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Anatomoechocardiographic correlation double inlet left ventricle
Anatomoechocardiographic Correlation Double Inlet Left Ventricle Luis Muñoz-Castellaños, MD, Nilda Espinola-Zavaleta, MD, PhD, and Candace Keirns, MD, Mexico City, Mexico
Double inlet left ventricle (LV) is a type of atrioventricular connection in which the morphologically LV receives more than 50% of the atrioventricular valves when they are separate, or more than 75% of a common atrioventricular valve. The aim of this study was to establish an anatomoechocardiographic correlation between the morphologic features of equivalent anatomic specimens and the echocardiographic images of patients to provide a means of interpreting the image correctly and a more precise diagnosis of the cardiac defect. Echo-
Double
inlet left ventricule (LV) is a type of atrioventricular connection in which this ventricle receives more than 50% of the flow of the two atrioventricular valves when these are separate, or more than 75% of the flow of a common atrioventricular valve.1 Three types exist: LV, right ventricular (RV), and univentricular. These types have been called by many names by different authors,2-4 and in the past were considered to be forms of a univentricular heart. Today the first two types are considered to be different entities within the concept of univentricular atrioventricular connection.5 In addition, these congenital anomalies include anatomic variations associated with malformations of the origins of the great vessels, the atrioventricular valves, and the septa. Double inlet LV is a complex congenital heart disease with a consistent alteration of the atrioventricular connection and variable ventriculoarterial connection.1 From an anatomic point of view it involves unequal ventricular development. The morphologically LV is the principal ventricle and is considered a superventricle that possesses two inlet portions represented by both atrioventricular valves, dilatation of the chamber, and hypertrophy of the
cardiography was used to study 18 patients with LV double inlet who were seen in a congenital heart disease clinic. The morphology of 17 hearts with this malformation from the department of embryology was analyzed to compare the anatomic features with their echocardiographic images. Echocardiography proved to be a noninvasive diagnostic tool that allowed characterization of anatomic and functional aspects of double inlet LV. (J Am Soc Echocardiogr 2005;18:237-43.)
walls. This contrasts with the rudimentary RV that only includes a trabecular portion and an outlet.6-10 The possibility of surgical treatment for this malformation now requires an anatomopathologic profile that focuses on the elements that can be addressed surgically.10 At the same time, an understanding of the morphologic peculiarities that occur in particular cases provides a frame of reference that facilitates interpretation of the echocardiographic images. Echocardiography is the noninvasive method that offers a detailed anatomic and functional evaluation of complex congenital heart disease at the patient’s bedside with a panorama of the evolution and prognosis of these patients.8,11 The aim of this study was to develop an anatomoechocardiographic correlation between the echocardiographic images of patients with equivalent anatomic specimens to achieve an adequate interpretation of the image and a more precise diagnosis of the malformation. Such information will be of great use for operation and may result in a better prognosis.
MATERIAL AND METHODS From the Department of Embriology (L.M.C.) and Echocardiography in Consulta Externa, Instituto Nacional de Cardiologia & “Ignacio Chavez.” Reprint requests: Nilda Espinola-Zavaleta, MD, PhD, Department of Echocardiography, Instituto Nacional de Cardiología, “Ignacio Chávez,” Juan Badiano No. 1, Col. Sección XVI, 14080, México, D.F., Mexico (E-mail: [email protected]). 0894-7317/$30.00 Copyright 2005 by the American Society of Echocardiography. doi:10.1016/j.echo.2004.11.009
In all, 18 patients (mean age 24.94 ⫾ 7.43 years, range 17-43) with double inlet LV were included in this study. Patients attended the adult congenital heart disease clinic of the Instituto Nacional de Cardiología “Ignacio Chávez” in Mexico City between January 1995 and January 2003. There were 3 female and 14 male patients. All patients underwent transthoracic echocardiography (TTE), transesophageal echocardiography (TEE), or both using commercially available equipment (Sonos 5500, Hewlett Pack-
237
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238 Muñoz-Castellaños, Espinola-Zavaleta, Keirns
ard, Palo Alto, Calif) with an S3 TTE probe and a multiplane TEE probe. In the TTE studies subcostal sections were used to evaluate the abdominal situs and the apical 4-chamber image to evaluate the characteristics of the atrioventricular valves (number, stenosis, atresia, and straddling) and their connection to the LV. Anatomic characteristics, position and type of rudimentary chamber, and the spatial relationship of the ventricles were also analyzed using apical and subcostal 4-chamber images and parasternal short axis at the level of the ventricles. To evaluate atrial septal defect and ventricular septal defect (VSD) parasternal long- and short-axis and apical 4-chamber and subcostal views were used. High TEE views were used to assess the characteristics of the atrial appendages and establish atrial situs. TEE 4-chamber sections at 0 degrees and transgastric sections at 0 and 90 degrees were used to evaluate characteristics and number of atrioventricular valves, subvalvular apparatus, septal defects and morphology, and position and spatial relationship of ventricles. Types of ventriculoarterial connections were determined using TTE 5-chamber apical and subcostal images with anterior angulation. Apical 5-chamber and parasternal sections were obtained to assess the relationship of the great arteries. The characteristics of semilunar valves and the position and relationship of the great arteries were evaluated using high-level TEE sections at 0 degrees and midlevel sections at 90 and 110 degrees. The severity of stenosis or insufficiency of semilunar valves was examined with color-coded and continuous wave Doppler echocardiography using previously established parameters.12,13 The morphology of 17 hearts with double inlet LV obtained from the department of embryology was also analyzed. Each specimen was described following the guidelines of the sequential segmental system used in the diagnosis of congenital heart disease.14 Atrial situs; number of atrioventricular valves and the form of their connection with the LV; straddling and stenosis of the atrioventricular valves; type of ventriculoarterial connection, morphologic characteristics, and spatial relationship of great arteries and ventricles; interventricular septum and its relationship with the crux cordis (point of intersection of the planes of the interatrial septum and atrioventricular junction represented by the fibrous valve anuli on the posterior face of the heart); and types of VSDs (bulvoventricular foramen) were determined. The morphologic features of the specimens were compared with the corresponding echocardiographic images to provide the anatomic basis of the latter.
RESULTS The morphologic characteristics of the anatomic specimens are shown in Tables 1, 2, and 3 and the echocardiographic findings of the patients in Table 4.
Table 1 Ventricular double inlet: Atrial situs Solitus Dextroisomerism Levoisomerism
No.
Percentage
13 3 1
76.5 17.6 5.9
Table 2 Left ventricular double inlet: Atrioventricular valves With two valves
With common valve
No.
Percentage
9
53
8
47
With tricuspid straddling* Without tricuspid straddling† Without straddling With straddling
6 3 4 4
*Four with mitral stenosis and one with tricuspid stenosis. †One with mitral stenosis.
