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Fig. 2. Color Doppler imaging displays the blood flows through the mitral valve (left) and tricuspid valve (right), which cross each other without mixing at the level of the atrioventricular junctions.
but rather found extensive mural contact, as opposed to cavity connection, at the level of the atrioventricular junctions. Only by making a series of apical 4-chamber or subcostal coronal views by tilting the transducer from posterior to anterior were we able to demonstrate, initially, the connection of the left-sided left atrium and the right-sided left ventricle through mitral valve at first (Fig. 1B). A more anterior angulation of the transducer then showed the rightsided right atrium to be connected to the left-sided right ventricle (Fig. 1C). In all patients, therefore, the sweeps showed the atrioventricular connections to be concordant, but crossing in terms of their spatial location. Color Doppler imaging displayed the twisted nature of the atrioventricular junctions, without mixing at the level of the atrioventricular valves (Fig. 2). By translational movement of the transducer from the level of the atrioventricular valves to the apex, with the signature pointed to 12 o'clock, the series of the ventricular short-axis views obtained displayed the right ventricle to be superior to the left ventricle, with the ventricular septum in horizontal position. We also noted an elongated distance between the orifices of the tricuspid valve and inferior vena cava when seen in the subcostal view, reflecting the anterior displacement of the tricuspid valve. All patients had associated huge perimembranous ventricular septal defects. 4. Discussion The anatomico-pathological feature of the criss-cross arrangement is the crossing of the blood streams at the level of the atrioventricular junctions such that each atrium connects to a ventricle on the other side of the body when assessed in the antero-posterior projection (Fig 3). This anomaly is generally considered to be caused by
abnormal clockwise or counter-clockwise rotation of the ventricular loop along its long axis, while the atrial chambers and the base of the heart remain relatively fixed. The end result is to produce twisted atrioventricular connections [5]. The etiology and the stage of embryologic development of the abnormal arrangement have yet to be elucidated, although some authors have made an effort to establish the morphogenesis from gene mutation [6]. The direction of the ventricular rotation is relative to the atrial arrangement, and the specific atrioventricular connections. For example, in patients with usual atrial arrangement and concordant atrioventricular connections, the morphologically right ventricle is unusually situated to the left of the morphologically left ventricle, which implies a clockwise rotation of the ventricles around the apex– base axis as seen from the apex. When the atrioventricular connections are discordant with usual atrial arrangement, then the morphologically right ventricle is typically found to the right of the morphologically left ventricle, implying a counter-clockwise rotation around the same axis. In other words, the unusual twisting of the ventricular mass occurs in such a fashion to place the right ventricular inlet superior and anterior to the left ventricular inlet [7]. In a few cases, nonetheless, opposite twisting has been observed such that the right ventricular inlet is positioned inferior and posterior relative to the left ventricular inlet [8,9]. In general, rather than the two inlets being parallel one to the other, they are positioned superoinferiorly, this feature accounting for the inability to image the four chambers and the two atrioventricular valves in the same plane simultaneously. This inability is the most important diagnostic feature of the crisscross arrangement. Tilting of the transducer from posterior, inferior to anterior, superior in continuous apical 4-chamber or subcostal coronal views, nonetheless, shows the two inflow tracts occupying separate
Fig. 3. The anatomic diagrams of criss-cross heart with double-outlet right ventricle. A shows the surface view from the right side. The RV is located anteriorly, superiorly and to the left of the LV. B shows the connection of the RA and the RV through the tricuspid valve (TV) and C shows the connection of the LA and the LV. D shows the casting figure displaying the right outlet crossing in front of the left outlet.
