Editorial. The four-chamber view: four reasons why it seems to fail in screening for cardiac abnormalities and suggestions to improve detection rate

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1 Ultrasound Obstet Gynecol 2003; 22: 3 10 Published online in Wiley InterScience ( DOI: /uog.187 Editorial The four-chamber view: four reasons why it seems to fail in screening for cardiac abnormalities and suggestions to improve detection rate R. CHAOUI Unit of Prenatal Diagnosis and Therapy, Department of Obstetrics and Gynecology, Charité Hospital, Humboldt University Berlin, Schumann Str. 20/21, D-10098, Berlin, Germany ( rabih.chaoui@charite.de) INTRODUCTION Congenital heart defects (CHDs) have a multifactorial etiology and therefore their prenatal detection cannot be achieved solely by concentrating on the high-risk population defined by parental medical history. Screening ultrasound is usually performed in the second trimester and is still the best means of detecting cardiac defects. Signs of cardiac disease are often subtle, necessitating careful targeted examination. In the 1980s, the fourchamber view was proposed as the most important plane for screening, allowing a greater detection rate for anomalies. Recently, however, incorporation of views of the great vessels has been recommended as part of the routine screening examination. Many studies in the last 10 years have emphasized the importance of cardiac screening, but they have achieved widely divergent results, with reported detection rates varying from 5% to 92% (Table 1). However, it should be noted that these studies employed different approaches, which are summarized in Table 2, and are therefore not directly comparable. The anticipated potential in the 1980s of the fourchamber view to detect most or at least the severe cardiac anomalies was fulfilled in very few areas and centers, and widespread improvements in detection rates were not achieved. In my opinion, there are four possible reasons why the four-chamber view appears to fail. This editorial analyses these four reasons and attempts to suggest solutions to increase detection rates. REASON 1: INADEQUATE EXAMINATION Inadequate examination is likely to be the most common cause of heart defects being overlooked in the four-chamber view. The inadequately examined heart is frequently reported as normal, or as a limited examination due to fetal position, when the heart is examined at an inappropriate angle. The heart may not be examined in any greater detail than to observe cardiac rhythm. As the remainder of the fetus is screened properly (for example, with careful examination to exclude markers such as a banana sign for neural tube defect, chromosomal anomalies and complex malformations), the institution may have good detection rates for these anomalies, but may be less successful in the detection of fetal cardiac anomalies. Two major problems are commonly encountered: firstly, the examiner may not be able to obtain an adequate four-chamber view with different fetal positions and, secondly, the image is not optimized for the analysis of the heart. Other technical aspects also contribute to unsatisfactory visualization of the heart, even at specialized centers, and include: gestational age (20 23 weeks is preferable to weeks 1 ), transducer frequency (5 MHz is better than 3.5 MHz 1 ) and objective fetal and maternal factors. DeVore et al. 2 analyzed factors influencing imaging during the second trimester of pregnancy and found that even in expert hands the heart could not be properly imaged in 9% of cases due to maternal body habitus and previous abdominal surgery, and early gestational age, but very rarely because of fetal position. An additional reason for inadequate examination is lack of time. In some units the whole fetal examination usually has to be achieved within a short time period (e.g min) due to the large number of patients being screened. Under these circumstances there may be no time Copyright 2003 ISUOG. Published by John Wiley & Sons, Ltd. E D ITORIAL

2 4 Chaoui Table 1 Summary of some studies with different detection rates of congenital heart defects CHD (n) Detection (%) Risk population and heart examination Copel et al. (1987) High risk, 4 CV Bromley et al. (1992) vs. 83 Mixed risk, 4CV vs. extended cardiac exam Vergani et al. (1992) Mixed risk, 4CV Sharland and Allan (1992) Mixed risk, 4CV, detectable in 4CV Achiron et al. (1992) vs. 78 Low risk, 4CV vs. extended cardiac exam Levi et al. (1995) Screening, not specified Ott (1995) vs. 62 Mixed risk, 4CV and left ventricular outflow, low risk vs. high risk Montana et al. (1996) Atlanta area registry, not specified Stoll et al. (1998) Alsace area registry, 4CV Buskens et al. (1996) Dutch study, low risk, 4CV Tegnander et al. (1995) Low risk, 4CV, critical CHDs Rustico et al. (1995) vs. 61 Low risk, extended echo, all vs. major CHDs Todros et al. (1997) vs. 35 Low risk, 4CV, all vs. detectable in 4CV Stumpflen et al. (1996) Mixed risk, extended echo at one center Yagel et al. (1997) Mixed risk, extended echo at three centers 4CV, four-chamber view; CHD, congenital heart defect. Table 2 Comparison of approaches used in different studies (Table 1) which affect the accuracy of fetal echocardiography High-risk vs. low-risk populations with different prevalences of CHD A few experienced examiners vs. many examiners with different levels of experience Differences in and accuracy of postnatal follow-up Examination throughout pregnancy vs. examination at a specified time (e.g. < 15 weeks or