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3D echocardiography in congenital heart disease: a valuable tool for the surgeon Marietta Charakida1, Kuberan Pushparajah1 & John Simpson*,1
Abstract: Real-time 3D echocardiography has been used increasingly in the assessment of patients with congenital heart disease. A number of studies have confirmed that this modality can be used as a complementary method to delineate morphology and spatial relationships of simple and more complex congenital heart lesions during surgical planning. Communication between the echocardiographer and surgeon can be simplified as simulation of surgical views can be achieved, thus minimizing the potential for error related to mental reconstruction. This review summarizes the available evidence for the role of real-time 3D echocardiography in congenital heart disease as an imaging modality to assist surgeons.
Echocardiography remains the dominant imaging modality for planning surgical repair of congenital heart disease lesions. The high temporal and spatial resolution of the technique means that this is frequently the sole imaging modality used prior to undertaking surgical repair [1] . Increasingly, other imaging modalities are being used to supplement echocardiographic data including both computed tomography (CT) and MRI. CT and MRI have the advantage of the absence of constraints of acoustic windows and the images are automatically orientated in an anatomic fashion with inclusion of external anatomic reference points. In this review we will concentrate on the use of 3D echocardiography in assisting the surgeon when congenital heart disease lesions are to be repaired.
Keywords
• 3D echocardiography • congenital heart disease • surgical • valvular disease
Traditional approach Traditionally, the echocardiographic method used to plan surgical repair has been by cross-sectional acquisition of a standardized series of sonographic cut planes and slower ‘sweeps’ of the area of interest so that a 3D appreciation of the anatomy is built up in the mind of the operator. The echocardiographic images can be obtained by transthoracic or by transesophageal echocardiography (TEE). In a minority of cases, intracardiac echocardiography has been applied to the surgical setting but has been far more widely used in the context of guidance of catheter intervention. From the perspective of the surgeon, guidance of the surgical procedure by cross-sectional echocardiography has largely been by preoperative review of imaging information coupled with intraoperative imaging both before and after the surgical repair. Assessment of the cardiac lesion at the time of repair by the surgeon is self-evidently essential to the cardiac repair but it is important for the cardiologist to understand the means by which the surgeon views and assesses the heart. The surgeon assesses the heart when the heart is arrested following the use of cardioplegia. Thus, their assessment of structures such as valves is not dynamic but static. Their view of intracardiac structures is most commonly achieved via the tricuspid valve by opening the right atrium. This type of approach is used to assess atrioventricular septal defects (AVSDs), ventricular septal defects (VSDs) and 1 Department of Congenital Heart Disease, Evelina London Children’s Hospital, London, SE1 7EH, UK *Author for correspondence: Tel.: +44 20 7188 2308; Fax: +44 20 7188 2307; [email protected]
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Review Charakida, Pushparajah & Simpson lesions such as tetralogy of Fallot. Opening the atrial septum permits visualization of the mitral valve (MV) to allow repair. For some lesions, such as aortic valve stenosis or subaortic stenosis, the surgeon will visualize the lesion via the aortic valve itself. Opening of the pulmonary valve may facilitate access to lesions such as doubly committed subarterial VSDs, which are located immediately below the semilunar valves. Occasionally, the A
surgeon will gain access to the muscular or apical region of the ventricular septum via a ventriculotomy but this tends to be used only when other access is impossible. Additional surgical testing of atrioventricular valves by rapid injection of saline into the ventricle provides additional direct information about valve competence during the procedure on the nonbeating heart. However, it should be emphasized that
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Figure 1. 3D echocardiography and atrioventricular junction. (A) 3D transesophageal echocardiographic view of the atrioventricular junction illustrating the mitral and tricuspid valves and the relative position of the aorta. This projection is from the atrial aspect and is orientated anatomically so that the relationships of structures are intuitive. (B) Simulated anatomic view of the atrioventricular junction from the atrial side. (C) 3D transesophageal echocardiographic view of the atrioventricular junction from the ventricular side. The mitral and tricuspid valves are seen en face and the aorta and right ventricular outflow tracts are also visible. (D) Simulated anatomic view of the mitral and tricuspid valves from the ventricular aspect. AMVL: Anterior mitral valve leaflet; Ao: Aorta; Inf: Inferior; L: Left; PMVL: Posterior mitral valve leaflet; R: Right; RVOT: Right ventricular outflow tract; Sup: Superior; TV: Tricuspid valve. (B & D) Courtesy of Heartworks (Inventive Medical, London, UK).
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Figure 2. 3D echocardiography in the assessment of mechanisms of mitral regurgitation. (A) Transthoracic 3D multiplanar reformatted imaging used to assess the mitral valve in a patient with prolapse of the A2 cusp. The red, green and blue planes of interrogation are freely adjusted so that the mitral valve can be cut in any given plane. In this example, the green plane is placed directly across the A2 and P2 scallops of the mitral valve (top right pane) with a corresponding long axis view in the top left pane and a plane through the width of the anterior mitral valve leaflet (lower left pane). This permits a systematic interrogation of the mitral valve using clearly defined imaging plane. (B) True cleft in the anterior leaflet of the mitral valve using anatomic orientation, visualized from the atrial aspect. AMVL: Anterior mitral valve leaflet; Inf: Inferior; L: Left; LA: Left atrium; LV: Left ventricle; MV: Mitral valve; R: Right; RA: Right atrium; Sup: Superior. For color images please see www.futuremedicine.com/doi/full/10.2217/fca.14.38.
the surgical view of the valves is from the atrial aspect and the chordal support on the ventricular aspect of the valve is less readily visualized and may require assistance of other technologies such as the cardioscope [2] . 3D echocardiography There have been dramatic advances in 3D echocardiographic techniques over the past decade [3] . Until the introduction of the matrix 3D ultrasound probe, 3D images were produced from multiple 2D images acquired over many cardiac cycles using either transthoracic or transesophageal rotational probes. This technique suffered from motion artifact and the time required for acquisition and offline analysis made it impossible to introduce into clinical workflow. The matrix ultrasound probe permitted real-time send/receive from a single probe where stacked piezoelectric crystals meant that there was a depth to the sonographic image so that a ‘pyramid’ of ultrasound data was created [4,5] . This technology
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has evolved to the extent that there are currently different 3D echocardiographic modalities, which have been tailored to address different clinical situations where the required field of view, color flow Doppler and frame rate requirements may vary. The exact nomenclature for the different 3D modalities varies between manufacturers but is summarized in brief. ‘Full volume’ acquisitions permit incorporation of a wide field of view into the 3D volumetric dataset. The volume may be acquired over one or multiple cardiac cycles, with acquisition gated to the electrocardiographic signal. Increasing the number of cardiac cycles for acquisition increases the temporal resolution but also the potential for movement artifacts. Arrhythmias and probe movement can cause ‘stitch artifacts’, which adversely affects imaging of anatomic structures. Suspension of respiration or breath holding, when possible, should be performed to reduce such artifacts. In the context of significant arrhythmias, live imaging modes are preferred because they avoid reconstruction of
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Review Charakida, Pushparajah & Simpson images when the heart rate is irregular. The ‘live 3D’ mode centers the echocardiographic image on a pyramidal-shaped slice of approximately 50° width and 30° depth to facilitate good temporal resolution in a more restricted imaging field than full volume acquisitions. The ‘zoom’ mode displays a user-defined area of interest in real time so it is unaffected by arrhythmia or patient movement. The position of the 3D volume can be adjusted to center it on a specific region and the size of the interrogation box is adjusted to optimize frame rate and image definition. Once a 3D echocardiographic data set has been acquired onto the ultrasound system this data can be retrospectively interrogated in any desired projection to visualize the cardiac structures of
interest. Multiple ‘cropping’ methods are available such as single-slice plane or more commonly cropping in any of the predetermined planes (x, y and z), which can be rotated and manipulated to align to relevant cardiac structures. This is a crucial advantage compared with conventional 2D imaging because imaging projections can be generated that are unique to 3D echocardio graphy and cannot be replicated by conventional 2D techniques. Volumetric analysis can also be performed manually or semi-automatically using segment ation techniques. Integration of this information can permit dyssynchrony assessment. Assessment of left ventricular function can be performed more accurately using 3D echocardiography as there
Figure 3. Multiplanar reformatted and rendered 3D images of the aortic valve demonstrating perforation of the right coronary cusp. The top left pane shows a short axis of the aortic valve. The plane of interrogation is shown in the top right pane where the line of sight is from the red dotted line. The lower right pane demonstrates the benefits of the 3D technique by having the depth of field to show the perforated cusp in a manner akin to the surgical visualization. LCC: Left coronary cusp; LV: Left ventricle; NCC: Noncoronary cusp; RCC: Right coronary cusp; RVOT: Right ventricular outflow tract. For color images please see www.futuremedicine.com/doi/full/10.2217/fca.14.38.