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planes, with each atrium joining a ventricle on the opposite side. Color flow mapping allows visualization of the crossover of the inflow streams, with no mixing, confirming the diagnosis of the criss-cross arrangement, and excluding the possible alternative diagnosis of absent atrioventricular connection or double-inlet ventricle. Our own experience, combined with analysis of previous case reports [10–12], leads us to conclude that the imaging of the two atrioventricular inlets on different planes, with one inlet crossing in front of the other, is the definitive diagnostic feature. Real-time echocardiography is the optimal technique providing a continuous sweep from posterior to anterior, and instantly revealing the abnormal superoinferior relationships of the junctions. Since the right ventricular inlet is located superiorly in most instances, it means that the left inlet is demonstrated first, and then the right inlet is shown with a more anterior angulation. This maneuver helps the operator to define the ventricular locations, and determine the twisted nature of the atrioventricular connections. The criss-cross arrangement is usually found in patients with biventricular atrioventricular connections, albeit also being seen in patients with double-inlet ventricle [13,14]. In the latter situation, the two atrioventricular valves connect with the dominant ventricle, but the right valve is located anteriorly and superiorly relative to the left valve, with the axes of the streams from the atrial chambers crossing within the dominant ventricle [13]. A superoinferior relationship of the ventricles is another feature of the criss-cross arrangement, hence the alternative description of superoinferior ventricles, or upstairs–downstairs heart. In all our cases, the morphologically right ventricle was superior to the left ventricle, and the ventricular septum was nearly horizontal. It has been shown [15,16], nonetheless, that other ventricular arrangements can be seen in the setting of criss-cross hearts. For example, the muscular ventricular septum can be oriented semivertically, while in some patients, the ventricles have been shown to be side-by-side, with a vertically oriented septum. Superoinferior ventricles can also be found in isolated cases without any ventricular rotation along the long axis, as in those with congenitally corrected transposition [12]. In fact, less than half of one series of patients described with superoinferior ventricles also exhibited the criss-cross arrangement [17]. A superoinferior arrangement of the ventricles, and a horizontal orientation of the muscular ventricular septum, therefore, should not be considered diagnostic features of the criss-cross arrangement. It is important to take note of ventricular topology when diagnosing the criss-cross arrangement. Ventricular topology described the handedness of the ventricular mass, irrespective of its location in space [18]. In most examples of patients having the criss-cross arrangement, the ventricular topology is as expected for the particular atrioventricular connections, despite the unusual spatial location of the ventricles relative to each other, this reflecting the twisted atrioventricular connections. In rare instances, however, there can be disharmony between the atrial arrangement and the ventricular topology in the setting of twisted atrioventricular connections, such that left hand ventricular topology is seen in the setting of usual atrial arrangement despite the presence of concordant atrioventricular connections [9]. This means that, in some instances, it will be essential to describe both the specific atrioventricular connections and the ventricular topology. Apart from these rare exceptions, nonetheless, the ventricular topology can be inferred from the pattern of atrioventricular connections by noting the twisted nature of the atrioventricular junctions. A review of 83 cases with the criss-cross arrangement by ValdesCrus and Cayre [19] revealed that all but one-twentieth had usual atrial arrangement, four-fifths had left-sided hearts and concordant atrioventricular connections, with just over half having discordant ventriculo-arterial connections, and almost one-third having double outlet from the morphological right ventricle. Pulmonary stenosis was also present in more than half of the cases, with integrity of the ventricular septum being very rare [20,21].
