Atrioventricular septal defect: An extended approach to prenatal sonographic imaging of the atrioventricular valves

An atrioventricular septal defect (AVSD) is diagnosed with prenatal sonography using the 4‐chamber view (4CV) of the fetal heart. Prenatal 2D sonographic imaging of normal and AVSD short axis (SAX) atrioventricular (AV) valve views have not been well described. The aim is to describe the 2D sonographic 4‐chamber and SAX view of the AV valves when an AVSD is present compared to normal AV valves. The 4CV AVSD heart demonstrates no offset of AV valves due to the abnormal valve structure. Complete and intermediate AVSD has a septum primum defect and inlet ventricular septal defect (VSD). The partial AVSDs have either a septum primum defect or just an inlet VSD with an intact primum septum. The SAX view of AVSD demonstrates the common AV junction and the bridging leaflets. In ventricular diastole valves have a “figure 8” and “dumbbell” shape in partial and complete AVSD, respectively. These appearances are not seen in the normal heart in SAX as both tricuspid and mitral valve are separate valves. The SAX view can be obtained by locating a sagittal aortic arch view and then scanning slightly towards the left side of the fetus, near the base of the heart and the AV valves. An in‐depth interrogation of the abnormal fetal heart is obtained without specialised 4D capable ultrasound machines providing information to assist in counselling during the pregnancy and for postnatal surgical planning. Future research to assess the feasibility of incorporating the SAX view into routine practice and by general sonographers is suggested.


| INTRODUCTION
The term atrioventricular septal defect (AVSD) covers a collection of heart defects of the atrial and ventricular septum and atrioventricular (AV) junction and valves.The postnatal incidence of AVSD is approximately 4-5.3 per 10,000 births. 1,2An AVSD can occur as an isolated defect, as part of a chromosomal anomaly particularly trisomy 21, heterotaxia syndrome or with other anomalies. 3Prenatal detection of an AVSD has improved in recent years especially in populations that have introduced routine combined first trimester screening for chromosome anomalies and a morphology scan. 4There are different types of AVSD, knowledge of the types and their prenatal ultrasound appearance will help identify an AVSD. 1,5cording to the International Paediatric and Congenital Cardiac Code (IPCCC) an AVSD can be subdivided into four types, that is, (1) a complete AVSD, (2) a partial AVSD, (3) an intermediate (or transitional) AVSD and (4) an unbalanced AVSD. 1,5Unbalanced AVSDs will not be discussed in this paper.All AVSDs have abnormal AV valves with an unwedged aorta.An unwedged aorta occurs when the aorta is situated anterior to the AV valve/s rather than wedged between the valves. 6igure 1B,C).The AVSD valve can have either five leaflets observed in a complete AVSD, or a three-leaflet left AV valve (LAVV) and fourleaflet right AV valve (RAVV) in both the partial and intermediate forms.
The AV valves in AVSD are not offset and are seen at the same level either bridging the interventricular septum (IVS) or attaching to the IVS or atrial septum. 1,5(Figure 1).Table 1 describes in more detail the distinct types of AVSD compared to the normal heart.
The prenatal sonographic appearances of a complete AVSD have been well described.Diagnosis is made with the 4CV demonstrating an absent septum primum, large inlet VSD, and no offset of the fiveleaflet AV valve at the level of the crux. 7,8More difficult to differentiate and diagnose prenatally are the intermediate AVSD and the two partial forms of AVSD.The intermediate AVSD, has a septum primum defect and a small restrictive inlet VSD with separate abnormal LAVV and RAVV 1,9 and to the inexperienced sonographer may appear similar to a partial AVSD or a normal heart.The first partial AVSD type is where there is no VSD (no ventricular shunt) with a septum primum defect.The second demonstrates no atrial septal primum defect (no atrial level shunt) with an inlet VSD. 1,10(Figure 2).or partial AVSD is present.2][13] The normal SAX AV

| SONOGRAPHIC IMAGING OF THE FETAL HEART
According to recent guidelines, the fetal morphology scan should include a thorough interrogation of the fetal heart. 14Assessment of the AV valves are incorporated into routine and tertiary level scanning using the 4CV.The following sections will describe the sonographic techniques and appearances of the normal and AVSD heart in the 4CV and additionally the SAX view of the AV valves.