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Figure 4. Aortic cusp prolapse with doubly committed subarterial defect. The top left pane shows a multiplanar reformatted long axis view of the left ventricle, in which the right coronary cusp is seen prolapsing into the ventricular septal defect. The lower right pane demonstrates a 3D-rendered view of the prolapsed aortic cusp as this is viewed from the right ventricle. LA: Left atrium; LV: Left ventricle; PV: Pulmonary valve; RCC: Right coronary cusp; RV: Right ventricle; TV: Tricuspid valve.
is no need for geometric assumptions about the shape of the left ventricle. The orientation of 3D echocardiographic views has been highly variable in clinical practice. This has posed a significant problem because the advantage of 3D echocardiography in terms of the ability to present novel projections can be nullified if the images produced are not presented in a consistent and intuitive manner for interpretation. Therefore we recommend that the optimal means of presenting 3D echocardiographic images is in an ‘anatomic’ manner because this matches the way in which magnetic resonance, CT and angiographic images are presented (Figure 1A–D) [6] . Thus, with increased application of multimodality imaging to structural heart disease, the various imaging modalities will be consistent with
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each other. A more detailed description of this approach has been published [7] . Recently, 3D echocardiographic standards have been published relating to adult patients [8] . For the most part, such recommendations have proposed anatomic or near anatomic image display. Some projections of atrioventricular valves have been described as ‘surgical’ views in that the valve is projected from the atrial aspect, closely matching the view of the surgeon approaching valve repair from the atrial side (Figure 1A & B, & Supplementary Video 1A & B, see online at www.futuremedicine.com/doi/ suppl/10.2217/fca.14.38) [9] . Clinical applications of 3D echocardiography 3D echocardiography can provide detailed functional information to assist in optimal selection
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Review Charakida, Pushparajah & Simpson of patients for surgical repair but its main advantage in presurgical planning relies on its ability to enhance morphological information for intracardiac structures. This knowledge can prove vital for better understanding of the pathophysiology and optimal surgical planning for the repair of a wide range of cardiac defects including valvular abnormalities as well as more complex cardiac abnormalities [10] . ●●Valvular heart disease
3D echocardiography has been used extensively in the diagnostic evaluation of valvular heart disease. Among the different valves, MV function and anatomy has been most extensively studied with 3D echocardiography [11,12] . The valve has a saddle shape configuration and complex interrelationships to chordae, papillary muscles and ventricular walls. Normal MV function relies on the integrated role of all these various components. There are numerous etiologies of MV disease and detailed preoperative comprehensive evaluation of the MV apparatus is vital not only to determine the feasibility for MV reconstruction but also to optimize the surgical technique for successful MV repair. Surgical repair rather than replacement of the MV assumes particular importance in growing patients because insertion of a prosthetic valve commits the patient to serial replacement to accommodate growth.
Figure 5. 3D-rendered view that demonstrates the circumferential extent of the subaortic membrane (asterisk) as this is viewed through the aortic valve. AoV: Aortic valve; LA: Left atrium; RA: Right atrium.
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Using real-time 3D (RT3D) TEE, a comprehensive assessment of the MV involves the acquisition of the so-called en face view, which mirrors the view that the surgeons will have when looking from the left atrium to MV. In addition, using the full volume data detailed characterization of the interrelationship of the MV to adjacent structures can be established from the ventricular perspective. In the presence of mitral regurgitation, the mechanisms of mitral regurgitation are important parameters to consider before surgical repair. Several studies have shown that 3D echocardiography is a more sensitive modality compared with 2D in identifying the area of pathology (i.e., abnormal MV leaflets and commissural defects, among others) in the MV apparatus but also to decipher complex geometric relationships (distortion and folding of the MV annulus), which can account for annular dilatation and be involved in the mechanisms of mitral regurgitation [13–16] . It can also provide complementary and additional information for localization of prolapsed scallops and MV clefts (Figure 2 & Supplementary Video 2B) . Studies using 3D TEE and color Doppler demonstrated the superiority of this modality for accurate assessment of the mechanisms of mitral regurgitation and provided additional information to the surgeons when MV repair was to be attempted [16] . The tricuspid valve can also be imaged effectively using 3D echocardiography. Projections can be obtained in an analogous manner to MV to localize areas of regurgitation and visualize morphological abnormalities of the valve leaflets. In more complex cases such as Ebstein’s anomaly, 3D echocardiography can complement cross-sectional imaging and demonstrate the abnormal rotation of the axis of the tricuspid valve, the anatomy of the chordal attachments and their extension to the right ventricular outflow tract thus providing detailed morphological information to the surgeons [17–21] . En face view of the valve and areas of ineffective coaptation can also be seen using 3D echocardiography [20] . This information will assist the surgeons in accurate evaluation of the size of the functional right ventricle and to estimate severity of tricuspid regurgitation. The anatomy of the tricuspid valve leaflets can be visualized including deficiency of leaflets. Importantly, redundant valve tissue can also be identified, which is central to techniques to recreate a more competent tricuspid valve orifice when repair of the tricuspid valve is to be undertaken.
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Figure 6. Straddling atrioventricular valves. 3D-rendered views that demonstrate: (A) straddling mitral valve chords to the right ventricular wall; and (B) straddling tricuspid valve chords to the left heart. Closure of the ventricular septal defect in these cases is challenging, as closure of the ventricular septal defect may compromise the function of the atrioventricular valves. Inf: Inferior; L: Left; LA: Left atrium; LV: Left ventricle; MV: Mitral valve; R: Right; RA: Right atrium; RV: Right ventricle; Sup: Superior; TV: Tricuspid valve.
As far as semilunar valves are concerned, RT3D echocardiography can be used to assist in presurgical planning or for intraoperative guidance and there are reports that this modality can be very useful in identifying aortic valve injury, which can involve leaflet tear or perforation and quantify the degree of aortic valve regurgitation (Figure 3 & Supplementary Videos 3A & 3B) [22–24] . 3D TEE can provide an en face view of the aortic valve to allow assessment of the coaptation lines and leaflet integrity with no out-of-plane motion, in contrast to 2D echocardiography. The presence of aortic cusp prolapse and its dynamic nature during the cardiac cycle can also be demonstrated using a 3D-rendered technique (Figure 4 & Supplementary Video 4) . Use of the multiplanar reformatted technique permits alignment to the prolapsing cusp in multiple planes to confirm which cusp is prolapsing and additional information on the alignment of aortic cusps to each other. This information is important when repair or resuspension of the aortic valve leaflet is to be undertaken to prevent long term progression of aortic valve regurgitation. ●●Outflow obstruction & subaortic
membrane
There are several mechanisms of left ventricular outflow obstruction, which can include
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the presence of fibromuscular stenosis, accessory left atrioventricular (AV) valve tissue, papillary muscles, accessory chords or diffuse hypoplasia resulting in tunnel stenosis [25,26] . Characterization of the mechanism of left ventricular outflow obstruction is important before embarking onto surgery as surgical resection is commonly performed through the aortic valve with restricted views [27] . 3D echocardiography can provide complementary information to cross-sectional imaging in such cases by providing detailed morphological information and intracardiac views from the ventricular side. Using this approach, accessory chords or papillary muscles and their attachments can be visualized and decision can be made on whether these represent part of the primary or secondary support apparatus of the valve leaflets and as to whether their resection will compromise valve function. This information can be very important for the surgeons as their field of view through the aortic valve is often limited and extensive resection may lead to significant aortic valve regurgitation postoperatively. Detailed characterization of the circumferential extent and severity of subaortic membrane has also been described with 3D by using a projection through the aortic valve combined with view from the ventricle and view of the long axis of the left
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Review Charakida, Pushparajah & Simpson ventricle (Figure 5 & Supplementary Video 5) [28,29] . Accurate analysis of the effective orifice area and measurement of the distance between the membrane and aortic valve leaflets will inform the surgeons on whether resection of the subaortic membrane is likely to compromise the aortic valve function. ●●Ventricular septal defects
Some types of VSDs, for example, apical muscular or inferior inlet or outlet defects might be difficult for the surgeon to repair as their view is often limited through the tricuspid valve, the defect can be quite distant from the tricuspid valve and in some cases the VSD position can be hidden in heavy right ventricular trabeculations [30] . In these cases, 3D echocardiography can provide key information in presurgical planning with regards to size, shape of the defect and accurate location [31] . The distance of the VSD from important landmarks such as tricuspid, pulmonary valve and moderator band can be accurately calculated. This information will assist in decision-making on whether catheter closure of the defect is likely to be successful or whether surgical intervention is the only approach forward [32] .