Of the associated anomalies, 2 deserve special emphasis. The first is hypoplasia of the tricuspid valve and right ventricle, found in 1 of our 4 patients. Marino et al. [22] found that the angle between the long axes of the atrioventricular valves correlated inversely with the size of the apical component of the right ventricle. The size and morphology of the tricuspid valve and the right ventricle should be accurately assessed preoperatively by echocardiography for planning of the optimal operative repair. The other notable feature is straddling of an atrioventricular valve. Echocardiography is known to be superior to angiography in the diagnosis of the valvar anomalies [7]. Indeed, the criss-cross arrangement with atrioventricular valvar straddling has now been detected during fetal life [23]. It is worth noting that the detection of a straddling valve is dependent on the experience of the operator. We suggest that the visualization of the two atrioventricular valvar attachments should be a routine in imaging the hearts with twisted atrioventricular junctions due to its frequent association, especially in patients with a large ventricular septal defect. It is also likely that diagnosis of straddling valves and twisted atrioventricular connections will be facilitated in the future as more centers gain access to magnetic resonance imaging and computed tomography. In conclusion, the failure to obtain a standard 4-chamber view in any cut is very characteristic when making the echocardiographic diagnosis of the criss-cross arrangement. The definitive appearance is twisted atrioventricular connections [5], with each atrium emptying into the ventricle on the opposite side as revealed by continuous subxiphoid or apical scanning. Use of transthoracic echocardiography, therefore, permits accurate diagnosis of this rare cardiac anomaly and the associated cardiac abnormalities. Acknowledgment The authors of this manuscript have certified that they comply with the Principles of Ethical Publishing in the International Journal of Cardiology [24]. References [1] Anderson RH, Shinebourne EA, Gerlis LM. Criss-cross atrioventricular relationships producing paradoxical atrioventricular concordance or discordance. Circulation 1974;50:176–80. [2] Ando M, Takao A, Cho E, et al. Criss-cross heart by abnormal rotation of bulboventricular loop: diagnostic considerations for complex cardiac anomaly. Proc Ped Circ Soc 1974;4:82–3. [3] Fyler DC. Trends. In: Fyler DC, editor. Nanda's pediatric cardiology. Philadelphia, PA: Hanley & Belfus; 1992. p. 273–80. [4] Hoffman P, Szymański P, Lubiszewska B, Różański J, Lipczyńska M, Klisiewicz A. Crisscross hearts in adults: echocardiographic evaluation and natural history. J Am Soc Echocardiogr 2009;22:134–40. [5] Seo J-W, Yoo S-J, Ho SY, Lee HJ, Anderson RH. Further morphological observations on hearts with twisted atrioventricular connections (criss-cross hearts). Cardiovasc Pathol 1992;1:211–7. [6] De Luca A, Sarkozy A, Consoli F, et al. Exclusion of Cx43 gene mutation as a major cause of criss-cross heart anomaly in man. Int J Cardiol Mar 16 2009 Electronic publication ahead of print, doi:10.1016/j.ijcard.2009.02.028. [7] Ekici E. Criss-cross heart with straddling right atrioventricular valve. Clin Cardiol 1984;7:503–8. [8] Seo JW, Choe GY, Ghi JG. An unusual ventricular loop associated with right juxtaposition of the atrial appendages. Int J Cardiol 1989;25:219–28. [9] Anderson RH, Smith A, Wilkinson JL. Disharmony between atrioventricular connections and segmental combinations: unusual variants of “criss-cross” hearts. J Am Coll Cardiol 1987;10:1274–7. [10] Robinson PJ, Kumpeng V, Macartney F. Cross sectional echocardiographic and angiocardiographic correlation in criss-cross hearts. Br Heart J 1985;54:61–7. [11] Van Mill G, Moulaert A, Harinck E, et al. Subcostal two-dimensional echocardiographic recognition of a criss-cross heart with discordant ventriculo-arterial connection. Pediatr Cardiol 1982;3:319–23. [12] Carminati M, Valsecchi O, Borghi A, et al. Cross-sectional echocardiographic study of criss-cross hearts and superoinferior ventricles. Am J Cardiol 1987;59:114–8. [13] Mori K, Harada M, Kuroda Y. Twisted atrioventricular valves in double inlet left ventricle. Cardiol Young 2002;12:401–3. [14] Kim TH, Yoo SJ, Ho SY, et al. Twisted atrioventricular connections in double inlet right ventricle: evaluation by magnetic resonance imaging. Cardiol Young 2000;10:567–73. [15] Han HS, Seo JW, Choi JY. Echocardiographic evaluation of hearts with twisted atrioventricular connections (criss-cross heart). Heart Vessels 1994;9:322–6.
Y.-L. Yang et al. / International Journal of Cardiology 140 (2010) 133–137 [16] Cantinotti M, Bell A, Hegde S, et al. A segmental approach to criss-cross heart by cardiac MRI. Int J Cardiol 2007;118:e103–5. [17] Anderson RH. Criss-cross hearts revisited. Pediatr Cardiol 1982;3:305–13. [18] Van Praagh S, La Corte M, Fellows KE, et al. Supero-inferior ventricles: anatomic and angiocardiographic findings in 10 postmortem cases. In: Van Praagh R, Takao A, editors. Etiology and morphogenesis of congenital heart disease. Mount Kisco, NY: Futura; 1980. p. 317–78. [19] Valdes-Crus LM, Cayre R. Superoinferior ventricles and crisscross heart. In: ValdesCrus LM, Cayre R, editors. Echocardiographic diagnosis of congenital heart disease. New York: Lippincott-Raven Publishers; 1999. p. 289–94.