weeks) Consideration of all cardiac defects vs. only severe CHDs detectable on the four-chamber view Examination of the heart not specified vs. examination of the four-chamber view vs. complete cardiac examination including assessment of the great vessels CHD, congenital heart defect. to wait for the fetus to change its position or to change the different presets of the machine or use other transducers. required to submit a logbook of 100 images documenting appropriate cardiac examination. The introduction of a routine heart measurement (e.g. heart width or ventricular proportions) could be another approach to oblige the examiner to document the plane adequately during every examination. Appropriate teaching followed by quality control could be expected to lead to appropriate examination of the heart routinely. To improve visualization, the heart should ideally be examined between 20 and 22 weeks gestation. A study from the Netherlands showed that integration of the four-chamber view into the standard examination at 15 centers achieved a detection rate for heart defects of only 4.5%: 44 heart anomalies were present within the group of 6922 fetuses examined, but only two were detected prenatally 5. In comparison, Sharland and Allan 6 have demonstrated that direct teaching can improve Suggestions for a solution Optimal analysis of the heart may be achieved by magnification of the image, using the zoom function (Figure 1), so that the heart fills a third to half of the screen, and by the use of the cine-loop to assess different phases of the cardiac cycle 3. At institutions where regular problems with visualization of the heart arise, internal quality control may be useful. The Fetal Medicine Foundation has successfully demonstrated reproducible measurements in the range of a few millimeters in the assessment of nuchal translucency 4.However,nosuch quality control exists for the examination of the fetal heart at this stage. Practical teaching with a handson approach for sonographers or perinatologists at specialized centers, followed by submission of a set of 50 images of a four-chamber view, for example, may lead to improvements in image quality. In Germany, in order to gain the qualification required to perform the examination, specialists in fetal echocardiography are Figure 1 Four-chamber view at a non-optimal magnification (a) and after application of zoom function and magnification of the image (b). Details are better visualized on the magnified image.

3 Editorial 5 detection rates. In the south-east Thames region in the UK sonographers were trained not only to obtain but also to interpret the four-chamber view, and were able to detect 69% of all complex heart anomalies detectable in this plane. This study is supported by the results of Tegnander et al. 7, who analyzed detection rates before and after introduction of a teaching program with the aim of obtaining the four-chamber view; detection rates increased from 18 to 39%. Further training in assessment of the great vessels increased detection rates to > 60% (Tegnander, pers. comm.). Recently, Garne et al. 8 analyzed data from 20 participating European centers on the effectiveness of screening ultrasound for CHDs. They found that established ultrasound screening programs increase detection rates. The highest rate was found in Western countries with a screening program (range, 20 48%), while the rate was low in Western countries without screening such as Denmark and the Netherlands (mean, 11%), and in Eastern countries (Croatia, Lithuania, Ukraine) with nonestablished screening policies (mean, 8%). Therefore, appropriate teaching, an established screening program with a checklist, and feedback of screening results seem to be the most effective strategies to increase detection rates of CHDs. The problem of time constraints combined with an inadequate fetal position is still one of the most commonly discussed issues in units performing routine screening ultrasound. In my opinion it is not only a problem of fetal position; it is also related to examiner skill how able she or he is to obtain within a short period of time the defined cross-sectional planes. When problems of lack of time emerge in a unit I suggest the examiner should document the number of cases per day which could not be properly examined and determine whether it is more effective to repeat the examination on a later occasion or to extend the examination time in these patients for an additional 5 10 min. It may be worthwhile reducing the counseling time to bare essentials or optimizing the administrative part of the examination concerned with entering patients data into the computer in order to lengthen the examination time. I have found that if the fetus is stubbornly fixed in a difficult position it helps if I ask the mother to go for a walk and return min later. I can then see her again in the short time slot between two patients and look only at the region not properly visualized previously (face or heart). Usually the fetus has by this time moved into an optimal position. REASON 2: THE FOUR-CHAMBERS ARE VISUALIZED BUT THE ANOMALY IS NOT DETECTED The term four-chamber view may imply that anomalies may only be present when not four chambers are found. For screening, there should be clear cut-offs to define a suspicious heart. Such cut-offs are present for other fetal structures especially when measurements are used (for example, 10 mm for the lateral cerebral ventricle, 10 mm for the cisterna magna, 6 mm to define pyelectasia, a 2-cm amniotic fluid