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In certain cases, it might be decided that the VSD is not amenable to immediate intervention and palliative pulmonary artery banding should be undertaken to improve clinical symptoms. In the presence of multiple defects, it can also be quite challenging using cross-sectional imaging and Doppler measurements to decide about the necessity to embark on complex surgery to close the various defects [33–36] . Using 3D echocardiography and different projections accurate sizing of the various defects can be performed to facilitate presurgical planning [37] . In some complicated cases, there can be straddling of the tricuspid or MV over the VSD (Figure 6 & Supplementary Video 6A & B) . VSD closure, in these circumstances, is complex, and surgeons prefer a full understanding of the anatomy of the defect and its relationship preoperatively [38] . Using 3D echocardiography, straddling chords can be demonstrated along their length from the point of origin on the atrioventricular valve to the point of insertion into the contralateral ventricle and this information can facilitate decision-making on whether closure of the VSD is likely to compromise the function of the straddling valve.
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Figure 7. 3D echocardiography and atrioventricular septal defect. (A) View of the left atrioventricular valve in a patient who has undergone previous atrioventricular septal defect repair. The superior and inferior bridging leaflets have been sutured to form a neoaortic leaflet. The mural and neoaortic leaflets show an identifiable zone of failure of coaptation. (B) This projection illustrates how the neoaortic leaflet and the mural leaflet fail to coapt with the neoaortic leaflet showing a degree of prolapse into the left atrium. Using the color flow Doppler the region of atrioventricular valve regurgitation is localized. IBL: Inferior bridging leaflet; Inf: Inferior; L: Left; LA: Left atrium; LV: Left ventricle; R: Right; SBL: Superior bridging leaflet; Sup: Superior.
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Figure 8. 3D echocardiography and double outlet right ventricle. (A) Rendered 3D echocardiographic projection from the apex of the heart demonstrating the relationship of the mitral valve, tricuspid valve, aorta and pulmonary artery to each other. An asterisk (*) shows the interventricular communication. This view is not achievable by cross-sectional echocardiography because of the lack of depth of field. (B) Rendered 3D echocardiographic projection of double outlet right ventricle. This projection is achieved by cropping away the free wall of the right ventricle so that the ventricular septum, interventricular communication and the great arteries are visualized from the right ventricular aspect. Both the apical and right ventricle projections assist in determining the optimal means of surgical repair. Inf: Inferior; L: Left; MV: Mitral valve; PA: Pulmonary artery; R: Right; RA: Right atrium; RV: Right ventricle; Sup: Superior; TV: Tricuspid valve. ●●Complex congenital heart defects
Recent innovations in the field of RT3D have allowed this modality to offer unique and clinically useful information in the evaluation of patients with complex congenital heart disease such as AVSD and double outlet right ventricle. Nearly all of patients with an AVSD will require surgical intervention at some stage in their life. The primary surgical repair consists of closure of interatrial and interventricular communication and repair of the atrioventricular valves. Accurate assessment of the morphology and its anatomic inter-relationships is very important to determine whether or not the atrioventricular valve is amenable to surgical repair and whether this can be divided into two separate AV valves with adequate function. In the decision-making process 3D echocardiography has proven invaluable for the qualitative and quantitative evaluation of AV function but also for the assessment of atrial and ventricular communications [39] . Hlavacek et al. showed that gated 3D views could be cropped to obtain en face views of the atrial and ventricular septa [40] . These views provide a clear understanding of the relationships of the bridging leaflets to
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the septal structures and how these relationships determine the level of shunting (atrial, ventricular or both) (Figure 7 & Supplementary Video 7A & B) . Following repair, although the surgeon has the opportunity to immediately inspect the AV valves and test their competency with saline, this technique is nonphysiologic and might not reflect their competence in dynamic moving heart. Following AVSD repair, the geometry of the left AV valve and its supporting apparatus is altered and as a result in some cases progressive left AV valve regurgitation may also develop. Using crosssectional imaging, it is often difficult to assess the number of jets as many may run along a commissure and can appear as multiple jets. It can also be difficult to delineate the origin of the regurgitant jet and relate it to valve pathology. Takahashi et al. demonstrated, by using 3D echocardiography, that the severity of left AV valve regurgitation following AVSD repair is linked to the dilatation of the valve annulus, leaflet prolapse and to the presence of an acute angle between the anterolateral papillary muscle and the left AV valve annulus [41] . Shortened chordae can be seen by 3D and their impact on leaflet mobility
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Review Charakida, Pushparajah & Simpson can be estimated. The sites of poor coaptation and specific commissural mismatch as mechanism of left AV valve regurgitation can be better appreciated using 3D echocardiography [42] . The complete line of apposition between the superior and inferior bridging leaflets can also be assessed. Reoperation for left AV valve regurgitation is technically demanding and can involve cleft closure, annular reduction, commissurotomy, patch augmentation of deficient leaflet tissue. Accurate characterization of the pathophysiology of the left AV valve regurgitation would therefore be necessary for the surgeons before embarking into a repeat surgery to repair or replace the regurgitant valve [43,44] . Another important association that has significant surgical implications is the presence of a double orifice left AV valve [45,46] . This information can be accurately obtained by 3D echocardiography whereas identification of this pathology with cross-sectional imaging has been disappointing. Hoohenkerk et al. have documented that in the presence of double orifice left AV valve, optimal surgical results are obtained by preserving the tissue bridge and tension apparatus and repairing the AV valve as a three-leaflet valve [47] . In other cases of complex congenital heart disease lesions, 3D echocardiography can also prove invaluable before planning a surgical repair. Double outlet right ventricle, transposition of the great arteries with ventricular septal defect and other cases with discordant atrioventricular and ventriculo-arterial connections are characteristic examples [48] . Understanding the complex relationships between the great arteries, the ventricular septal defect and the atrioventricular and semilunar valves is vital before embarking into surgical repair (Figure 8 & Supplementary Video 8A & B) . Depending on the underlying morphology, the surgical approach might involve an arterial switch operation, baffling of the left ventricular outflow to the ascending aorta or a single ventricle repair when septation cannot be achieved [49] . In such cases, 3D echocardiography can produce unique projections, which can include all of the components of the planned surgical repair with added depth thus allowing accurate presurgical planning and facilitating surgical decision-making [9] . Conclusion A number of studies have demonstrated that 3D echocardiography can provide incremental information to cross sectional imaging and enhance morphological information for complex
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congenital heart disease lesions. Intracardiac connections and relationships can be delineated and anatomy can be projected in various ways to guide surgical procedures. The added depth of field of view can often allow demonstration of all the components of the planned surgical repair in one projection. Therefore, discussions and decisions about surgical procedures can be made using ‘real’ images rather than running the risk of misinterpretation by individually mentally reconstructed projections. Nevertheless, despite its increasing use the technique remains a complementary method to cross-sectional imaging and further technological advances are required to resolve some of its technical limitations and allow its integration in routine clinical practice. Future perspective Developments in cardiac surgery mean that patients with increasingly complex cardiac lesions may be judged candidates for surgical repair. This emphasizes the need for detailed preoperative imaging investigation to provide all necessary information for an effective surgical repair. Multimodality imaging is commonly employed to take advantage of the strengths of different techniques including 3D echocardiography, MRI and CT. However, 3D echocardiography has the advantage of being portable at the point of care, noninvasive and no other current technique can provide the depth of field and temporal resolution to assess heart valves. Additionally, 3D echocardiography is cheap compared with MRI and CT. Future developments in 3D echocardiographic techniques will address some current limitations such as spatial and temporal resolution. Postprocessing algorithms that are currently limited to a research level will allow for fusion of multiple images into one to increase the field of view and eliminate acoustic shadowing [50] . This includes not just B-mode image data, but also integration of color Doppler data, which provides a noninvasive method of flow visualization and quantification [51] . These will enhance the scope of 3D color Doppler, which is constrained by a limited field of view, low temporal resolution and stitching artifact from multiple interleaved acquisitions. Emerging technologies to enhance frame rates to several hundred frames per second has already been described in a research setting [52] . This will overcome visualization of rapidly moving structures such as atrioventricular and semilunar
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3D echocardiography in congenital heart disease valves. The availability of powerful post processing hardware and software is such that the long postprocessing times, which have hindered the clinical application of these technologies, will also decrease significantly. Another significant advantage of 3D echocardiography is the potential for automation with the ability to acquire real-time 3D color Doppler data within a single cardiac cycle [53] . This will see integration of automated systems to allow quick image acquisition and postprocessing with minimal inter-user variability available for bedside echocardiographic assessment. The developments in matrix array probes and image processing algorithms will lead to further miniaturization of probes, which is especially relevant in pediatric patients. 3D TEE probes are only available for adults, but it is realistic to expect that these will be small enough for pediatric use in the coming years. The 3D display for preoperative planning will also improve with increased display options including holographic projections [54] . Additionally, the improved displays will be able to match the higher frame rates of the acquired images. 3D echocardiography must also be capable of integration with other imaging modalities such as fluoroscopy, CT or MRI. The translation of integration
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of MRI, CT and fluoroscopy with 3D echocardiography from a research technique to a more standard commercially available technology can be expected in the near future. Although these developments are heavily reliant on industry, the drive for industry participation must be led by clinicians working with physicists and engineers with a close contact to a clinical environment to allow rapid testing and validation of prototypes in a clinical environment with the aim of providing clinical benefit. Imaging vendors will have to match the clinical demand for fast, high-quality imaging with minimal postprocessing time at the bedside and in the operating theater. Over the next decade, it is likely that 3D echocardiography will become firmly integrated into surgical planning and perioperative imaging. As the technology becomes more commonplace, adherence to international guidelines and recommendations formed of expert consensus will lead to a uniform approach to image display, which will allow rapid understanding of images being displayed by both the imaging and surgical teams. As patients with congenital heart disease reach adulthood, long-term complications will inevitably become apparent and reconstructive surgeries in these cases can also be challenging. Optimal results will heavily rely on accurate preoperative
Executive summary 3D acquisition ●●
A number of 3D echocardiographic modalities (full-volume acquisition, live 3D echocardiographic imaging) are available and can provide complementary morphological and functional information for simple and complex congenital heart disease lesions to tailor surgical needs.