Table 3 Left ventricular double inlet: Ventriculoarterial connection and relationship of great arteries Discordant
7 (41.2%)
Concordant
5 (29.4%)
Right ventricular double outlet
5 (29.4%)
Left anterior aorta Right anterior aorta Crossed Side to side Crossed Left anterior aorta Right anterior aorta
3 4 4 1 2 2 1
Anatomic Characteristics Atrial situs was predominantly solitus, followed by dextroisomerism and levoisomerism (Table 1). There were similar numbers of specimens with a common atrioventricular and two atrioventricular valves. In 7 hearts no valvular straddling occurred, and the two atrioventricular valves or the common atrioventricular valve were implanted entirely in LV. In 9 specimens of the group with two atrioventricular valves, 5 of these were stenotic (Table 2). The predominant ventriculoarterial connection was discordant with the remaining specimens equally divided between concordant and double outlet RV. The relationship between the great arteries appears in Table 3. The LV was communicated to the rudimentary RV through a septal defect of variable size. In the 3 specimens with two atrioventricular valves completely connected to the LV the VSD was subinfundibular, small, and restricted. In those specimens with straddling valve the VSD was large and occupied a part of the inlet. In all of the hearts there was a deviation in the position of the interventricular septum. In 12 specimens with normally lateralized ventricles the deviation was to the right and in 5
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Muñoz-Castellaños, Espinola-Zavaleta, Keirns 239
Table 4 Echocardiographic findings Case No.
Age, y
G F/M
1
33
M
Solitus
2
2
25
M
Solitus
1
3
17
F
Solitus
2
-
4
20
M
Solitus
2
-
5
17
F
Dextroisomerism
1
-
6
28
M
Dextroisomerism
1
-
7
27
M
Dextroisomerism
2
8
20
M
Dextroisomerism
1
9
20
M
Levoisomerism
1
10
43
F
Solitus
2
11
28
M
Solitus
1
12
18
M
Solitus*
1
13
25
M
Solitus
2
DOAV, straddling, severe regurgitation -
14
33
M
Solitus
2
Right valve stenosis
15
21
M
Dextroisomerism
2
Severe regurgitation
16
17
M
Dextroisomerism
1
-
17
22
M
Solitus
2
18
37
F
Solitus
2
Situs
No. of valves
Valve characteristics
LV stenosis, parachute -
Left imperforate valve Left valve stenosis, straddling Straddling
Left valve stenosis, parachute valve Left valve stenosis
Ventriculoarterial connection
Other anomalies
Discordant, left anterior aorta Discordant, left anterior aorta Discordant, left anterior aorta RVDO, left anterior aorta RVDO, left anterior aorta RVDO, right anterior aorta RVDO, left anterior aorta Discordant, right anterior aorta LVDO, right anterior aorta LVDO, left anterior aorta Concordant, left anterior aorta Concordant, left anterior aorta
2 ASDs, VSD
Right anterosuperior
2 ASDs, PS
Right anterosuperior
VSD, PS
Left posteroinferior
VSD, mPS
Right anterosuperior
ASD, VSD, PA, dextrocardia VSD, mPS, dextrocardia VSD, PA
Right anterosuperior Left anterosuperior
VSD, PS
Right anterosuperior
VSD, PS
Left anterosuperior
ASD, VSD, PS
Right anterosuperior
VSD, PH
Right anterosuperior
VSD, mPS
Right anterosuperior
VSD, ASD, PS
Left anterosuperior
VSD, PS
Left anterorsuperior
ASD, VSD, PS
Left anterosuperior
ASD, VSD, mPS ASD, VSD, PS
Right anteriosuperior Right anterosuperior
ASD, PH
Left posteroinferior
Discordant, left anterior aorta RVDO, right anterior aorta RVDO, right anterior aorta Discordant, left anterior aorta Concordant, left anterior aorta Concordant, left anterior aorta
Rudimentary RV position
Left anterosuperior
ASD, Atrial septal defect; DOAV, double orifice of atrioventricular valve; F, female; LVDO, left ventricular double outlet; M, male; m, mild; PA, pulmonary atresia; PH, pulmonary hypertension; PS, pulmonary stenosis; RVDO, right ventricular double outlet; VSD, ventricular septal defect. *With right juxtaposition of atrial appendages.
with inverted ventricles the deviation was to the left. In neither situation did the septum reach the crux cordis. In 12 specimens the rudimentary chamber was located on the right with the morphologically LV in a left posteroinferior position and the morphologically RV in a right anterosuperior position. In 5 hearts the rudimentary chamber was located on the left. In these cases the LV was in a right posteroinferior position and the RV in left anterosuperior position. Echocardiographic Characteristics In all, 11 patients had situs solitus, 6 had dextroisomersim, and 1 had levoisomerism. In 10 cases there were two separate atrioventricular valves and in 8, a
common atrioventricular valve. In 15 cases all of the flow of both atrioventricular valves was entirely into the LV. One case showed tricuspid straddling and two had common atrioventricular valves. As far as the left atrioventricular valve was concerned, there was atresia in one case and stenosis in 4. The latter included two with parachute valves and two with thickening. One patient had stenosis of the right atrioventricular valve. The ventriculoarterial connection was most frequently discordant, followed by RV double outlet and, least frequently, concordant and double outlet LV. Twelve cases had associated pulmonary stenosis and two, pulmonary atresia. In 7 patients atrial septal defect and VSD were identified (including one case with two interatrial
240 Muñoz-Castellaños, Espinola-Zavaleta, Keirns
A
C
B
Journal of the American Society of Echocardiography March 2005
IS
D
Figure 1 A, Four-chamber transesophageal echocardiographic image with posterior angulation shows situs solitus and left (1) and right (2) atrioventricular valves opening into left ventricle (LV). B, Anatomic specimen showing same findings. Observe dilatation and hypertrophy of LV with greater number of papillary muscles (arrow). C, Transverse transgastric image of both ventricles with two atrioventricular valves in LV. Rudimentary right ventricle (RV) separated by interventricular septum (*) can be seen. D, Anatomic specimen shows same morphologic findings. Ventricular septal defect (VSD) connects to RV (arrow). IS, Interatrial septum; LA, left atrium; RA, right atrium.
defects). In 11 only VSDs were found (including one with two interventricular defects). In all cases the diameter of the VSD was greater than 1 cm. The position of the rudimentary RV was most frequently right anterosuperior, followed by left anterosuperior and left posteroinferior (Table 4). Anatomoechocardiographic Correlation When echocardiographic images of double inlet LV were compared with specimens, a strong correlation was evident with atrial situs (Figures 1– 4), with atrioventricular valves separated by the interatrial septum connected to the LV (Figures 1, 4 – 6), the crux cordis that projected toward the LV, the interventricular septum displaced toward the right or left that did not reach the crux cordis (Figures 1– 4), the common atrioventricular valve (Figures 2– 4, and 7), valve stenosis, and valve straddling (Figures 2, 3, 5, and 6). Acceptable correspondence was also established between images and specimens regarding ventriculoarterial connection (Figures 8 and 9), spatial position of the principal (morphologically left) ventricle and the rudimentary (morphologically right) ventricle, either normally lateralized or inverted, and type and size of the VSDs (Figures 2– 4, and 7).