pocket for oligohydramnios, femur length or abdominal circumference < 5th centile, nuchal translucency > 95th centile). Cut-offs for cardiac examination are defined by checklists, but unfortunately they are often only familiar to specialists in fetal echocardiography and are forgotten, or not used, by sonographers during routine examination. This may be the second reason why many heart defects are overlooked despite appropriate scanning techniques. Many examiners may expect severe distortion of the four-chamber anatomy or obvious cardiomegaly to be associated with cardiac anomalies. However, some heart defects detectable in the four-chamber view present with four-chamber anatomy and thus are often overlooked. Their detection may only be possible with careful examination, including targeted exclusion of possible abnormalities. Therefore, strict adherence to a checklist and knowledge of possible anomalies is mandatory for success at this level. There are, however, a few conditions in which a heart defect may be overlooked even by experts, despite detailed knowledge and careful examination. As a result, sensitivities range in specialized centers between 80 and 90%. Factors mentioned in Reason 1 above, such as transducer frequency, gestational age, insonation angle, examination time and maternal factors (e.g. obesity), may play an important additional role in determining whether a defect is overlooked, and if the defect is small for the gestational age at which screening occurs, it may go undetected. Suggestions for a solution Teaching should not only include how to obtain a fourchamber plane but it should also focus on the patterns of detectable anomalies. Tricks and hints as to how the anomaly can be detected or ruled out should be emphasized. The teacher should not only teach the most common heart defects one by one, but mainly focus on the prenatal signs of the abnormality which should raise suspicion for referral to a specialist. Examples are shown in Figures 2 and 3. In the case of atrioventricular septal defect (Figure 2), four chambers are found and the defect, which manifests in the crux of the heart, may be overlooked. The anomaly may be suspected when the heart is magnified and different phases of the cardiac cycle are analyzed with the cine-loop technique. During diastole, the defect of the interatrial and interventricular septa in the center of the heart can be visualized. In systole, when the valves are closed, they are found in a horizontal plane rather than at different levels as in normal hearts. In coarctation of the aorta (Figure 3) there is typically a discrepancy in the left/right ventricular width, but the four chambers are present and have normal contractility. In some forms of hypoplastic left and right hearts the chambers appear of equal size and the anomaly may be overlooked. Recognition of decreased contractility of the abnormal chamber aids detection. The presence of

4 6 Chaoui a b Figure 2 Atrioventricular septal defect at 22 weeks. This cardiac anomaly can be easily overlooked since four chambers are present. During systole (a) the closed atrioventricular valves are at the same level; during diastole (b) the gap in the crux of the heart is recognizable. multicenter study evaluating the prevalence and spectrum of prenatally detected heart anomalies in the UK, Bull 9 found that 69% of all univentricular and 66% of all hypoplastic left hearts were detected prenatally, compared with only 38% of all atrioventricular septal defects. LV RV Figure 3 Coarctation of the aorta can be overlooked on four-chamber view screening. The four chambers are present and show normal contractility but there is a discrepancy in the ventricular widths, the left ventricle (LV) being narrower than the right (RV). a persistent left superior vena cava may be a sign of an associated cardiac anomaly: the cross-section of this vein may be visualized as a small cyst on the border of the left atrium. Univentricular hearts are obviously easier to detect than are some of the anomalies described previously. In a REASON 3: THE ANOMALY EVOLVES IN UTERO With evolving experience in fetal echocardiography we have learned that not all heart defects are already present in early or mid-pregnancy; they may develop in utero. This has been demonstrated for left and right semilunar valve obstruction10 13 and other conditions (see also Maeno et al. 14 ). Rarely, it has been reported that a heart documented as normal on real-time and color Doppler imaging developed into hypoplastic left or right heart. In most cases, the heart had left or right ventricular dysfunction associated with severe aortic or pulmonary stenosis detected during the second trimester. Followup in the late third trimester revealed (anatomical or hemodynamic) valve atresia and absence of growth of the ventricular cavity. Tricuspid valve incompetence may resolve but it may worsen, depending on the underlying condition. In the example shown in Figure 4, the four chambers appeared of normal size on second-trimester ultrasound examination, but color Doppler revealed severe tricuspid insufficiency due to associated pulmonary atresia. This insufficiency leads to massive dilatation of the heart in the late third trimester. Deterioration in utero was the rationale for attempts to stop or reverse ventricular damage by balloon valvuloplasty in utero in fetuses with critical aortic or pulmonary stenosis Rhabdomyoma is a further cardiac abnormality which rarely presents in the second trimester but may be detected later in gestation.