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[20] Alday LE, Juaneda E. Superoinferior ventricles with criss-cross atrioventricular connections and intact ventricular septum. Pediatr Cardiol 1993;14:238–41. [21] Fontes VF, de Souza JA, Pontes Jùnior SC. Criss-cross heart with intact ventricular septum. Int J Cardiol 1990;26:382–5. [22] Marino B, Sanders SP, Pasquini L, et al. Two-dimensional echocardiographic anatomy in crisscross heart. Am J Cardiol 1986;58:325–33. [23] Ngeh N, Api O, Iasci A, et al. Criss-cross heart: report of three cases with doubleinlet ventricles diagnosed in utero. Ultrasound Obstet Gynecol 2008;31:461–5. [24] Coats AJ. Ethical authorship and publishing. Int J Cardiol 2009;131:149–50.
Contents lists available at ScienceDirect
International Journal of Cardiology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j c a r d
Editorial
Echocardiographic characteristics of the criss-cross heart Ya-Li Yang a, Xin-Fang Wang a, Tsung O. Cheng a,b,⁎, Ming-Xing Xie a, Qing Lü a, Lin He a, Xiao-Fang Lu a, Jing Wang a, Ling Li a, Robert H. Anderson c a Department of Ultrasonography, Union Hospital of Tongji Medical College, Huazhong University of Science and Technology, Hubei Provincial Key Laboratory of Molecular Imaging, Wuhan 430022, China b Department of Medicine, George Washington University Medical Center, 2150 Pennsylvania Avenue, N.W., Washington, D.C. 20037, USA c Cardiac Unit, Institute of Child Health, University College, London, UK
a r t i c l e
i n f o
Article history: Received 17 August 2009 Accepted 20 August 2009 Available online 16 September 2009 Keywords: Echocardiography Criss-cross heart Crossing atrioventricular connections Superoinferior ventricles Congenital heart disease
a b s t r a c t Objective: To assess the ultrasonic characteristics of the criss-cross heart, and explore the value of echocardiography in the diagnosis of this rare congenital cardiac defect. Methods: We reviewed the echocardiographic findings in 4 patients having criss-crossed atrioventricular connections at our hospital, and compared the findings with observations at surgery in 3 of the patients. Results: In all 4 patients, there was usual atrial arrangement, right hand ventricular topology, and concordant atrioventricular connections. The inlet components of the ventricular mass, however, crossed such that the apical component of the morphologically right ventricle was situated anteriorly and superiorly, and extended to the left relative to the apex of the morphologically left ventricle. The ventriculo-arterial connections were concordant in 1 patient, double outlet from the morphologically right ventricle in 2, and discordant in the other. In all 4 patients, it proved impossible to obtain the standard 4-chamber view showing simultaneously all four chambers and both atrioventricular valves. A series of apical 4-chamber or subcostal coronal views, obtained by tilting the transducer from posterior to anterior, demonstrate initially the connection of the leftsided left atrium and the right-sided left ventricle through the mitral valve. More anterior angulation of the transducer then showed the right-sided right atrium to be connected to the left-sided right ventricle through the tricuspid valve, confirming the presence of twisted atrioventricular connections. Color Doppler imaging displayed the crossing of the atrioventricular connections without mixing of the streams. Short-axis views across the ventricular mass confirmed that the right ventricle was superior, anterior, and to the left of the left ventricle, and demonstrated the horizontal position of the ventricular septum. When viewed subcostally, the distance between the tricuspid valve and the orifice of the inferior vena cava was significantly increased relative to normal findings. The echocardiographic findings were confirmed during surgical interventions in 3 patients, apart from the failure to diagnose one instance of persistent patency of the left superior vena cava. Conclusions: The failure to obtain a characteristic 4-chamber view in any cut was diagnostic for recognition of the criss-crossed atrioventricular junctions. Transthoracic echocardiography provides definitive images of this rare arrangement, and accurately defines the associated cardiac abnormalities. © 2009 Published by Elsevier Ireland Ltd.