Figure 2 A, Internal view of left ventricle (LV) of heart with dextroisomerism. Observe common atrioventricular valve with mild overriding. B, Internal view of right ventricle (RV) of same anatomic specimen showing straddling valve with insertion in crest of ventricular septum (arrow). C, Fourchamber image of LV double inlet with common atrioventricular valve straddling RV (arrow). 3, Common atrioventricular valve; RA, right atrium; VSD, ventricular septal defect.
DISCUSSION The first description of this cardiac malformation was made by Holmes in 1824.15 It was later referred to in the atlas of Abbott16 in 1936 and in the text of Taussig17 in 1947. In 1968 De la Cruz and Miller6 called this malformation “double inlet LV.” This congenital malformation of the heart probably originates from a partial or complete block in the left to right expansion process of the atrioventricular canal. The result is the persistence of the connection of both atria with the primitive ventricle, primordium of the morphologically LV, and underdevelopment of the RV. The RV lacks the inlet portion and its atrioventricular valve is retained by the LV. It has a bipartite (trabecular and outlet) or monopartite (trabecular) constitution if both the inlet and the outlet are missing, as occurs in combination with the LV double outlet, an extremely rare condition. Double inlet LV is considered as a single functional ventricle with a rudimentary outlet chamber without inlet portion. If a chamber lacks the inlet portion in the ventricular mass, it loses the category of ventricle. In the straddling forms the RV is more fully developed with a sinus portion that provides blood flow to this ventricle, and this chamber resembles a hypoplastic RV. When there is no straddling of atrioventricular valves the RV is very rudimentary. The LV with double inlet possesses the apparatus of two atrioventricular valves, which implies a greater number of papillary muscles. This characteristic can
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Muñoz-Castellaños, Espinola-Zavaleta, Keirns 241
A
IS
RA 2
*
RV
BB
LA 1 LV
VD
Ao
RA
PA
LA
RV
VP AI
D
CC PV LA
RA
RA
RV VD
LV
PA
Ao LA
RV LV
VI
Figure 3 A, Transesophageal echocardiographic (TEE) image showing dextroisomerism and double inlet left ventricle (LV) through straddling common atrioventricular valve. Observe insertion of chordae tendinae into right edge of interventricular septum over ventricular septal defect (arrow). B, Anatomic specimen with dextroisomerism shows atria that form common chamber and common atrioventricular valve that straddles ventricular septal defect (arrow). Atrioventricular flow is predominantly into LV. C, TEE image shows situs solitus with common atrium connected to LV through common atrioventricular valve without straddling. Observe normal lateralization of both ventricles. D, Anatomic specimen with atrial situs solitus and LV double inlet through common atrioventricular valve. Compare rudimentary right ventricle in echocardiographic image with anatomic specimen. 3, Common atrioventricular valve; CA, common atrium; LA, left atrium; RA, right atrium; VSD, ventricular septal defect.
lead to the false impression of trabeculations and incorrect identification as the morphologically RV. This confusion is resolved by observing the anatomic characteristics of the ventricular septum, which is smooth in the basal portion and trabecular in the apical third.10 The most common kind of double inlet is to the LV. This is explained by the fact that this type of atrioventricular connection is established in the early phases of embryonic development of the heart, when both atria have continuity with the LV primordium. Complete forms of double inlet LV represent the persistence of a condition involving the connection of the atria to the LV present in the embryonic heart of the horizon XIII of Streeter.18 Straddling forms of LV double inlet correspond to stages XIV and XV of Streeter19 when the atrioventricular canal has begun the process of widening and the bulbus cordis (primordium of the RV) receives a sinus portion that
Figure 4 A, Transesophageal echocardiogram (TEE) shows double inlet left ventricle (LV) through two atrioventricular valves in situs solitus, with normally lateralized ventricles. B, External view of heart with double inlet LV and situs solitus shows right-sided position of rudimentary ventricle. C, TEE image of heart in situs solitus with double inlet LV through common atriobentricular valve with inverted ventricles. D, Anatomic specimen shows ventricular inversion. 1, Left atrioventricular valve; 2, right atrioventricular valve; Ao, aorta; IS, interatrial septum; LA, left atrium; LV, left ventricle; PA, pulmonary artery; RA, right atrium; RV, right ventricle. *, Crux cordis.
Figure 5 A, Transesophageal echocardiogram shows two valve rings opening into left ventricle (LV) with stenosis of atrioventricular valves and straddling of left atrioventricular valve. B, Anatomic specimen demonstrates LV dilatation and hypertrophy. Right atrioventricular valve straddles with part of its insertion over crest of ventricular septum and toward right ventricle. Left atrioventricular valve is stenotic. 1, Left atrioventricular valve; 2, right atrioventricular valve; LA, left atrium; RA, right atrium; VSD, ventricular septal defect.
differentiates into a tricuspid valve less than 50% of the flow of which goes into the RV or into a common atrioventricular valve through which less than 25% of the flow goes into the RV.
242 Muñoz-Castellaños, Espinola-Zavaleta, Keirns
Figure 6 A and B, Short-axis transthoracic image at level of both ventricles and 4-chamber image with posterior angulation show stenosis of parachute left atrioventricular valve (arrows). C, Anatomic specimen corroborates characteristics observed in echocardiographic image. PM, Papillary muscle. 1, Left atrioventricular valve; 2, right atrioventricular valve; LA, left atrium; LV, left ventricle; RA, right atrium.
Figure 7 A, Subcostal echocardiographic image at ventricular level with double inlet left ventricle showing common atrioventricular valve (3) in this chamber. B, Observe correspondence between anatomic specimen and echocardiographic image. Interatrial septum (IS) can be seen through valve. LV, Left ventricle.
Before the advent of 2-dimensional echocardiography, angiography was the diagnostic technique of choice for LV double inlet. However, it is an invasive technique that cannot be performed at the patient’s bedside. Two-dimensional echocardiography with 3 modalities of Doppler and segmental analysis have made it possible to characterize the different complex congenital malformations of the heart.20-23 In this comparative anatomoechocardiographic study of LV double inlet, we found that TTE information was incomplete, whereas TEE technique provided precise information regarding atrial situs, number and characteristics of the atrioventricular
Journal of the American Society of Echocardiography March 2005
Figure 8 A, Transthoracic 5-chamber image with anterior angulation in double inlet left ventricle (LV) shows discordant ventriculoarterial connection with stenotic pulmonary valve (left) and aorta (Ao) (right). B, Anatomic specimen shows open right ventricle connected to right-sided aorta and pulmonary artery (PA) in left posterior position connected to LV. RV, Right ventricle; VSD, ventricular septal defect.