Valvular heart disease ●●
The mitral valve has a complex configuration and it is ideally suited for 3D echocardiography. Preoperative
reconstruction of the mitral valve apparatus can be achieved, inter-relationships can be delineated and presurgical planning can be optimized to maximize opportunities for successful mitral valve repair. A similar approach can be extended to the tricuspid valve and other atrioventricular valves. Outflow obstruction ●●
Important information about the type and degree of outflow obstruction will inform the surgeons on whether extensive resection is likely to compromise the integrity of the valve apparatus.
Ventricular septal defects ●●
The size, shape and location of ventricular septal defects can be accurately assessed by 3D echocardiography. The
presence of straddling atrioventricular valves and their connections can be accurately assessed before embarking in complex surgical procedures. Complex congenital heart disease lesions ●●
Surgical strategy and repair can be facilitated by information obtained using 3D echocardiography for complex cardiac lesions such as atrioventricular septal defects and double outlet right ventricle.
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Review Charakida, Pushparajah & Simpson imaging and planning. Understanding of the anatomical substrate using 3D echocardiography would be necessary together with other imaging modalities and real-time 3D echocardiographic guidance is likely to be routine clinical practice. Acknowledgements The authors would like to thank Heartworks for the system that they used to generate the anatomical images presented in this paper.
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The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties. No writing assistance was utilized in the production of this manuscript.
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•• Highlights the importance of anatomic orientation for 3D echocardiographic images. Consistency in 3D echocardiographic projections allows comparisons between different imaging modalities and enhances understanding.
Margonato A. Accuracy of real-time 3D echocardiography in the evaluation of functional anatomy of mitral regurgitation. Int. J. Cardiol. 127(3), 342–349 (2008). regurgitation mechanism assessed by 2D and 3D echocardiography in patient with an abnormal left coronary artery arising from the pulmonary artery. Arch. Cardiovasc. Dis. 101(9), 585–587 (2008). 15 Maragiannis D, Little SH. Quantification of
mitral valve regurgitation: new solutions provided by 3D echocardiography. Curr. Cardiol. Rep. 15(8), 384 (2013). 16 Zakkar M, Patni R, Punjabi PP. Mitral valve
regurgitation and 3D echocardiography. Future Cardiol. 6(2), 231–242 (2010). 17 Taktak A, Acar P, Dulac Y et al. [A new
approach to the tricuspid valve in Ebstein’s anomaly by real time 3D echocardiography]. Arch. Mal. Coeur Vaiss. 98(5), 531–537 (2005). 18 Bharucha T, Anderson RH, Lim ZS,
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dimensional echocardiography in valvular heart disease. Curr. Opin. Cardiol. 20(2), 122–126 (2005). 24 Dreyfus J, Feldman LJ, Lepage L et al.
Iatrogenic aortic valve perforation assessed using three-dimensional transoesophageal echocardiography. Arch. Cardiovasc. Dis. 104(8–9), 486–487 (2011). 25 Dall’Agata A, Cromme-Dijkhuis AH,
Meijboom FJ et al. Use of three-dimensional echocardiography for analysis of outflow obstruction in congenital heart disease. Am. J. Cardiol. 83(6), 921–925 (1999). 26 Ge S, Warner JG Jr, Fowle KM et al.
Morphology and dynamic change of discrete subaortic stenosis can be imaged and quantified with three-dimensional transesophageal echocardiography. J. Am. Soc. Echocardiogr. 10(7), 713–716 (1997).
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3D echocardiography in congenital heart disease 27 Khaw AV, von Bardeleben RS, Strasser C et al.
Direct measurement of left ventricular outflow tract by transthoracic real-time 3D-echocardiography increases accuracy in assessment of aortic valve stenosis. Int. J. Cardiol. 136(1), 64–71 (2009). 28 Bandarupalli N, Faulkner M, Nanda NC,
Pothineni KR. Erroneous diagnosis of significant obstruction by Doppler in a patient with discrete subaortic membrane: correct diagnosis by 3D-transthoracic echocardiography. Echocardiography 25(9), 1004–1006 (2008). 29 Marechaux S, Juthier F, Banfi C, Vincentelli A,
Prat A, Ennezat PV. Illustration of the echocardiographic diagnosis of subaortic membrane stenosis in adults: surgical and live three-dimensional transoesophageal findings. Eur. J. Echocardiogr. 12(1), E2 (2011). 30 Sivakumar K, Singhi A, Pavithran S. En face
reconstruction of VSD on RV septal surface using real-time 3D echocardiography. JACC Cardiovasc. Imaging 5(11), 1176–1180 (2012). 31 Kardon RE, Cao QL, Masani N et al. New
insights and observations in three-dimensional echocardiographic visualization of ventricular septal defects. Experimental and clinical studies. Circulation 98(13), 1307–1314 (1998). 32 Charakida M, Qureshi S, Simpson JM. 3D
echocardiography for planning and guidance of interventional closure of VSD. JACC Cardiovasc. Imaging 6(1), 120–123 (2013). 33 Backer CL, Winters RC, Zales VR et al.
Restrictive ventricular septal defect: how small is too small to close? Ann. Thorac. Surg. 56(5), 1014–1018 (1993). 34 Ishii M, Hashino K, Eto G et al. Quantitative
assessment of severity of ventricular septal defect by three-dimensional reconstruction of color Doppler-imaged vena contracta and flow convergence region. Circulation 103(5), 664–669 (2001). 35 Van den Bosch AE, Ten Harkel DJ, McGhie JS
et al. Feasibility and accuracy of real-time 3-dimensional echocardiographic assessment of ventricular septal defects. J. Am. Soc. Echocardiogr. 19(1), 7–13 (2006). 36 Kirklin JK, Castaneda AR, Keane JF,
Fellows KE, Norwood WI. Surgical management of multiple ventricular septal defects. J. Thorac. Cardiovasc. Surg. 80(4), 485–493 (1980). 37 Mercer-Rosa L, Seliem MA, Fedec A, Rome J,
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echocardiography in imaging muscular ventricular septal defects: does this have any impact on individual patient treatment? J. Am. Soc. Echocardiogr. 19(12), 1511–1519 (2006). •• Describes novel projections and additional information, which can be obtained by 3D echocardiography in the assessment of ventricular septal defects. 38 Huhta JC, Edwards WD, Danielson GK, Feldt
RH. Abnormalities of the tricuspid valve in complete transposition of the great arteries with ventricular septal defect. J. Thorac. Cardiovasc. Surg. 83(4), 569–576 (1982). 39 Kutty S, Smallhorn JF. Evaluation of
atrioventricular septal defects by threedimensional echocardiography: benefits of navigating the third dimension. J. Am. Soc. Echocardiogr. 25(9), 932–944 (2012). •• Comprehensive review about the use of 3D echocardiography in the evaluation of patients with atrioventricular septal defects. The geometrical complexity of the common atrioventricular valve and postoperative concerns following atrioventricular septal defect repair are highlighted. 40 Hlavacek AM, Crawford FA Jr, Chessa KS,
Shirali GS. Real-time three-dimensional echocardiography is useful in the evaluation of patients with atrioventricular septal defects. Echocardiography 23(3), 225–231 (2006). 41 Takahashi K, Mackie AS, Rebeyka IM et al.