1. Introduction Criss-cross heart, a term first coined in 1974 by Anderson et al. [1], and Ando et al. [2], is a rare arrangement in congenitally malformed hearts, the atrioventricular connections crossing at the level of the atrioventricular junctions such that the apical components of the ventricles occupy unexpected positions. Its frequency is no more than 8 per 1,000,000, and it is found in less than 0.1% of congenitally malformed hearts [3]. To date, nonetheless, at least 150 cases are described in the literature [4], and it has been shown that the essence
⁎ Corresponding author. The George Washington University Medical Center, 2150 Pennsylvania Avenue N.W., Washington, D.C. 20037, USA. Tel.: +1 202 741 2426; fax: +1 202 741 2324. E-mail address: [email protected] (T.O. Cheng). 0167-5273/$ – see front matter © 2009 Published by Elsevier Ireland Ltd. doi:10.1016/j.ijcard.2009.08.039
of the lesion is twisted atrioventricular connections [5]. Patients with the criss-cross arrangement usually have numerous coexisting cardiac defects, such that accurate diagnosis is a significant challenge. Most patients are usually described as case reports, and it is unusual to find series of patients in whom the echocardiographic findings have been analyzed in detail. We describe here the echocardiographic results of 4 patients found to have the criss-cross arrangement subsequent to admission to the Union Hospital. 2. Materials and methods 2.1. Patient population Between April, 2002, and June, 2009, we observed twisted atrioventricular connections in 3 male and 1 female patients admitted
134
Y.-L. Yang et al. / International Journal of Cardiology 140 (2010) 133–137
Table 1 Echocardiographic results and operative findings in patients with criss-cross heart. Patients Sex Age 1 2
F M
3 4
M M
Cardiac location
6 years Levocardia 2 months Ectopia cordis 4 months Mesocardia 2 years Levocardia
Atrial Situs
Ventricular A-V loop connection
Solitus D-loop Solitus D-loop Solitus D-loop Solitus D-loop
V-A connection
Associated cardiac anomalies
Concordant DORV VSD, ASD, PS Concordant Concordant VSD, ASD, hypoplastic TV and RV, PS Concordant TGA VSD, multiple ASD, PS, DA Concordant DORV VSD, PFO, PS, DA
Surgery
Operative findings
Glenn anastomosis None
Same /
Switch operation Total cavopulmonary anastomosis
Same LSVC, the others same
A-V: atrio-ventricular; ASD: atrial septal defect; DA: dextroaortic arch; DORV: double-outlet right ventricle; LSVC: persistent left superior vena cava; PFO: patent foramen ovale; PS: pulmonary stenosis; RV: right ventricle; TGA: complete transposition of great arteries; TV: tricuspid valve; V-A: ventriculo-arterial; VSD: ventricular septal defect.
to the Union Hospital, Wuhan. Their age at presentation ranged from 2 months to 6 years, with a median of 2.1 years. Their chief complaints were cyanosis when crying or exercising in 3 cases, palpitation and chest distress in 2 cases, and an extrathoracic location of the heart in one case. The routine physical examination revealed systolic cardiac murmurs at the left upper sternal border and/or cardiac apex. All patients underwent chest X-rays examination, electrocardiography, and echocardiography. The diagnosis was confirmed by intraoperative findings in 3 patients, while the patient with the ectopic heart was discharged from the hospital without operation, in accordance with the wishes of the family. 2.2. Echocardiography All 4 patients underwent a complete transthoracic cross-sectional and Doppler echocardiographic examination using a cardiac ultrasound system (GE Vivid 7, Vingmed, Horten, Norway/GE Vivid 7 Dimension, Vingmed, Horten, Norway/Philips IE 33, Andover, MA, USA) with a 3.5–7.5 MHz probe. The anatomical and haemodynamic abnormalities were observed by following the strict sequential segmental approach. The key planes included parasternal long-axis and short-axis views of the ventricles, apical 4-chamber views, apical 5-chamber views, subcostal coronal views, and some modified, nonstandard views showing the relative positions of the atrioventricular junctions. All cardiac segments, their arrangement, relations, and connections were thoroughly identified and reviewed. In particular, we documented the spatial arrangement of the atrioventricular connections, the relative location of the atrial and ventricular chambers in space, the orientation of the ventricular septum, the ventricular morphology, and the attachments and morphology of the atrioventricular valves. All associated malformations were recorded. The
echocardiographic characteristics were compared with the results obtained at surgery in the 3 patients undergoing surgical intervention. 3. Results We have summarized the echocardiographic and surgical findings in Table 1. All 4 patients had usual atrial arrangement and right hand ventricular topology (D ventricular loop) with concordant atrioventricular connections. In each case, however, the atrioventricular junctions crossed such that the apical component of the morphologically right ventricle was situated anteriorly, superiorly, and in part to the left of the apical component of the morphologically left ventricle. The ventriculo-arterial connections were concordant in 1 patient with an overriding aortic valve, double outlet from the morphologically right ventricle with an anterior aorta in 2, and discordant in the other. All 4 patients had interatrial communications within the oval fossa or probe patency of the oval foramen, ventricular septal defects, and pulmonary stenosis. In 2 patients, the aortic arch was right-sided, while individual patients had hypoplasia of the tricuspid valve and right ventricle, thoraco-abdominal exteriorization of the heart, and persistent patency of the left superior vena cava, respectively. The echocardiographic diagnosis of the criss-cross arrangement, and the associated cardiac abnormalities, were confirmed during surgical intervention in 3 patients, apart from the persistent left superior caval vein, which had not been noted preoperatively. We observed several characteristic echocardiographic findings. First, in no patients were we able to obtain a standard 4-chamber view by either subxiphoid or apical scanning. It proved impossible to find a plane showing the four chambers and both atrioventricular valves simultaneously (Fig. 1A). Second, we were unable to show any connection between the atrium and the ventricle on the same side,