Figure 9 A, Transthoracic echocardiographic image with anterior angulation shows discordant ventriculoarterial connection in double inlet left ventricle. Great arteries arise from inappropriate ventricles with subpulmonary stenosis (arrow). Ventricles are normally lateralized. B, Anatomic specimen shows same characteristics described for echocardiographic image. Ao, Aorta; LA, left atrium; LV, left ventricle; PA, pulmonary artery; RA, right atrium; RV, right ventricle.
valves, subvalvular apparatus, ventriculoarterial connection (including semilunar valves and the spatial relationship of great vessels), position of the rudimentary RV, and associated anomalies such as septal defects.24 Echocardiography is a noninvasive, reproducible technique that can be performed at the patient’s bedside. It shows strong correlation with the anatomic findings of corresponding specimens. A comprehension of the morphology of LV double inlet provides a frame of reference for the correct interpretation of diagnostic images and the intentional search for elements that will establish the diagnosis
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of congenital malformations of the heart with precision, as this comparative study demonstrates. Certain characteristics, such as straddling of atrioventricular valves, deserve special emphasis in the echocardiographic evaluation.25,26 These efforts have the goal of obtaining precise and complete information to establish or confirm a diagnosis in a timely manner so that the surgeon can select the appropriate intervention that will improve the quality of life and prognosis of the patient.26,27 In conclusion, echocardiography is a noninvasive diagnostic technique that has demonstrated excellent correlation of images with the morphologic findings of anatomic specimens. Thus, it provides the opportunity to characterize the anatomic and functional features of LV double inlet for patients and orient optimal surgical treatment. REFERENCES 1. Becker AE, Anderson RH. Pathology of congenital heart disease. London: Butterworth; 1981. p. 241–56. 2. Van Praagh R, Ongley PA, Swan HJC. Anatomic types of single or common ventricle in man, morphologic and geometric aspects of 68 necropsied cases. Am J Cardiol 1964;13:367-86. 3. Lev M, Libertson RR, Kirkpatrick JR, Eckner FAO, Arcilla RA. Single (primitive) ventricle. Circulation 1969;39:577-91. 4. Anderson RH, Becker AE, Freedom RM, Quero-Jimenez M, Macartney FJ, Shinebourne EA, et al. Problems in the nomenclature of the univentricular heart. Herz 1979;4:97-102. 5. Anderson RH. Weasel words in pediatric cardiology: single ventricle. Int J Cardiol 1983;2:425-9. 6. De la Cruz MV, Miller BL. Double inlet left ventricle. Circulation 1968;37:249-60. 7. Rigby ML, Anderson RH, Gibson D, Jones OD, Joseph MC, Shinebourne EA. Two-dimensional echocardiographic categorization of the univentricular heart: ventricular morphology, type, and mode of atrioventricular connection. Br Heart J 1981;46:603-12. 8. Freedom RM, Picchio F, Duncan WJ, Harder JR, Maes CAF, Rowe RD. The atrioventricular junction in the univentricular heart: a two-dimensional echocardiographic analysis. Pediatr Cardiol 1982;3:105-17. 9. Huhta JC, Seward JB, Tajik AJ, Hagler DJ, Edwards WD. Two-dimensional echocardiographic spectrum of univentricular atrioventricular connection. J Am Coll Cardiol 1985;5: 149-57. 10. Muñoz-Castellanos L, Ramírez S, Kuri Nivon M, Salinas Sánchez C. Doble entrada ventricular izquierda: Morfología y anatomía quirúrgica. Arch Inst Cardiol Mex 2000;70:136-47. 11. Shiraishi H, Silverman NH. Echocardiographic spectrum of double inlet ventricle: evaluation of the univentricular communication. J Am Coll Cardiol 1990;15:1401-8.
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12. Hatle L, Angelsen B. Doppler ultrasound in cardiology. Philadelphia: Lea and Febiger; 1982. 13. Berman W. Pulsed Doppler in clinical pediatrics. New York: Futura Publishing Company; 1983. 14. Tynan MJ, Becker AE, Macartney FJ, Jimenez M, Shinebourne EA, Anderson RH. Nomenclature and classification of congenital heart disease. Br Heart J 1979;41:544-53. 15. Holmes AF. Case of malformation of the heart. Trans MedicoChirurgical Soc Edinburgh 1824;1:252-9. 16. Abbott ME. Atlas of congenital cardiac diseases. New York: American Heart Association; 1936. 17. Taussig MB. Congenital malformations of the heart. New York: The Commonwealth Fund; 1947. 18. Streeter GL. Developmental horizons in human embryos: descriptions of age group XIII, embryos about 4 or 5 millimeters long, and age group XIV, period of indentation of the lens vesicle. Carnegie Contrib Embryol 1948;541:211-45. 19. Streeter GL. Developmental horizons in human embryos: description of age group XV, XVI, XVII and XVIII, being the third issue of a surgery of the Carnegie collection. Carnegie Contrib Embryol 1948;211:133-203. 20. Sahn DJ, Harder JR, Freedom RM, Duncan WJ, Rowe RD, Allen HD, et al. Cross-sectional echocardiographic diagnosis and subclassification of univentricular hearts: imaging studies of atrioventricular valves, septal structures and rudimentary outflow chambers. Circulation 1982;66:1070-7. 21. Bevilacqua M, Sanders SP, Van Praagh S, Colan SD, Parness I. Double-inlet single left ventricle: echocardiographic anatomy with emphasis on the morphology of the atrioventricular valves and ventricular septal defect. J Am Coll Cardiol 1991; 18:559-68. 22. Freedom RM, Picchio F, Duncan WJ, Harder JR, Rowe RD. The atrioventricular junction in the univentricular heart: a two-dimensional echocardiographic analysis. Pediatr Cardiol 1982;3:105-17. 23. Fasoli G, Daliento L, Rossi M, Scattolin G, Roelandt J. M-mode contrast echocardiography in patients with univentricular heart. Eur Heart J 1983;4:415-23. 24. Seward JB, Khandheria BK, Oh JK, Abel MD, Hughes RW, Edwards WD, et al. Transesophageal echocardiography: technique, anatomic correlations, implementation, and clinical applications. Mayo Clinic Proc 1988;63:649-80. 25. Tandon R, Becker AE, Moller JH, Edwards JE. Double inlet left ventricle: straddling tricuspid valve. B Heart J 1974;36: 747-59. 26. Rice MJ, Seward JB, Edwards WD, Hagler DJ, Danielson GK, Puga FJ, et al. Straddling atrioventricular valve: two-dimensional echocardiographic diagnosis, classification and surgical implications. Am J Cardiol 1985;55:505-13. 27. Mair DD, Hagler DJ, Julsrud PR, Puga FJ, Scaf HV, Danielson GK. Early and late results of the modified Fontan procedure for double-inlet left ventricle: the Mayo Clinic experience. J Am Coll Cardiol 1991;18:1727-32.