| Normal 4-chamber heart
The normal 4CV demonstrates AV valves that are offset with the TV set more apically.There is an intact interventricular septum and an atrial septum primum is visible posterior to the crux between the atria.
The offset of the AV valves is best appreciated with an apical 4CV (Figure 3).

| Normal short axis view of the AV valves
The SAX view allows imaging of the ventricles, IVS and AV valves in imaged from the fetal anterior chest wall. 8The MV has a "fish mouth" or "smiley face" appearance, is visualised distal to the IVS and can be seen opening and closing in real time.(Figure 4; Video 2).The TV is not visualised at this level due to its apical displacement.

| Abnormal 4-chamber view
The 4CV of the AVSD heart demonstrates a linear insertion of the AV valves (no offset).In a complete AVSD there is an inlet VSD and a septum primum defect and one valvular orifice.(Figure 5; Video 3).An intermediate AVSD demonstrates similar valve and septal defect appearances except there are two valvular orifices present and the VSD is small (Figure 1; Table 1).The partial AVSD, will demonstrate a septum primum defect but no VSD visible, (Figure 6; Video 4) or an inlet VSD with no atrial septum primum defect (Figure 2).An inlet VSD is located inferior to the RAVV and is visualised by scanning inferiorly or towards the fetal diaphragm from the standard apical 4CV.an atrial level shunt.The importance of recognising the linear AV valves in the 4CV and the "figure 8" and "dumbbell" SAX views when AVSD is present and not relying just on identifying a septum primum defect or VSD, is demonstrated from these cases.
While the SAX view has been described postnatally 2 and prenatally using 4D volume rendering [11][12][13] we believe this is the first report to describe the 2D SAX AVSD prenatal sonographic appearances.
While the diagnosis of AVSD has traditionally been made by the 4CV, the SAX AV valve view which directly assesses the abnormal AV valves will improve the assessment, especially in the case of the more subtle partial or intermediate AVSD.Imaging the SAX view requires a degree of skill, however, if a sonographer can obtain a sagittal aortic arch view, then the SAX view is well within their skill set.We recommend magnifying the sonographic image of the AV valves to enable visualisation of the abnormal valves and storing a cine clip for later review as needed.Although fetal heart screening recommendations only specify five axial views of the fetal heart, 14 many sonographers can and do scan beyond this.Indeed, sonographers scanning at a tertiary level routinely scan the fetal heart using extended views.
The diagnosis of a complete AVSD in the 4CV has been well described, however partial AVSD may be more difficult to diagnose, 9 especially for the sonographer performing routine screening with less exposure to abnormal hearts.Additionally, general sonographers often lack feedback on the final diagnosis of a heart anomaly which may valves, not variations of normal. 17In the complete AVSD, the AV valves have superior and inferior bridging leaflets seen with the linear (bridging) insertion of the AV valves in the 4CV and SAX view, a left mural valve, and a right antero-superior and right inferior valves, five leaflets in total. 10(Figures 1 and 8).In the partial and intermediate forms of AVSD the terminology used is a three leaflet LAVV and four leaflet RAVV. 1 (Figures 1 and 7).With a partial AVSD the bridging valves still demonstrate no offset at the heart crux but are attached to either the atrial or ventricular septum meaning there is only an atrial or ventricular shunt, not an atrioventricular shunt.The current definition of AVSD would support a sonographic view that enables better visualisation and interrogation of the AV valves in these more difficult cases.