Fig. 1. Subcostal coronal sections by echocardiography. A shows 4 chambers, and it seems that the atrioventricular connections are discordant. Note, however, that the two atrioventricular valves are not imaged clearly, and the two ventricular apexes are separate. B demonstrates the connection of the left-sided left atrium (LA) and the right-sided left ventricle (LV) through mitral valve. With anterior tilting from B, C demonstrates the connection of the right-sided right atrium (RA) and the left-sided right ventricle (RV) through the tricuspid valve. The atrioventricular connections are concordant. The arrows in B and C indicate the openings of the two valves, which cross each other.
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Fig. 2. Color Doppler imaging displays the blood flows through the mitral valve (left) and tricuspid valve (right), which cross each other without mixing at the level of the atrioventricular junctions.
but rather found extensive mural contact, as opposed to cavity connection, at the level of the atrioventricular junctions. Only by making a series of apical 4-chamber or subcostal coronal views by tilting the transducer from posterior to anterior were we able to demonstrate, initially, the connection of the left-sided left atrium and the right-sided left ventricle through mitral valve at first (Fig. 1B). A more anterior angulation of the transducer then showed the rightsided right atrium to be connected to the left-sided right ventricle (Fig. 1C). In all patients, therefore, the sweeps showed the atrioventricular connections to be concordant, but crossing in terms of their spatial location. Color Doppler imaging displayed the twisted nature of the atrioventricular junctions, without mixing at the level of the atrioventricular valves (Fig. 2). By translational movement of the transducer from the level of the atrioventricular valves to the apex, with the signature pointed to 12 o'clock, the series of the ventricular short-axis views obtained displayed the right ventricle to be superior to the left ventricle, with the ventricular septum in horizontal position. We also noted an elongated distance between the orifices of the tricuspid valve and inferior vena cava when seen in the subcostal view, reflecting the anterior displacement of the tricuspid valve. All patients had associated huge perimembranous ventricular septal defects. 4. Discussion The anatomico-pathological feature of the criss-cross arrangement is the crossing of the blood streams at the level of the atrioventricular junctions such that each atrium connects to a ventricle on the other side of the body when assessed in the antero-posterior projection (Fig 3). This anomaly is generally considered to be caused by
abnormal clockwise or counter-clockwise rotation of the ventricular loop along its long axis, while the atrial chambers and the base of the heart remain relatively fixed. The end result is to produce twisted atrioventricular connections [5]. The etiology and the stage of embryologic development of the abnormal arrangement have yet to be elucidated, although some authors have made an effort to establish the morphogenesis from gene mutation [6]. The direction of the ventricular rotation is relative to the atrial arrangement, and the specific atrioventricular connections. For example, in patients with usual atrial arrangement and concordant atrioventricular connections, the morphologically right ventricle is unusually situated to the left of the morphologically left ventricle, which implies a clockwise rotation of the ventricles around the apex– base axis as seen from the apex. When the atrioventricular connections are discordant with usual atrial arrangement, then the morphologically right ventricle is typically found to the right of the morphologically left ventricle, implying a counter-clockwise rotation around the same axis. In other words, the unusual twisting of the ventricular mass occurs in such a fashion to place the right ventricular inlet superior and anterior to the left ventricular inlet [7]. In a few cases, nonetheless, opposite twisting has been observed such that the right ventricular inlet is positioned inferior and posterior relative to the left ventricular inlet [8,9]. In general, rather than the two inlets being parallel one to the other, they are positioned superoinferiorly, this feature accounting for the inability to image the four chambers and the two atrioventricular valves in the same plane simultaneously. This inability is the most important diagnostic feature of the crisscross arrangement. Tilting of the transducer from posterior, inferior to anterior, superior in continuous apical 4-chamber or subcostal coronal views, nonetheless, shows the two inflow tracts occupying separate
Fig. 3. The anatomic diagrams of criss-cross heart with double-outlet right ventricle. A shows the surface view from the right side. The RV is located anteriorly, superiorly and to the left of the LV. B shows the connection of the RA and the RV through the tricuspid valve (TV) and C shows the connection of the LA and the LV. D shows the casting figure displaying the right outlet crossing in front of the left outlet.