Double inlet left ventricle (LV) is a type of atrioventricular connection in which the morphologically LV receives more than 50% of the atrioventricular valves when they are separate, or more than 75% of a common atrioventricular valve. The aim of this study was to establish an anatomoechocardiographic correlation between the morphologic features of equivalent anatomic specimens and the echocardiographic images of patients to provide a means of interpreting the image correctly and a more precise diagnosis of the cardiac defect. Echo-
Double
inlet left ventricule (LV) is a type of atrioventricular connection in which this ventricle receives more than 50% of the flow of the two atrioventricular valves when these are separate, or more than 75% of the flow of a common atrioventricular valve.1 Three types exist: LV, right ventricular (RV), and univentricular. These types have been called by many names by different authors,2-4 and in the past were considered to be forms of a univentricular heart. Today the first two types are considered to be different entities within the concept of univentricular atrioventricular connection.5 In addition, these congenital anomalies include anatomic variations associated with malformations of the origins of the great vessels, the atrioventricular valves, and the septa. Double inlet LV is a complex congenital heart disease with a consistent alteration of the atrioventricular connection and variable ventriculoarterial connection.1 From an anatomic point of view it involves unequal ventricular development. The morphologically LV is the principal ventricle and is considered a superventricle that possesses two inlet portions represented by both atrioventricular valves, dilatation of the chamber, and hypertrophy of the
cardiography was used to study 18 patients with LV double inlet who were seen in a congenital heart disease clinic. The morphology of 17 hearts with this malformation from the department of embryology was analyzed to compare the anatomic features with their echocardiographic images. Echocardiography proved to be a noninvasive diagnostic tool that allowed characterization of anatomic and functional aspects of double inlet LV. (J Am Soc Echocardiogr 2005;18:237-43.)
walls. This contrasts with the rudimentary RV that only includes a trabecular portion and an outlet.6-10 The possibility of surgical treatment for this malformation now requires an anatomopathologic profile that focuses on the elements that can be addressed surgically.10 At the same time, an understanding of the morphologic peculiarities that occur in particular cases provides a frame of reference that facilitates interpretation of the echocardiographic images. Echocardiography is the noninvasive method that offers a detailed anatomic and functional evaluation of complex congenital heart disease at the patient’s bedside with a panorama of the evolution and prognosis of these patients.8,11 The aim of this study was to develop an anatomoechocardiographic correlation between the echocardiographic images of patients with equivalent anatomic specimens to achieve an adequate interpretation of the image and a more precise diagnosis of the malformation. Such information will be of great use for operation and may result in a better prognosis.
MATERIAL AND METHODS From the Department of Embriology (L.M.C.) and Echocardiography in Consulta Externa, Instituto Nacional de Cardiologia & “Ignacio Chavez.” Reprint requests: Nilda Espinola-Zavaleta, MD, PhD, Department of Echocardiography, Instituto Nacional de Cardiología, “Ignacio Chávez,” Juan Badiano No. 1, Col. Sección XVI, 14080, México, D.F., Mexico (E-mail: [email protected]). 0894-7317/$30.00 Copyright 2005 by the American Society of Echocardiography. doi:10.1016/j.echo.2004.11.009
In all, 18 patients (mean age 24.94 ⫾ 7.43 years, range 17-43) with double inlet LV were included in this study. Patients attended the adult congenital heart disease clinic of the Instituto Nacional de Cardiología “Ignacio Chávez” in Mexico City between January 1995 and January 2003. There were 3 female and 14 male patients. All patients underwent transthoracic echocardiography (TTE), transesophageal echocardiography (TEE), or both using commercially available equipment (Sonos 5500, Hewlett Pack-
237
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238 Muñoz-Castellaños, Espinola-Zavaleta, Keirns
ard, Palo Alto, Calif) with an S3 TTE probe and a multiplane TEE probe. In the TTE studies subcostal sections were used to evaluate the abdominal situs and the apical 4-chamber image to evaluate the characteristics of the atrioventricular valves (number, stenosis, atresia, and straddling) and their connection to the LV. Anatomic characteristics, position and type of rudimentary chamber, and the spatial relationship of the ventricles were also analyzed using apical and subcostal 4-chamber images and parasternal short axis at the level of the ventricles. To evaluate atrial septal defect and ventricular septal defect (VSD) parasternal long- and short-axis and apical 4-chamber and subcostal views were used. High TEE views were used to assess the characteristics of the atrial appendages and establish atrial situs. TEE 4-chamber sections at 0 degrees and transgastric sections at 0 and 90 degrees were used to evaluate characteristics and number of atrioventricular valves, subvalvular apparatus, septal defects and morphology, and position and spatial relationship of ventricles. Types of ventriculoarterial connections were determined using TTE 5-chamber apical and subcostal images with anterior angulation. Apical 5-chamber and parasternal sections were obtained to assess the relationship of the great arteries. The characteristics of semilunar valves and the position and relationship of the great arteries were evaluated using high-level TEE sections at 0 degrees and midlevel sections at 90 and 110 degrees. The severity of stenosis or insufficiency of semilunar valves was examined with color-coded and continuous wave Doppler echocardiography using previously established parameters.12,13 The morphology of 17 hearts with double inlet LV obtained from the department of embryology was also analyzed. Each specimen was described following the guidelines of the sequential segmental system used in the diagnosis of congenital heart disease.14 Atrial situs; number of atrioventricular valves and the form of their connection with the LV; straddling and stenosis of the atrioventricular valves; type of ventriculoarterial connection, morphologic characteristics, and spatial relationship of great arteries and ventricles; interventricular septum and its relationship with the crux cordis (point of intersection of the planes of the interatrial septum and atrioventricular junction represented by the fibrous valve anuli on the posterior face of the heart); and types of VSDs (bulvoventricular foramen) were determined. The morphologic features of the specimens were compared with the corresponding echocardiographic images to provide the anatomic basis of the latter.
RESULTS The morphologic characteristics of the anatomic specimens are shown in Tables 1, 2, and 3 and the echocardiographic findings of the patients in Table 4.
Table 1 Ventricular double inlet: Atrial situs Solitus Dextroisomerism Levoisomerism
No.
Percentage
13 3 1
76.5 17.6 5.9
Table 2 Left ventricular double inlet: Atrioventricular valves With two valves
With common valve
No.
Percentage
9
53
8
47
With tricuspid straddling* Without tricuspid straddling† Without straddling With straddling
6 3 4 4
*Four with mitral stenosis and one with tricuspid stenosis. †One with mitral stenosis.