Two-dimensional versus transthoracic real-time three-dimensional echocardiography in the evaluation of the mechanisms and sites of atrioventricular valve regurgitation in a congenital heart disease population. J. Am. Soc. Echocardiogr. 23(7), 726–734 (2010). 42 van den Bosch AE, van Dijk VF, McGhie JS
et al. Real-time transthoracic three-dimensional echocardiography provides additional information of left-sided AV valve morphology after AVSD repair. Int. J. Cardiol. 106(3), 360–364 (2006). 43 Kanani M, Elliott M, Cook A, Juraszek A,
Devine W, Anderson RH. Late incompetence of the left atrioventricular valve after repair of atrioventricular septal defects: the morphologic perspective. J. Thorac. Cardiovasc. Surg. 132(3), 640–646, 646.e1–3 (2006). 44 Roman KS, Nii M, Macgowan CK, Barrea C,
Coles J, Smallhorn JF. The impact of patch augmentation on left atrioventricular valve dynamics in patients with atrioventricular septal defects: early and midterm follow-up. J. Am. Soc. Echocardiogr. 19(11), 1382–1392 (2006).
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DR, Rijlaarsdam ME, Hazekamp MG. Long-term results of reoperation for left atrioventricular valve regurgitation after correction of atrioventricular septal defects. Ann. Thorac. Surg. 93(3), 849–855 (2012). 46 Hoohenkerk GJ, Bruggemans EF, Rijlaarsdam
M, Schoof PH, Koolbergen DR, Hazekamp MG. More than 30 years’ experience with surgical correction of atrioventricular septal defects. Ann. Thorac. Surg. 90(5), 1554–1561 (2010). 47 Hoohenkerk GJ, Wenink AC, Schoof PH et al.
Results of surgical repair of atrioventricular septal defect with double-orifice left atrioventricular valve. J. Thorac. Cardiovasc. Surg. 138(5), 1167–1171 (2009). 48 Chen GZ, Huang GY, Tao ZY, Liu XQ,
Lin QS. Value of real-time 3-dimensional echocardiography sectional diagnosis in complex congenital heart disease evaluated by receiver operating characteristic analysis. J. Am. Soc. Echocardiogr. 21(5), 458–463 (2008). 49 Pushparajah K, Barlow A, Tran VH et al.
A systematic three-dimensional echocardiographic approach to assist surgical planning in double outlet right ventricle. Echocardiogr. 30(2), 234–238 (2013). •• Provides novel views of intracardiac relations in patients with double outlet right ventricle morphology. This information is valuable during surgical planning. 50 Yao C, Simpson JM, Schaeffter T, Penney GP.
Multi-view 3D echocardiography compounding based on feature consistency. Phys. Med. Biol. 56(18), 6109–6128 (2011). 51 Gomez A, Pushparajah K, Simpson JM, Giese
D, Schaeffter T, Penney G. A sensitivity analysis on 3D velocity reconstruction from multiple registered echo Doppler views. Med. Image Anal. 17(6), 616–631 (2013). 52 Perrin DP, Vasilyev NV, Marx GR, Del Nido
PJ. Temporal enhancement of 3D echocardiography by frame reordering. JACC Cardiovasc. Imaging 5(3), 300–304 (2012). 53 Thavendiranathan P, Liu S, Datta S et al.
Automated quantification of mitral inflow and aortic outflow stroke volumes by threedimensional real-time volume color-flow Doppler transthoracic echocardiography: comparison with pulsed-wave Doppler and cardiac magnetic resonance imaging. J. Am. Soc. Echocardiogr. 25(1), 56–65 (2012). 54 Van den Bosch AE, Koning AH, Meijboom FJ
et al. Dynamic 3D echocardiography in virtual reality. Cardiovasc. Ultrasound 3, 37 (2005).
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3D echocardiography in congenital heart disease: a valuable tool for the surgeon Marietta Charakida1, Kuberan Pushparajah1 & John Simpson*,1
Abstract: Real-time 3D echocardiography has been used increasingly in the assessment of patients with congenital heart disease. A number of studies have confirmed that this modality can be used as a complementary method to delineate morphology and spatial relationships of simple and more complex congenital heart lesions during surgical planning. Communication between the echocardiographer and surgeon can be simplified as simulation of surgical views can be achieved, thus minimizing the potential for error related to mental reconstruction. This review summarizes the available evidence for the role of real-time 3D echocardiography in congenital heart disease as an imaging modality to assist surgeons.
Echocardiography remains the dominant imaging modality for planning surgical repair of congenital heart disease lesions. The high temporal and spatial resolution of the technique means that this is frequently the sole imaging modality used prior to undertaking surgical repair [1] . Increasingly, other imaging modalities are being used to supplement echocardiographic data including both computed tomography (CT) and MRI. CT and MRI have the advantage of the absence of constraints of acoustic windows and the images are automatically orientated in an anatomic fashion with inclusion of external anatomic reference points. In this review we will concentrate on the use of 3D echocardiography in assisting the surgeon when congenital heart disease lesions are to be repaired.
Keywords
• 3D echocardiography • congenital heart disease • surgical • valvular disease
Traditional approach Traditionally, the echocardiographic method used to plan surgical repair has been by cross-sectional acquisition of a standardized series of sonographic cut planes and slower ‘sweeps’ of the area of interest so that a 3D appreciation of the anatomy is built up in the mind of the operator. The echocardiographic images can be obtained by transthoracic or by transesophageal echocardiography (TEE). In a minority of cases, intracardiac echocardiography has been applied to the surgical setting but has been far more widely used in the context of guidance of catheter intervention. From the perspective of the surgeon, guidance of the surgical procedure by cross-sectional echocardiography has largely been by preoperative review of imaging information coupled with intraoperative imaging both before and after the surgical repair. Assessment of the cardiac lesion at the time of repair by the surgeon is self-evidently essential to the cardiac repair but it is important for the cardiologist to understand the means by which the surgeon views and assesses the heart. The surgeon assesses the heart when the heart is arrested following the use of cardioplegia. Thus, their assessment of structures such as valves is not dynamic but static. Their view of intracardiac structures is most commonly achieved via the tricuspid valve by opening the right atrium. This type of approach is used to assess atrioventricular septal defects (AVSDs), ventricular septal defects (VSDs) and 1 Department of Congenital Heart Disease, Evelina London Children’s Hospital, London, SE1 7EH, UK *Author for correspondence: Tel.: +44 20 7188 2308; Fax: +44 20 7188 2307; [email protected]
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Review Charakida, Pushparajah & Simpson lesions such as tetralogy of Fallot. Opening the atrial septum permits visualization of the mitral valve (MV) to allow repair. For some lesions, such as aortic valve stenosis or subaortic stenosis, the surgeon will visualize the lesion via the aortic valve itself. Opening of the pulmonary valve may facilitate access to lesions such as doubly committed subarterial VSDs, which are located immediately below the semilunar valves. Occasionally, the A
surgeon will gain access to the muscular or apical region of the ventricular septum via a ventriculotomy but this tends to be used only when other access is impossible. Additional surgical testing of atrioventricular valves by rapid injection of saline into the ventricle provides additional direct information about valve competence during the procedure on the nonbeating heart. However, it should be emphasized that
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Figure 1. 3D echocardiography and atrioventricular junction. (A) 3D transesophageal echocardiographic view of the atrioventricular junction illustrating the mitral and tricuspid valves and the relative position of the aorta. This projection is from the atrial aspect and is orientated anatomically so that the relationships of structures are intuitive. (B) Simulated anatomic view of the atrioventricular junction from the atrial side. (C) 3D transesophageal echocardiographic view of the atrioventricular junction from the ventricular side. The mitral and tricuspid valves are seen en face and the aorta and right ventricular outflow tracts are also visible. (D) Simulated anatomic view of the mitral and tricuspid valves from the ventricular aspect. AMVL: Anterior mitral valve leaflet; Ao: Aorta; Inf: Inferior; L: Left; PMVL: Posterior mitral valve leaflet; R: Right; RVOT: Right ventricular outflow tract; Sup: Superior; TV: Tricuspid valve. (B & D) Courtesy of Heartworks (Inventive Medical, London, UK).