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planes, with each atrium joining a ventricle on the opposite side. Color flow mapping allows visualization of the crossover of the inflow streams, with no mixing, confirming the diagnosis of the criss-cross arrangement, and excluding the possible alternative diagnosis of absent atrioventricular connection or double-inlet ventricle. Our own experience, combined with analysis of previous case reports [10–12], leads us to conclude that the imaging of the two atrioventricular inlets on different planes, with one inlet crossing in front of the other, is the definitive diagnostic feature. Real-time echocardiography is the optimal technique providing a continuous sweep from posterior to anterior, and instantly revealing the abnormal superoinferior relationships of the junctions. Since the right ventricular inlet is located superiorly in most instances, it means that the left inlet is demonstrated first, and then the right inlet is shown with a more anterior angulation. This maneuver helps the operator to define the ventricular locations, and determine the twisted nature of the atrioventricular connections. The criss-cross arrangement is usually found in patients with biventricular atrioventricular connections, albeit also being seen in patients with double-inlet ventricle [13,14]. In the latter situation, the two atrioventricular valves connect with the dominant ventricle, but the right valve is located anteriorly and superiorly relative to the left valve, with the axes of the streams from the atrial chambers crossing within the dominant ventricle [13]. A superoinferior relationship of the ventricles is another feature of the criss-cross arrangement, hence the alternative description of superoinferior ventricles, or upstairs–downstairs heart. In all our cases, the morphologically right ventricle was superior to the left ventricle, and the ventricular septum was nearly horizontal. It has been shown [15,16], nonetheless, that other ventricular arrangements can be seen in the setting of criss-cross hearts. For example, the muscular ventricular septum can be oriented semivertically, while in some patients, the ventricles have been shown to be side-by-side, with a vertically oriented septum. Superoinferior ventricles can also be found in isolated cases without any ventricular rotation along the long axis, as in those with congenitally corrected transposition [12]. In fact, less than half of one series of patients described with superoinferior ventricles also exhibited the criss-cross arrangement [17]. A superoinferior arrangement of the ventricles, and a horizontal orientation of the muscular ventricular septum, therefore, should not be considered diagnostic features of the criss-cross arrangement. It is important to take note of ventricular topology when diagnosing the criss-cross arrangement. Ventricular topology described the handedness of the ventricular mass, irrespective of its location in space [18]. In most examples of patients having the criss-cross arrangement, the ventricular topology is as expected for the particular atrioventricular connections, despite the unusual spatial location of the ventricles relative to each other, this reflecting the twisted atrioventricular connections. In rare instances, however, there can be disharmony between the atrial arrangement and the ventricular topology in the setting of twisted atrioventricular connections, such that left hand ventricular topology is seen in the setting of usual atrial arrangement despite the presence of concordant atrioventricular connections [9]. This means that, in some instances, it will be essential to describe both the specific atrioventricular connections and the ventricular topology. Apart from these rare exceptions, nonetheless, the ventricular topology can be inferred from the pattern of atrioventricular connections by noting the twisted nature of the atrioventricular junctions. A review of 83 cases with the criss-cross arrangement by ValdesCrus and Cayre [19] revealed that all but one-twentieth had usual atrial arrangement, four-fifths had left-sided hearts and concordant atrioventricular connections, with just over half having discordant ventriculo-arterial connections, and almost one-third having double outlet from the morphological right ventricle. Pulmonary stenosis was also present in more than half of the cases, with integrity of the ventricular septum being very rare [20,21].