Table 3 Left ventricular double inlet: Ventriculoarterial connection and relationship of great arteries Discordant
7 (41.2%)
Concordant
5 (29.4%)
Right ventricular double outlet
5 (29.4%)
Left anterior aorta Right anterior aorta Crossed Side to side Crossed Left anterior aorta Right anterior aorta
3 4 4 1 2 2 1
Anatomic Characteristics Atrial situs was predominantly solitus, followed by dextroisomerism and levoisomerism (Table 1). There were similar numbers of specimens with a common atrioventricular and two atrioventricular valves. In 7 hearts no valvular straddling occurred, and the two atrioventricular valves or the common atrioventricular valve were implanted entirely in LV. In 9 specimens of the group with two atrioventricular valves, 5 of these were stenotic (Table 2). The predominant ventriculoarterial connection was discordant with the remaining specimens equally divided between concordant and double outlet RV. The relationship between the great arteries appears in Table 3. The LV was communicated to the rudimentary RV through a septal defect of variable size. In the 3 specimens with two atrioventricular valves completely connected to the LV the VSD was subinfundibular, small, and restricted. In those specimens with straddling valve the VSD was large and occupied a part of the inlet. In all of the hearts there was a deviation in the position of the interventricular septum. In 12 specimens with normally lateralized ventricles the deviation was to the right and in 5
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Muñoz-Castellaños, Espinola-Zavaleta, Keirns 239
Table 4 Echocardiographic findings Case No.
Age, y
G F/M
1
33
M
Solitus
2
2
25
M
Solitus
1
3
17
F
Solitus
2
-
4
20
M
Solitus
2
-
5
17
F
Dextroisomerism
1
-
6
28
M
Dextroisomerism
1
-
7
27
M
Dextroisomerism
2
8
20
M
Dextroisomerism
1
9
20
M
Levoisomerism
1
10
43
F
Solitus
2
11
28
M
Solitus
1
12
18
M
Solitus*
1
13
25
M
Solitus
2
DOAV, straddling, severe regurgitation -
14
33
M
Solitus
2
Right valve stenosis
15
21
M
Dextroisomerism
2
Severe regurgitation
16
17
M
Dextroisomerism
1
-
17
22
M
Solitus
2
18
37
F
Solitus
2
Situs
No. of valves
Valve characteristics
LV stenosis, parachute -
Left imperforate valve Left valve stenosis, straddling Straddling
Left valve stenosis, parachute valve Left valve stenosis
Ventriculoarterial connection
Other anomalies
Discordant, left anterior aorta Discordant, left anterior aorta Discordant, left anterior aorta RVDO, left anterior aorta RVDO, left anterior aorta RVDO, right anterior aorta RVDO, left anterior aorta Discordant, right anterior aorta LVDO, right anterior aorta LVDO, left anterior aorta Concordant, left anterior aorta Concordant, left anterior aorta
2 ASDs, VSD
Right anterosuperior
2 ASDs, PS
Right anterosuperior
VSD, PS
Left posteroinferior
VSD, mPS
Right anterosuperior
ASD, VSD, PA, dextrocardia VSD, mPS, dextrocardia VSD, PA
Right anterosuperior Left anterosuperior
VSD, PS
Right anterosuperior
VSD, PS
Left anterosuperior
ASD, VSD, PS
Right anterosuperior
VSD, PH
Right anterosuperior
VSD, mPS
Right anterosuperior
VSD, ASD, PS
Left anterosuperior
VSD, PS
Left anterorsuperior
ASD, VSD, PS
Left anterosuperior
ASD, VSD, mPS ASD, VSD, PS
Right anteriosuperior Right anterosuperior
ASD, PH
Left posteroinferior
Discordant, left anterior aorta RVDO, right anterior aorta RVDO, right anterior aorta Discordant, left anterior aorta Concordant, left anterior aorta Concordant, left anterior aorta
Rudimentary RV position
Left anterosuperior
ASD, Atrial septal defect; DOAV, double orifice of atrioventricular valve; F, female; LVDO, left ventricular double outlet; M, male; m, mild; PA, pulmonary atresia; PH, pulmonary hypertension; PS, pulmonary stenosis; RVDO, right ventricular double outlet; VSD, ventricular septal defect. *With right juxtaposition of atrial appendages.
with inverted ventricles the deviation was to the left. In neither situation did the septum reach the crux cordis. In 12 specimens the rudimentary chamber was located on the right with the morphologically LV in a left posteroinferior position and the morphologically RV in a right anterosuperior position. In 5 hearts the rudimentary chamber was located on the left. In these cases the LV was in a right posteroinferior position and the RV in left anterosuperior position. Echocardiographic Characteristics In all, 11 patients had situs solitus, 6 had dextroisomersim, and 1 had levoisomerism. In 10 cases there were two separate atrioventricular valves and in 8, a
common atrioventricular valve. In 15 cases all of the flow of both atrioventricular valves was entirely into the LV. One case showed tricuspid straddling and two had common atrioventricular valves. As far as the left atrioventricular valve was concerned, there was atresia in one case and stenosis in 4. The latter included two with parachute valves and two with thickening. One patient had stenosis of the right atrioventricular valve. The ventriculoarterial connection was most frequently discordant, followed by RV double outlet and, least frequently, concordant and double outlet LV. Twelve cases had associated pulmonary stenosis and two, pulmonary atresia. In 7 patients atrial septal defect and VSD were identified (including one case with two interatrial
240 Muñoz-Castellaños, Espinola-Zavaleta, Keirns
A
C
B
Journal of the American Society of Echocardiography March 2005
IS
D
Figure 1 A, Four-chamber transesophageal echocardiographic image with posterior angulation shows situs solitus and left (1) and right (2) atrioventricular valves opening into left ventricle (LV). B, Anatomic specimen showing same findings. Observe dilatation and hypertrophy of LV with greater number of papillary muscles (arrow). C, Transverse transgastric image of both ventricles with two atrioventricular valves in LV. Rudimentary right ventricle (RV) separated by interventricular septum (*) can be seen. D, Anatomic specimen shows same morphologic findings. Ventricular septal defect (VSD) connects to RV (arrow). IS, Interatrial septum; LA, left atrium; RA, right atrium.
defects). In 11 only VSDs were found (including one with two interventricular defects). In all cases the diameter of the VSD was greater than 1 cm. The position of the rudimentary RV was most frequently right anterosuperior, followed by left anterosuperior and left posteroinferior (Table 4). Anatomoechocardiographic Correlation When echocardiographic images of double inlet LV were compared with specimens, a strong correlation was evident with atrial situs (Figures 1– 4), with atrioventricular valves separated by the interatrial septum connected to the LV (Figures 1, 4 – 6), the crux cordis that projected toward the LV, the interventricular septum displaced toward the right or left that did not reach the crux cordis (Figures 1– 4), the common atrioventricular valve (Figures 2– 4, and 7), valve stenosis, and valve straddling (Figures 2, 3, 5, and 6). Acceptable correspondence was also established between images and specimens regarding ventriculoarterial connection (Figures 8 and 9), spatial position of the principal (morphologically left) ventricle and the rudimentary (morphologically right) ventricle, either normally lateralized or inverted, and type and size of the VSDs (Figures 2– 4, and 7).