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Figure 2. 3D echocardiography in the assessment of mechanisms of mitral regurgitation. (A) Transthoracic 3D multiplanar reformatted imaging used to assess the mitral valve in a patient with prolapse of the A2 cusp. The red, green and blue planes of interrogation are freely adjusted so that the mitral valve can be cut in any given plane. In this example, the green plane is placed directly across the A2 and P2 scallops of the mitral valve (top right pane) with a corresponding long axis view in the top left pane and a plane through the width of the anterior mitral valve leaflet (lower left pane). This permits a systematic interrogation of the mitral valve using clearly defined imaging plane. (B) True cleft in the anterior leaflet of the mitral valve using anatomic orientation, visualized from the atrial aspect. AMVL: Anterior mitral valve leaflet; Inf: Inferior; L: Left; LA: Left atrium; LV: Left ventricle; MV: Mitral valve; R: Right; RA: Right atrium; Sup: Superior. For color images please see www.futuremedicine.com/doi/full/10.2217/fca.14.38.
the surgical view of the valves is from the atrial aspect and the chordal support on the ventricular aspect of the valve is less readily visualized and may require assistance of other technologies such as the cardioscope [2] . 3D echocardiography There have been dramatic advances in 3D echocardiographic techniques over the past decade [3] . Until the introduction of the matrix 3D ultrasound probe, 3D images were produced from multiple 2D images acquired over many cardiac cycles using either transthoracic or transesophageal rotational probes. This technique suffered from motion artifact and the time required for acquisition and offline analysis made it impossible to introduce into clinical workflow. The matrix ultrasound probe permitted real-time send/receive from a single probe where stacked piezoelectric crystals meant that there was a depth to the sonographic image so that a ‘pyramid’ of ultrasound data was created [4,5] . This technology
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has evolved to the extent that there are currently different 3D echocardiographic modalities, which have been tailored to address different clinical situations where the required field of view, color flow Doppler and frame rate requirements may vary. The exact nomenclature for the different 3D modalities varies between manufacturers but is summarized in brief. ‘Full volume’ acquisitions permit incorporation of a wide field of view into the 3D volumetric dataset. The volume may be acquired over one or multiple cardiac cycles, with acquisition gated to the electrocardiographic signal. Increasing the number of cardiac cycles for acquisition increases the temporal resolution but also the potential for movement artifacts. Arrhythmias and probe movement can cause ‘stitch artifacts’, which adversely affects imaging of anatomic structures. Suspension of respiration or breath holding, when possible, should be performed to reduce such artifacts. In the context of significant arrhythmias, live imaging modes are preferred because they avoid reconstruction of
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Review Charakida, Pushparajah & Simpson images when the heart rate is irregular. The ‘live 3D’ mode centers the echocardiographic image on a pyramidal-shaped slice of approximately 50° width and 30° depth to facilitate good temporal resolution in a more restricted imaging field than full volume acquisitions. The ‘zoom’ mode displays a user-defined area of interest in real time so it is unaffected by arrhythmia or patient movement. The position of the 3D volume can be adjusted to center it on a specific region and the size of the interrogation box is adjusted to optimize frame rate and image definition. Once a 3D echocardiographic data set has been acquired onto the ultrasound system this data can be retrospectively interrogated in any desired projection to visualize the cardiac structures of
interest. Multiple ‘cropping’ methods are available such as single-slice plane or more commonly cropping in any of the predetermined planes (x, y and z), which can be rotated and manipulated to align to relevant cardiac structures. This is a crucial advantage compared with conventional 2D imaging because imaging projections can be generated that are unique to 3D echocardio graphy and cannot be replicated by conventional 2D techniques. Volumetric analysis can also be performed manually or semi-automatically using segment ation techniques. Integration of this information can permit dyssynchrony assessment. Assessment of left ventricular function can be performed more accurately using 3D echocardiography as there
Figure 3. Multiplanar reformatted and rendered 3D images of the aortic valve demonstrating perforation of the right coronary cusp. The top left pane shows a short axis of the aortic valve. The plane of interrogation is shown in the top right pane where the line of sight is from the red dotted line. The lower right pane demonstrates the benefits of the 3D technique by having the depth of field to show the perforated cusp in a manner akin to the surgical visualization. LCC: Left coronary cusp; LV: Left ventricle; NCC: Noncoronary cusp; RCC: Right coronary cusp; RVOT: Right ventricular outflow tract. For color images please see www.futuremedicine.com/doi/full/10.2217/fca.14.38.
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Figure 4. Aortic cusp prolapse with doubly committed subarterial defect. The top left pane shows a multiplanar reformatted long axis view of the left ventricle, in which the right coronary cusp is seen prolapsing into the ventricular septal defect. The lower right pane demonstrates a 3D-rendered view of the prolapsed aortic cusp as this is viewed from the right ventricle. LA: Left atrium; LV: Left ventricle; PV: Pulmonary valve; RCC: Right coronary cusp; RV: Right ventricle; TV: Tricuspid valve.
is no need for geometric assumptions about the shape of the left ventricle. The orientation of 3D echocardiographic views has been highly variable in clinical practice. This has posed a significant problem because the advantage of 3D echocardiography in terms of the ability to present novel projections can be nullified if the images produced are not presented in a consistent and intuitive manner for interpretation. Therefore we recommend that the optimal means of presenting 3D echocardiographic images is in an ‘anatomic’ manner because this matches the way in which magnetic resonance, CT and angiographic images are presented (Figure 1A–D) [6] . Thus, with increased application of multimodality imaging to structural heart disease, the various imaging modalities will be consistent with
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each other. A more detailed description of this approach has been published [7] . Recently, 3D echocardiographic standards have been published relating to adult patients [8] . For the most part, such recommendations have proposed anatomic or near anatomic image display. Some projections of atrioventricular valves have been described as ‘surgical’ views in that the valve is projected from the atrial aspect, closely matching the view of the surgeon approaching valve repair from the atrial side (Figure 1A & B, & Supplementary Video 1A & B, see online at www.futuremedicine.com/doi/ suppl/10.2217/fca.14.38) [9] . Clinical applications of 3D echocardiography 3D echocardiography can provide detailed functional information to assist in optimal selection
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Review Charakida, Pushparajah & Simpson of patients for surgical repair but its main advantage in presurgical planning relies on its ability to enhance morphological information for intracardiac structures. This knowledge can prove vital for better understanding of the pathophysiology and optimal surgical planning for the repair of a wide range of cardiac defects including valvular abnormalities as well as more complex cardiac abnormalities [10] . ●●Valvular heart disease
3D echocardiography has been used extensively in the diagnostic evaluation of valvular heart disease. Among the different valves, MV function and anatomy has been most extensively studied with 3D echocardiography [11,12] . The valve has a saddle shape configuration and complex interrelationships to chordae, papillary muscles and ventricular walls. Normal MV function relies on the integrated role of all these various components. There are numerous etiologies of MV disease and detailed preoperative comprehensive evaluation of the MV apparatus is vital not only to determine the feasibility for MV reconstruction but also to optimize the surgical technique for successful MV repair. Surgical repair rather than replacement of the MV assumes particular importance in growing patients because insertion of a prosthetic valve commits the patient to serial replacement to accommodate growth.
Figure 5. 3D-rendered view that demonstrates the circumferential extent of the subaortic membrane (asterisk) as this is viewed through the aortic valve. AoV: Aortic valve; LA: Left atrium; RA: Right atrium.