| STRENGTHS/LIMITATIONS
This paper describes an additional view of the fetal heart that is easily obtained in routine fetal heart examinations.When imaged routinely this view will allow sonographers to recognise abnormal AV valves and increase the detection of fetal heart abnormalities.There is a clear description of the normal and abnormal appearances of the valves with a table, images, live videos, and line drawings to help recognise the relevant anatomy.
Many of the images used to illustrate the heart in this paper were at a gestation of 27+ weeks, as this was ideal for demonstrating the Extended views will improve evaluation of the fetal AV valves enabling greater confidence in diagnosis, especially if an intermediate F I G U R E 1 En face representation of relationship of great arteries and atrioventricular valves with (A) normal atrioventricular valves (B) complete atrioventricular septal defect and (C) partial and intermediate atrioventricular septal defect.Ao, aorta; IBL, inferior bridging leaflet; IVS, interventricular septum; LAVV, left atrioventricular valve; LML, left mural leaflet; PA, pulmonary artery; RAL, right anterior leaflet; RAVV, right atrioventricular valve; RPL, right posterior leaflet; SBL, superior bridging leaflet.T A B L E 1 Comparison of normal heart with spectrum of atrioventricular septal defects.
valves have proved difficult to image and interpret using 2D ultrasound especially as the tricuspid valve (TV) sits more apically compared to the mitral valve (MV).As the AV valves are at the same level when an AVSD is present, 2D assessment of the valves is feasible with this method more readily available in non-specialist centres.The aim of this work is to describe the 2D sonographic 4CV and SAX view features of the AV valves when an AVSD is present compared to normal AV valves to increase prenatal detection of AVSD especially in the more difficult forms where there is no ASD or VSD present.
an additional dimension, obtained by rotating the transducer 90 to the 4CV.In this view, the AV valves can be visualised en face.The SAX view can be obtained in 2D by obtaining a sagittal aortic arch view then sliding or fanning the transducer slightly towards the left side of the fetus.Alternatively, should an apical SAX view of the ventricles be visualised then a small sliding or fanning movement to the right of the fetus will enable visualisation towards the base of F I G U R E 2 Representation of atrioventricular septal defects (AVSD) demonstrating attachment of bridging leaflets and level of shunting (arrows).Note complete and intermediate AVSD have atrial and ventricular shunts.Complete AVSD has one valvular orifice.An intermediate AVSD has two valvular orifices and a restrictive VSD which may make it more difficult to image prenatally.Partial AVSD have two valvular orifices and either an atrial or ventricular shunt.AVSD, atrioventricular septal defect; LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle.F I G U R E 3 Normal 4-chamber heart at 27 + 4 weeks gestation demonstrating offset of the tricuspid valves which is set more apically than the mitral valve.LV, left ventricle; MV, mitral valve; RV, right ventricle; TV, tricuspid valve.the heart and AV valves.(Video 1).When the AV valves are imaged in the SAX view, typically, only the MV is seen with the left and right ventricle separated by the IVS.The inlet and muscular components of the IVS can be seen, and an optimal zero degrees colour Doppler angle is obtained for interrogation of the IVS especially if the heart is