Figure 2 A, Internal view of left ventricle (LV) of heart with dextroisomerism. Observe common atrioventricular valve with mild overriding. B, Internal view of right ventricle (RV) of same anatomic specimen showing straddling valve with insertion in crest of ventricular septum (arrow). C, Fourchamber image of LV double inlet with common atrioventricular valve straddling RV (arrow). 3, Common atrioventricular valve; RA, right atrium; VSD, ventricular septal defect.
DISCUSSION The first description of this cardiac malformation was made by Holmes in 1824.15 It was later referred to in the atlas of Abbott16 in 1936 and in the text of Taussig17 in 1947. In 1968 De la Cruz and Miller6 called this malformation “double inlet LV.” This congenital malformation of the heart probably originates from a partial or complete block in the left to right expansion process of the atrioventricular canal. The result is the persistence of the connection of both atria with the primitive ventricle, primordium of the morphologically LV, and underdevelopment of the RV. The RV lacks the inlet portion and its atrioventricular valve is retained by the LV. It has a bipartite (trabecular and outlet) or monopartite (trabecular) constitution if both the inlet and the outlet are missing, as occurs in combination with the LV double outlet, an extremely rare condition. Double inlet LV is considered as a single functional ventricle with a rudimentary outlet chamber without inlet portion. If a chamber lacks the inlet portion in the ventricular mass, it loses the category of ventricle. In the straddling forms the RV is more fully developed with a sinus portion that provides blood flow to this ventricle, and this chamber resembles a hypoplastic RV. When there is no straddling of atrioventricular valves the RV is very rudimentary. The LV with double inlet possesses the apparatus of two atrioventricular valves, which implies a greater number of papillary muscles. This characteristic can
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Muñoz-Castellaños, Espinola-Zavaleta, Keirns 241
A
IS
RA 2
*
RV
BB
LA 1 LV
VD
Ao
RA
PA
LA
RV
VP AI
D
CC PV LA
RA
RA
RV VD
LV
PA
Ao LA
RV LV
VI
Figure 3 A, Transesophageal echocardiographic (TEE) image showing dextroisomerism and double inlet left ventricle (LV) through straddling common atrioventricular valve. Observe insertion of chordae tendinae into right edge of interventricular septum over ventricular septal defect (arrow). B, Anatomic specimen with dextroisomerism shows atria that form common chamber and common atrioventricular valve that straddles ventricular septal defect (arrow). Atrioventricular flow is predominantly into LV. C, TEE image shows situs solitus with common atrium connected to LV through common atrioventricular valve without straddling. Observe normal lateralization of both ventricles. D, Anatomic specimen with atrial situs solitus and LV double inlet through common atrioventricular valve. Compare rudimentary right ventricle in echocardiographic image with anatomic specimen. 3, Common atrioventricular valve; CA, common atrium; LA, left atrium; RA, right atrium; VSD, ventricular septal defect.
lead to the false impression of trabeculations and incorrect identification as the morphologically RV. This confusion is resolved by observing the anatomic characteristics of the ventricular septum, which is smooth in the basal portion and trabecular in the apical third.10 The most common kind of double inlet is to the LV. This is explained by the fact that this type of atrioventricular connection is established in the early phases of embryonic development of the heart, when both atria have continuity with the LV primordium. Complete forms of double inlet LV represent the persistence of a condition involving the connection of the atria to the LV present in the embryonic heart of the horizon XIII of Streeter.18 Straddling forms of LV double inlet correspond to stages XIV and XV of Streeter19 when the atrioventricular canal has begun the process of widening and the bulbus cordis (primordium of the RV) receives a sinus portion that
Figure 4 A, Transesophageal echocardiogram (TEE) shows double inlet left ventricle (LV) through two atrioventricular valves in situs solitus, with normally lateralized ventricles. B, External view of heart with double inlet LV and situs solitus shows right-sided position of rudimentary ventricle. C, TEE image of heart in situs solitus with double inlet LV through common atriobentricular valve with inverted ventricles. D, Anatomic specimen shows ventricular inversion. 1, Left atrioventricular valve; 2, right atrioventricular valve; Ao, aorta; IS, interatrial septum; LA, left atrium; LV, left ventricle; PA, pulmonary artery; RA, right atrium; RV, right ventricle. *, Crux cordis.
Figure 5 A, Transesophageal echocardiogram shows two valve rings opening into left ventricle (LV) with stenosis of atrioventricular valves and straddling of left atrioventricular valve. B, Anatomic specimen demonstrates LV dilatation and hypertrophy. Right atrioventricular valve straddles with part of its insertion over crest of ventricular septum and toward right ventricle. Left atrioventricular valve is stenotic. 1, Left atrioventricular valve; 2, right atrioventricular valve; LA, left atrium; RA, right atrium; VSD, ventricular septal defect.
differentiates into a tricuspid valve less than 50% of the flow of which goes into the RV or into a common atrioventricular valve through which less than 25% of the flow goes into the RV.
242 Muñoz-Castellaños, Espinola-Zavaleta, Keirns
Figure 6 A and B, Short-axis transthoracic image at level of both ventricles and 4-chamber image with posterior angulation show stenosis of parachute left atrioventricular valve (arrows). C, Anatomic specimen corroborates characteristics observed in echocardiographic image. PM, Papillary muscle. 1, Left atrioventricular valve; 2, right atrioventricular valve; LA, left atrium; LV, left ventricle; RA, right atrium.
Figure 7 A, Subcostal echocardiographic image at ventricular level with double inlet left ventricle showing common atrioventricular valve (3) in this chamber. B, Observe correspondence between anatomic specimen and echocardiographic image. Interatrial septum (IS) can be seen through valve. LV, Left ventricle.
Before the advent of 2-dimensional echocardiography, angiography was the diagnostic technique of choice for LV double inlet. However, it is an invasive technique that cannot be performed at the patient’s bedside. Two-dimensional echocardiography with 3 modalities of Doppler and segmental analysis have made it possible to characterize the different complex congenital malformations of the heart.20-23 In this comparative anatomoechocardiographic study of LV double inlet, we found that TTE information was incomplete, whereas TEE technique provided precise information regarding atrial situs, number and characteristics of the atrioventricular
Journal of the American Society of Echocardiography March 2005
Figure 8 A, Transthoracic 5-chamber image with anterior angulation in double inlet left ventricle (LV) shows discordant ventriculoarterial connection with stenotic pulmonary valve (left) and aorta (Ao) (right). B, Anatomic specimen shows open right ventricle connected to right-sided aorta and pulmonary artery (PA) in left posterior position connected to LV. RV, Right ventricle; VSD, ventricular septal defect.