Of the associated anomalies, 2 deserve special emphasis. The first is hypoplasia of the tricuspid valve and right ventricle, found in 1 of our 4 patients. Marino et al. [22] found that the angle between the long axes of the atrioventricular valves correlated inversely with the size of the apical component of the right ventricle. The size and morphology of the tricuspid valve and the right ventricle should be accurately assessed preoperatively by echocardiography for planning of the optimal operative repair. The other notable feature is straddling of an atrioventricular valve. Echocardiography is known to be superior to angiography in the diagnosis of the valvar anomalies [7]. Indeed, the criss-cross arrangement with atrioventricular valvar straddling has now been detected during fetal life [23]. It is worth noting that the detection of a straddling valve is dependent on the experience of the operator. We suggest that the visualization of the two atrioventricular valvar attachments should be a routine in imaging the hearts with twisted atrioventricular junctions due to its frequent association, especially in patients with a large ventricular septal defect. It is also likely that diagnosis of straddling valves and twisted atrioventricular connections will be facilitated in the future as more centers gain access to magnetic resonance imaging and computed tomography. In conclusion, the failure to obtain a standard 4-chamber view in any cut is very characteristic when making the echocardiographic diagnosis of the criss-cross arrangement. The definitive appearance is twisted atrioventricular connections [5], with each atrium emptying into the ventricle on the opposite side as revealed by continuous subxiphoid or apical scanning. Use of transthoracic echocardiography, therefore, permits accurate diagnosis of this rare cardiac anomaly and the associated cardiac abnormalities. Acknowledgment The authors of this manuscript have certified that they comply with the Principles of Ethical Publishing in the International Journal of Cardiology [24]. References [1] Anderson RH, Shinebourne EA, Gerlis LM. Criss-cross atrioventricular relationships producing paradoxical atrioventricular concordance or discordance. Circulation 1974;50:176–80. [2] Ando M, Takao A, Cho E, et al. Criss-cross heart by abnormal rotation of bulboventricular loop: diagnostic considerations for complex cardiac anomaly. Proc Ped Circ Soc 1974;4:82–3. [3] Fyler DC. Trends. In: Fyler DC, editor. Nanda's pediatric cardiology. Philadelphia, PA: Hanley & Belfus; 1992. p. 273–80. [4] Hoffman P, Szymański P, Lubiszewska B, Różański J, Lipczyńska M, Klisiewicz A. Crisscross hearts in adults: echocardiographic evaluation and natural history. J Am Soc Echocardiogr 2009;22:134–40. [5] Seo J-W, Yoo S-J, Ho SY, Lee HJ, Anderson RH. Further morphological observations on hearts with twisted atrioventricular connections (criss-cross hearts). Cardiovasc Pathol 1992;1:211–7. [6] De Luca A, Sarkozy A, Consoli F, et al. Exclusion of Cx43 gene mutation as a major cause of criss-cross heart anomaly in man. Int J Cardiol Mar 16 2009 Electronic publication ahead of print, doi:10.1016/j.ijcard.2009.02.028. [7] Ekici E. Criss-cross heart with straddling right atrioventricular valve. Clin Cardiol 1984;7:503–8. [8] Seo JW, Choe GY, Ghi JG. An unusual ventricular loop associated with right juxtaposition of the atrial appendages. Int J Cardiol 1989;25:219–28. [9] Anderson RH, Smith A, Wilkinson JL. Disharmony between atrioventricular connections and segmental combinations: unusual variants of “criss-cross” hearts. J Am Coll Cardiol 1987;10:1274–7. [10] Robinson PJ, Kumpeng V, Macartney F. Cross sectional echocardiographic and angiocardiographic correlation in criss-cross hearts. Br Heart J 1985;54:61–7. [11] Van Mill G, Moulaert A, Harinck E, et al. Subcostal two-dimensional echocardiographic recognition of a criss-cross heart with discordant ventriculo-arterial connection. Pediatr Cardiol 1982;3:319–23. [12] Carminati M, Valsecchi O, Borghi A, et al. Cross-sectional echocardiographic study of criss-cross hearts and superoinferior ventricles. Am J Cardiol 1987;59:114–8. [13] Mori K, Harada M, Kuroda Y. Twisted atrioventricular valves in double inlet left ventricle. Cardiol Young 2002;12:401–3. [14] Kim TH, Yoo SJ, Ho SY, et al. Twisted atrioventricular connections in double inlet right ventricle: evaluation by magnetic resonance imaging. Cardiol Young 2000;10:567–73. [15] Han HS, Seo JW, Choi JY. Echocardiographic evaluation of hearts with twisted atrioventricular connections (criss-cross heart). Heart Vessels 1994;9:322–6.
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