4. 2 |
Abnormal short axis view of the AV valvesThe AVSD SAX view of the valves will demonstrate the common AV junction (in partial AVSD) or common AV valves (in complete AVSD) more clearly.A partial AVSD (septum primum defect without a VSD component), will show a "figure8" appearance when the AV valves are fully opened in ventricular diastole, with the LAVV and RAVV sitting closer to and at the same level as the IVS compared to a normal heart.The centre of the "figure 8" abuts the IVS.(Figure 7A,B; Video 5).If a complete AVSD is present the inlet VSD can be seen in V I D E O 1 Video at 27 + 4 weeks gestation demonstrating short axis view in a normal heart obtained by scanning from the apex of the heart where the short axis view of the ventricles are demonstrated on the left side of the fetus, to the right sided sagittal aortic arch.Note this is an alternative method to the technique described in the text where the sagittal heart has been scanned from right to left.Video content can be viewed at https:// onlinelibrary.wiley.com/doi/10.1002/sono.12370F I G U R E 4 Sonographic image at 27 + 4 weeks gestation (A) and drawing (B) of short axis view at base of normal heart demonstrating "smiley face" mitral valve.Note distance of mitral valve from the interventricular septum (double arrow).Due to the apical offset a normal tricuspid valve is usually not seen at this level.IVS, interventricular septum; LV, left ventricle; MV, mitral valve; RV, right ventricle.the SAX view (Video 6) and during diastole with the AV valves fully open, a "dumbbell" appearance of the AV valves is demonstrated.(Figure 8A,B).If there is an atrial shunt only with a partial AVSD then the IVS appears intact at this level with the bridging valves attaching to the IVS.(Video 5).5 | DISCUSSIONThis work describes the 4CV and SAX view of the AV valves for the diagnosis of partial and complete AVSD, this is important because all AVSDs have abnormal AV valves.A complete AVSD has a large nonrestrictive inlet VSD resulting in bidirectional ventricular shunting in the fetus,15 one valvular orifice compared with the intermediate and partial forms which have two valvular orifices and separate ventricular inflows.1 The complete AVSD demonstrates a common pathway of flow with colour Doppler, from the atria to the ventricles separating at the IVS.11Absolute identification of the intermediate type of AVSD may be difficult to achieve prenatally due to the separate abnormal AV valves and potentially very small inlet VSD.This restrictive inlet VSD results in similar pressure gradients between the ventricles with little left to right or no flow across the VSD.This absence of flow across the VSD makes the prenatal diagnosis of intermediate AVSD more difficult.16The separation of the AV valves can be difficult to appreciate on prenatal sonography and the appearances of intermediate AVSD can overlap with a complete AVSD and a partial AVSD with V I D E O 2 Video at 24 + 2 demonstrating the mitral valve (arrow) short axis view in a normal heart.Video content can be viewed at https://onlinelibrary.wiley.com/doi/10.1002/sono.12370F I G U R E 5 4-chamber view of complete AVSD at 27 + 1 weeks gestation.Note septum primum defect (arrow head), no offset of atrioventricular valves (arrow), and inlet ventricular septal defect (dashed arrow).V I D E O 3 Video demonstrating 4-chamber view of complete atrioventricular septal defect at 27 + 1 weeks gestation.Video content can be viewed at https://onlinelibrary.wiley.com/doi/10.1002/sono.12370F I G U R E 6 4-chamber view of partial AVSD at 27 + 6 weeks gestation demonstrating no offset of AV valves (arrow).There is attachment of the AV bridging leaflets to the interventricular septum with an atrial level shunt (septum primum defect) (arrow head).
limit their learning.Incorporating the SAX view where abnormal valves can be visualised may help in the diagnosis of partial and intermediate AVSD.It will also help in counselling during pregnancy and future surgical planning for the baby. 2 Recognition of abnormal AV valves should prompt a fetal cardiologist review.Correct nomenclature should be noted, it is incorrect to label the AVSD AV valves as a bicuspid valve, MV or TV or state there is a "cleft in the MV." 2 This is because the LAVV and RAVV are abnormal V I D E O 4 Video demonstrating 2D and colour Doppler of 4-chamber view of partial atrioventricular septal defect with septum primum defect at 27 + 6 weeks gestation.Video content can be viewed at https:// onlinelibrary.wiley.com/doi/10.1002/sono.12370F I G U R E 7 Sonographic image at 27 + 4 weeks gestation (A) and drawing (B) of short axis view at base of heart in partial atrioventricular septal defect (AVSD).Note the atrioventricular valve (AVV) forms a "figure 8" with the left and right sided AVV visible at the same level and sitting close to the interventricular septum.IBL, inferior bridging leaflet; IVS, interventricular septum; LML, left mural leaflet; LV, left ventricle; RAL, right anterior leaflet; RV, right ventricle; RPL, right posterior leaflet; SBL, superior bridging leaflet.

V I D E O 5
Video demonstrating short axis view of partial atrioventricular septal defect valves at 27 + 6 weeks gestation.Video content can be viewed at https://onlinelibrary.wiley.com/doi/10.1002/sono.12370V I D E O 6 Video demonstrating short axis view of complete atrioventricular septal defect valves at 20 + 3 weeks gestation.In this view, the bridging AV valves "dumbbell" shape and inlet VSD (arrow) can be seen.Video content can be viewed at https://onlinelibrary.wiley.com/doi/10.1002/sono.12370F I G U R E 8 Sonographic image at 28 weeks gestation (A) and drawing (B) of short axis view at base of heart in complete atrioventricular septal defect (AVSD).Note the atrioventricular valve (AVV) forms a "dumbbell" shape with the left and right sided AVV visible at the same level in diastole.IBL, inferior bridging leaflet; IVS, interventricular septum; LML, left mural leaflet; LV, left ventricle; RAL, right anterior leaflet; RV, right ventricle; RPL, right posterior leaflet; SBL, superior bridging leaflet.AV valves, however this does not mean that abnormal valves cannot be recognised in the SAX view at earlier gestations as demonstrated by Video 6.We acknowledge that the AVSD images used in this article were obtained by experienced operators.Future research should evaluate less experienced sonographers' ability to obtain the SAX view of the AV valves and if obtaining this view improves the identification of an AVSD.