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Using real-time 3D (RT3D) TEE, a comprehensive assessment of the MV involves the acquisition of the so-called en face view, which mirrors the view that the surgeons will have when looking from the left atrium to MV. In addition, using the full volume data detailed characterization of the interrelationship of the MV to adjacent structures can be established from the ventricular perspective. In the presence of mitral regurgitation, the mechanisms of mitral regurgitation are important parameters to consider before surgical repair. Several studies have shown that 3D echocardiography is a more sensitive modality compared with 2D in identifying the area of pathology (i.e., abnormal MV leaflets and commissural defects, among others) in the MV apparatus but also to decipher complex geometric relationships (distortion and folding of the MV annulus), which can account for annular dilatation and be involved in the mechanisms of mitral regurgitation [13–16] . It can also provide complementary and additional information for localization of prolapsed scallops and MV clefts (Figure 2 & Supplementary Video 2B) . Studies using 3D TEE and color Doppler demonstrated the superiority of this modality for accurate assessment of the mechanisms of mitral regurgitation and provided additional information to the surgeons when MV repair was to be attempted [16] . The tricuspid valve can also be imaged effectively using 3D echocardiography. Projections can be obtained in an analogous manner to MV to localize areas of regurgitation and visualize morphological abnormalities of the valve leaflets. In more complex cases such as Ebstein’s anomaly, 3D echocardiography can complement cross-sectional imaging and demonstrate the abnormal rotation of the axis of the tricuspid valve, the anatomy of the chordal attachments and their extension to the right ventricular outflow tract thus providing detailed morphological information to the surgeons [17–21] . En face view of the valve and areas of ineffective coaptation can also be seen using 3D echocardiography [20] . This information will assist the surgeons in accurate evaluation of the size of the functional right ventricle and to estimate severity of tricuspid regurgitation. The anatomy of the tricuspid valve leaflets can be visualized including deficiency of leaflets. Importantly, redundant valve tissue can also be identified, which is central to techniques to recreate a more competent tricuspid valve orifice when repair of the tricuspid valve is to be undertaken.
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Figure 6. Straddling atrioventricular valves. 3D-rendered views that demonstrate: (A) straddling mitral valve chords to the right ventricular wall; and (B) straddling tricuspid valve chords to the left heart. Closure of the ventricular septal defect in these cases is challenging, as closure of the ventricular septal defect may compromise the function of the atrioventricular valves. Inf: Inferior; L: Left; LA: Left atrium; LV: Left ventricle; MV: Mitral valve; R: Right; RA: Right atrium; RV: Right ventricle; Sup: Superior; TV: Tricuspid valve.
As far as semilunar valves are concerned, RT3D echocardiography can be used to assist in presurgical planning or for intraoperative guidance and there are reports that this modality can be very useful in identifying aortic valve injury, which can involve leaflet tear or perforation and quantify the degree of aortic valve regurgitation (Figure 3 & Supplementary Videos 3A & 3B) [22–24] . 3D TEE can provide an en face view of the aortic valve to allow assessment of the coaptation lines and leaflet integrity with no out-of-plane motion, in contrast to 2D echocardiography. The presence of aortic cusp prolapse and its dynamic nature during the cardiac cycle can also be demonstrated using a 3D-rendered technique (Figure 4 & Supplementary Video 4) . Use of the multiplanar reformatted technique permits alignment to the prolapsing cusp in multiple planes to confirm which cusp is prolapsing and additional information on the alignment of aortic cusps to each other. This information is important when repair or resuspension of the aortic valve leaflet is to be undertaken to prevent long term progression of aortic valve regurgitation. ●●Outflow obstruction & subaortic
membrane
There are several mechanisms of left ventricular outflow obstruction, which can include
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the presence of fibromuscular stenosis, accessory left atrioventricular (AV) valve tissue, papillary muscles, accessory chords or diffuse hypoplasia resulting in tunnel stenosis [25,26] . Characterization of the mechanism of left ventricular outflow obstruction is important before embarking onto surgery as surgical resection is commonly performed through the aortic valve with restricted views [27] . 3D echocardiography can provide complementary information to cross-sectional imaging in such cases by providing detailed morphological information and intracardiac views from the ventricular side. Using this approach, accessory chords or papillary muscles and their attachments can be visualized and decision can be made on whether these represent part of the primary or secondary support apparatus of the valve leaflets and as to whether their resection will compromise valve function. This information can be very important for the surgeons as their field of view through the aortic valve is often limited and extensive resection may lead to significant aortic valve regurgitation postoperatively. Detailed characterization of the circumferential extent and severity of subaortic membrane has also been described with 3D by using a projection through the aortic valve combined with view from the ventricle and view of the long axis of the left
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Review Charakida, Pushparajah & Simpson ventricle (Figure 5 & Supplementary Video 5) [28,29] . Accurate analysis of the effective orifice area and measurement of the distance between the membrane and aortic valve leaflets will inform the surgeons on whether resection of the subaortic membrane is likely to compromise the aortic valve function. ●●Ventricular septal defects
Some types of VSDs, for example, apical muscular or inferior inlet or outlet defects might be difficult for the surgeon to repair as their view is often limited through the tricuspid valve, the defect can be quite distant from the tricuspid valve and in some cases the VSD position can be hidden in heavy right ventricular trabeculations [30] . In these cases, 3D echocardiography can provide key information in presurgical planning with regards to size, shape of the defect and accurate location [31] . The distance of the VSD from important landmarks such as tricuspid, pulmonary valve and moderator band can be accurately calculated. This information will assist in decision-making on whether catheter closure of the defect is likely to be successful or whether surgical intervention is the only approach forward [32] .
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In certain cases, it might be decided that the VSD is not amenable to immediate intervention and palliative pulmonary artery banding should be undertaken to improve clinical symptoms. In the presence of multiple defects, it can also be quite challenging using cross-sectional imaging and Doppler measurements to decide about the necessity to embark on complex surgery to close the various defects [33–36] . Using 3D echocardiography and different projections accurate sizing of the various defects can be performed to facilitate presurgical planning [37] . In some complicated cases, there can be straddling of the tricuspid or MV over the VSD (Figure 6 & Supplementary Video 6A & B) . VSD closure, in these circumstances, is complex, and surgeons prefer a full understanding of the anatomy of the defect and its relationship preoperatively [38] . Using 3D echocardiography, straddling chords can be demonstrated along their length from the point of origin on the atrioventricular valve to the point of insertion into the contralateral ventricle and this information can facilitate decision-making on whether closure of the VSD is likely to compromise the function of the straddling valve.
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Figure 7. 3D echocardiography and atrioventricular septal defect. (A) View of the left atrioventricular valve in a patient who has undergone previous atrioventricular septal defect repair. The superior and inferior bridging leaflets have been sutured to form a neoaortic leaflet. The mural and neoaortic leaflets show an identifiable zone of failure of coaptation. (B) This projection illustrates how the neoaortic leaflet and the mural leaflet fail to coapt with the neoaortic leaflet showing a degree of prolapse into the left atrium. Using the color flow Doppler the region of atrioventricular valve regurgitation is localized. IBL: Inferior bridging leaflet; Inf: Inferior; L: Left; LA: Left atrium; LV: Left ventricle; R: Right; SBL: Superior bridging leaflet; Sup: Superior.