Figure 9 A, Transthoracic echocardiographic image with anterior angulation shows discordant ventriculoarterial connection in double inlet left ventricle. Great arteries arise from inappropriate ventricles with subpulmonary stenosis (arrow). Ventricles are normally lateralized. B, Anatomic specimen shows same characteristics described for echocardiographic image. Ao, Aorta; LA, left atrium; LV, left ventricle; PA, pulmonary artery; RA, right atrium; RV, right ventricle.
valves, subvalvular apparatus, ventriculoarterial connection (including semilunar valves and the spatial relationship of great vessels), position of the rudimentary RV, and associated anomalies such as septal defects.24 Echocardiography is a noninvasive, reproducible technique that can be performed at the patient’s bedside. It shows strong correlation with the anatomic findings of corresponding specimens. A comprehension of the morphology of LV double inlet provides a frame of reference for the correct interpretation of diagnostic images and the intentional search for elements that will establish the diagnosis
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of congenital malformations of the heart with precision, as this comparative study demonstrates. Certain characteristics, such as straddling of atrioventricular valves, deserve special emphasis in the echocardiographic evaluation.25,26 These efforts have the goal of obtaining precise and complete information to establish or confirm a diagnosis in a timely manner so that the surgeon can select the appropriate intervention that will improve the quality of life and prognosis of the patient.26,27 In conclusion, echocardiography is a noninvasive diagnostic technique that has demonstrated excellent correlation of images with the morphologic findings of anatomic specimens. Thus, it provides the opportunity to characterize the anatomic and functional features of LV double inlet for patients and orient optimal surgical treatment. REFERENCES 1. Becker AE, Anderson RH. Pathology of congenital heart disease. London: Butterworth; 1981. p. 241–56. 2. Van Praagh R, Ongley PA, Swan HJC. Anatomic types of single or common ventricle in man, morphologic and geometric aspects of 68 necropsied cases. Am J Cardiol 1964;13:367-86. 3. Lev M, Libertson RR, Kirkpatrick JR, Eckner FAO, Arcilla RA. Single (primitive) ventricle. Circulation 1969;39:577-91. 4. Anderson RH, Becker AE, Freedom RM, Quero-Jimenez M, Macartney FJ, Shinebourne EA, et al. Problems in the nomenclature of the univentricular heart. Herz 1979;4:97-102. 5. Anderson RH. Weasel words in pediatric cardiology: single ventricle. Int J Cardiol 1983;2:425-9. 6. De la Cruz MV, Miller BL. Double inlet left ventricle. Circulation 1968;37:249-60. 7. Rigby ML, Anderson RH, Gibson D, Jones OD, Joseph MC, Shinebourne EA. Two-dimensional echocardiographic categorization of the univentricular heart: ventricular morphology, type, and mode of atrioventricular connection. Br Heart J 1981;46:603-12. 8. Freedom RM, Picchio F, Duncan WJ, Harder JR, Maes CAF, Rowe RD. The atrioventricular junction in the univentricular heart: a two-dimensional echocardiographic analysis. Pediatr Cardiol 1982;3:105-17. 9. Huhta JC, Seward JB, Tajik AJ, Hagler DJ, Edwards WD. Two-dimensional echocardiographic spectrum of univentricular atrioventricular connection. J Am Coll Cardiol 1985;5: 149-57. 10. Muñoz-Castellanos L, Ramírez S, Kuri Nivon M, Salinas Sánchez C. Doble entrada ventricular izquierda: Morfología y anatomía quirúrgica. Arch Inst Cardiol Mex 2000;70:136-47. 11. Shiraishi H, Silverman NH. Echocardiographic spectrum of double inlet ventricle: evaluation of the univentricular communication. J Am Coll Cardiol 1990;15:1401-8.
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12. Hatle L, Angelsen B. Doppler ultrasound in cardiology. Philadelphia: Lea and Febiger; 1982. 13. Berman W. Pulsed Doppler in clinical pediatrics. New York: Futura Publishing Company; 1983. 14. Tynan MJ, Becker AE, Macartney FJ, Jimenez M, Shinebourne EA, Anderson RH. Nomenclature and classification of congenital heart disease. Br Heart J 1979;41:544-53. 15. Holmes AF. Case of malformation of the heart. Trans MedicoChirurgical Soc Edinburgh 1824;1:252-9. 16. Abbott ME. Atlas of congenital cardiac diseases. New York: American Heart Association; 1936. 17. Taussig MB. Congenital malformations of the heart. New York: The Commonwealth Fund; 1947. 18. Streeter GL. Developmental horizons in human embryos: descriptions of age group XIII, embryos about 4 or 5 millimeters long, and age group XIV, period of indentation of the lens vesicle. Carnegie Contrib Embryol 1948;541:211-45. 19. Streeter GL. Developmental horizons in human embryos: description of age group XV, XVI, XVII and XVIII, being the third issue of a surgery of the Carnegie collection. Carnegie Contrib Embryol 1948;211:133-203. 20. Sahn DJ, Harder JR, Freedom RM, Duncan WJ, Rowe RD, Allen HD, et al. Cross-sectional echocardiographic diagnosis and subclassification of univentricular hearts: imaging studies of atrioventricular valves, septal structures and rudimentary outflow chambers. Circulation 1982;66:1070-7. 21. Bevilacqua M, Sanders SP, Van Praagh S, Colan SD, Parness I. Double-inlet single left ventricle: echocardiographic anatomy with emphasis on the morphology of the atrioventricular valves and ventricular septal defect. J Am Coll Cardiol 1991; 18:559-68. 22. Freedom RM, Picchio F, Duncan WJ, Harder JR, Rowe RD. The atrioventricular junction in the univentricular heart: a two-dimensional echocardiographic analysis. Pediatr Cardiol 1982;3:105-17. 23. Fasoli G, Daliento L, Rossi M, Scattolin G, Roelandt J. M-mode contrast echocardiography in patients with univentricular heart. Eur Heart J 1983;4:415-23. 24. Seward JB, Khandheria BK, Oh JK, Abel MD, Hughes RW, Edwards WD, et al. Transesophageal echocardiography: technique, anatomic correlations, implementation, and clinical applications. Mayo Clinic Proc 1988;63:649-80. 25. Tandon R, Becker AE, Moller JH, Edwards JE. Double inlet left ventricle: straddling tricuspid valve. B Heart J 1974;36: 747-59. 26. Rice MJ, Seward JB, Edwards WD, Hagler DJ, Danielson GK, Puga FJ, et al. Straddling atrioventricular valve: two-dimensional echocardiographic diagnosis, classification and surgical implications. Am J Cardiol 1985;55:505-13. 27. Mair DD, Hagler DJ, Julsrud PR, Puga FJ, Scaf HV, Danielson GK. Early and late results of the modified Fontan procedure for double-inlet left ventricle: the Mayo Clinic experience. J Am Coll Cardiol 1991;18:1727-32.