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3D echocardiography in congenital heart disease
A
Review
B
Figure 8. 3D echocardiography and double outlet right ventricle. (A) Rendered 3D echocardiographic projection from the apex of the heart demonstrating the relationship of the mitral valve, tricuspid valve, aorta and pulmonary artery to each other. An asterisk (*) shows the interventricular communication. This view is not achievable by cross-sectional echocardiography because of the lack of depth of field. (B) Rendered 3D echocardiographic projection of double outlet right ventricle. This projection is achieved by cropping away the free wall of the right ventricle so that the ventricular septum, interventricular communication and the great arteries are visualized from the right ventricular aspect. Both the apical and right ventricle projections assist in determining the optimal means of surgical repair. Inf: Inferior; L: Left; MV: Mitral valve; PA: Pulmonary artery; R: Right; RA: Right atrium; RV: Right ventricle; Sup: Superior; TV: Tricuspid valve. ●●Complex congenital heart defects
Recent innovations in the field of RT3D have allowed this modality to offer unique and clinically useful information in the evaluation of patients with complex congenital heart disease such as AVSD and double outlet right ventricle. Nearly all of patients with an AVSD will require surgical intervention at some stage in their life. The primary surgical repair consists of closure of interatrial and interventricular communication and repair of the atrioventricular valves. Accurate assessment of the morphology and its anatomic inter-relationships is very important to determine whether or not the atrioventricular valve is amenable to surgical repair and whether this can be divided into two separate AV valves with adequate function. In the decision-making process 3D echocardiography has proven invaluable for the qualitative and quantitative evaluation of AV function but also for the assessment of atrial and ventricular communications [39] . Hlavacek et al. showed that gated 3D views could be cropped to obtain en face views of the atrial and ventricular septa [40] . These views provide a clear understanding of the relationships of the bridging leaflets to
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the septal structures and how these relationships determine the level of shunting (atrial, ventricular or both) (Figure 7 & Supplementary Video 7A & B) . Following repair, although the surgeon has the opportunity to immediately inspect the AV valves and test their competency with saline, this technique is nonphysiologic and might not reflect their competence in dynamic moving heart. Following AVSD repair, the geometry of the left AV valve and its supporting apparatus is altered and as a result in some cases progressive left AV valve regurgitation may also develop. Using crosssectional imaging, it is often difficult to assess the number of jets as many may run along a commissure and can appear as multiple jets. It can also be difficult to delineate the origin of the regurgitant jet and relate it to valve pathology. Takahashi et al. demonstrated, by using 3D echocardiography, that the severity of left AV valve regurgitation following AVSD repair is linked to the dilatation of the valve annulus, leaflet prolapse and to the presence of an acute angle between the anterolateral papillary muscle and the left AV valve annulus [41] . Shortened chordae can be seen by 3D and their impact on leaflet mobility
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Review Charakida, Pushparajah & Simpson can be estimated. The sites of poor coaptation and specific commissural mismatch as mechanism of left AV valve regurgitation can be better appreciated using 3D echocardiography [42] . The complete line of apposition between the superior and inferior bridging leaflets can also be assessed. Reoperation for left AV valve regurgitation is technically demanding and can involve cleft closure, annular reduction, commissurotomy, patch augmentation of deficient leaflet tissue. Accurate characterization of the pathophysiology of the left AV valve regurgitation would therefore be necessary for the surgeons before embarking into a repeat surgery to repair or replace the regurgitant valve [43,44] . Another important association that has significant surgical implications is the presence of a double orifice left AV valve [45,46] . This information can be accurately obtained by 3D echocardiography whereas identification of this pathology with cross-sectional imaging has been disappointing. Hoohenkerk et al. have documented that in the presence of double orifice left AV valve, optimal surgical results are obtained by preserving the tissue bridge and tension apparatus and repairing the AV valve as a three-leaflet valve [47] . In other cases of complex congenital heart disease lesions, 3D echocardiography can also prove invaluable before planning a surgical repair. Double outlet right ventricle, transposition of the great arteries with ventricular septal defect and other cases with discordant atrioventricular and ventriculo-arterial connections are characteristic examples [48] . Understanding the complex relationships between the great arteries, the ventricular septal defect and the atrioventricular and semilunar valves is vital before embarking into surgical repair (Figure 8 & Supplementary Video 8A & B) . Depending on the underlying morphology, the surgical approach might involve an arterial switch operation, baffling of the left ventricular outflow to the ascending aorta or a single ventricle repair when septation cannot be achieved [49] . In such cases, 3D echocardiography can produce unique projections, which can include all of the components of the planned surgical repair with added depth thus allowing accurate presurgical planning and facilitating surgical decision-making [9] . Conclusion A number of studies have demonstrated that 3D echocardiography can provide incremental information to cross sectional imaging and enhance morphological information for complex
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congenital heart disease lesions. Intracardiac connections and relationships can be delineated and anatomy can be projected in various ways to guide surgical procedures. The added depth of field of view can often allow demonstration of all the components of the planned surgical repair in one projection. Therefore, discussions and decisions about surgical procedures can be made using ‘real’ images rather than running the risk of misinterpretation by individually mentally reconstructed projections. Nevertheless, despite its increasing use the technique remains a complementary method to cross-sectional imaging and further technological advances are required to resolve some of its technical limitations and allow its integration in routine clinical practice. Future perspective Developments in cardiac surgery mean that patients with increasingly complex cardiac lesions may be judged candidates for surgical repair. This emphasizes the need for detailed preoperative imaging investigation to provide all necessary information for an effective surgical repair. Multimodality imaging is commonly employed to take advantage of the strengths of different techniques including 3D echocardiography, MRI and CT. However, 3D echocardiography has the advantage of being portable at the point of care, noninvasive and no other current technique can provide the depth of field and temporal resolution to assess heart valves. Additionally, 3D echocardiography is cheap compared with MRI and CT. Future developments in 3D echocardiographic techniques will address some current limitations such as spatial and temporal resolution. Postprocessing algorithms that are currently limited to a research level will allow for fusion of multiple images into one to increase the field of view and eliminate acoustic shadowing [50] . This includes not just B-mode image data, but also integration of color Doppler data, which provides a noninvasive method of flow visualization and quantification [51] . These will enhance the scope of 3D color Doppler, which is constrained by a limited field of view, low temporal resolution and stitching artifact from multiple interleaved acquisitions. Emerging technologies to enhance frame rates to several hundred frames per second has already been described in a research setting [52] . This will overcome visualization of rapidly moving structures such as atrioventricular and semilunar
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3D echocardiography in congenital heart disease valves. The availability of powerful post processing hardware and software is such that the long postprocessing times, which have hindered the clinical application of these technologies, will also decrease significantly. Another significant advantage of 3D echocardiography is the potential for automation with the ability to acquire real-time 3D color Doppler data within a single cardiac cycle [53] . This will see integration of automated systems to allow quick image acquisition and postprocessing with minimal inter-user variability available for bedside echocardiographic assessment. The developments in matrix array probes and image processing algorithms will lead to further miniaturization of probes, which is especially relevant in pediatric patients. 3D TEE probes are only available for adults, but it is realistic to expect that these will be small enough for pediatric use in the coming years. The 3D display for preoperative planning will also improve with increased display options including holographic projections [54] . Additionally, the improved displays will be able to match the higher frame rates of the acquired images. 3D echocardiography must also be capable of integration with other imaging modalities such as fluoroscopy, CT or MRI. The translation of integration
Review
of MRI, CT and fluoroscopy with 3D echocardiography from a research technique to a more standard commercially available technology can be expected in the near future. Although these developments are heavily reliant on industry, the drive for industry participation must be led by clinicians working with physicists and engineers with a close contact to a clinical environment to allow rapid testing and validation of prototypes in a clinical environment with the aim of providing clinical benefit. Imaging vendors will have to match the clinical demand for fast, high-quality imaging with minimal postprocessing time at the bedside and in the operating theater. Over the next decade, it is likely that 3D echocardiography will become firmly integrated into surgical planning and perioperative imaging. As the technology becomes more commonplace, adherence to international guidelines and recommendations formed of expert consensus will lead to a uniform approach to image display, which will allow rapid understanding of images being displayed by both the imaging and surgical teams. As patients with congenital heart disease reach adulthood, long-term complications will inevitably become apparent and reconstructive surgeries in these cases can also be challenging. Optimal results will heavily rely on accurate preoperative
Executive summary 3D acquisition ●●
A number of 3D echocardiographic modalities (full-volume acquisition, live 3D echocardiographic imaging) are available and can provide complementary morphological and functional information for simple and complex congenital heart disease lesions to tailor surgical needs.
Valvular heart disease ●●
The mitral valve has a complex configuration and it is ideally suited for 3D echocardiography. Preoperative
reconstruction of the mitral valve apparatus can be achieved, inter-relationships can be delineated and presurgical planning can be optimized to maximize opportunities for successful mitral valve repair. A similar approach can be extended to the tricuspid valve and other atrioventricular valves. Outflow obstruction ●●
Important information about the type and degree of outflow obstruction will inform the surgeons on whether extensive resection is likely to compromise the integrity of the valve apparatus.
Ventricular septal defects ●●
The size, shape and location of ventricular septal defects can be accurately assessed by 3D echocardiography. The
presence of straddling atrioventricular valves and their connections can be accurately assessed before embarking in complex surgical procedures. Complex congenital heart disease lesions ●●
Surgical strategy and repair can be facilitated by information obtained using 3D echocardiography for complex cardiac lesions such as atrioventricular septal defects and double outlet right ventricle.
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Review Charakida, Pushparajah & Simpson imaging and planning. Understanding of the anatomical substrate using 3D echocardiography would be necessary together with other imaging modalities and real-time 3D echocardiographic guidance is likely to be routine clinical practice. Acknowledgements The authors would like to thank Heartworks for the system that they used to generate the anatomical images presented in this paper.
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