5 Editorial 7 a b LV RV LA RA Figure 4 The same heart at 22 weeks (a) and 36 weeks (b) showing the development of cardiomegaly in utero. The fetus had pulmonary atresia with an intact septum. During pregnancy the right ventricle (RV) did not grow as expected and tricuspid insufficiency led to dilation of the right atrium (RA). LA, left atrium; LV, left ventricle. Detection of cardiac defects in early pregnancy has become increasingly reliable in recent years, particularly with widespread adoption of the week scan, and fetuses with increased nuchal translucency being defined as being at high risk for heart defects. It must be borne in mind, however, that early fetal echocardiography may be reliable but it is not (yet?) as accurate as second-trimester examination and cannot replace it. Suggestions for a solution It seems impossible to avoid overlooking anomalies which develop in utero with screening ultrasound. However, this appears to be a relatively rare cause of overlooked cardiac anomalies compared with cases being missed on screening. The accurate detection of a severe, isolated, heart anomaly or those in association with extracardiac malformations may lead to mid-trimester termination of pregnancy. In many detected cases, however, especially with isolated CHD, planned delivery at a tertiary center with optimized neonatal care is possible. Since heart anomalies developing in utero may be missed at secondtrimester screening, the fetal heart should be examined if third-trimester scanning is performed. Yagel et al. 20 analyzed the impact of gestational age in detection of heart defects. In early pregnancy (13 16 weeks), 64% of CHDs were detected and this increased to 81% when a second examination was added at weeks. This rate was similar to the group examined primarily at weeks, in which 78% of CHDs were detected. An additional scan during the third trimester showed cumulative detection up to 85% in both groups. REASON 4: THE HEART ANOMALY IS NOT DETECTABLE IN THE FOUR-CHAMBER VIEW ON REAL-TIME SCANNING It is known that the four-chamber view cannot detect the majority of heart anomalies 21. Many conotruncal anomalies are associated with normal four-chamber anatomy. Therefore, this is the wrong screening test for a number of anomalies primarily involving the great vessels. Examination of the four-chamber view with routine prenatal ultrasound will miss some severe heart anomalies unless additional findings such as large ventricular septal defect or small ventricular cavity are present. Examples of such anomalies include transposition of the great arteries (Figure 5), tetralogy of Fallot, double-outlet right ventricle, truncus arteriosus communis and interruption of the aortic arch. Relying on the real-time four-chamber view may lead to overlooked cases in which detection could be significantly aided by color Doppler, most commonly in cases of muscular ventricular septal defect and tricuspid valve regurgitation, which is found in many fetal conditions 22. A few other defects are only detectable postnatally, such as some forms of coarctation of the aorta, septum secundum atrial defect and patent ductus arteriosus.

6 8 Chaoui LV RV LV RV TP Ao Figure 5 Complete transposition of the great arteries. The four-chamber view appears normal but visualization of the great vessels shows a typical parallel course (arrows). The pulmonary trunk (TP) arises from the left ventricle (LV) and the aorta (Ao) from the right ventricle (RV). Suggestions for a solution The cardiac scan is a dynamic examination and should not use only one fixed plane such as the four-chamber view; it should include visualization of the great vessels as well 21. Over 15 years ago, the four-chamber view was proposed as part of the routine screening examination. Since then, several generations of ultrasound equipment have been used and great experience has been acquired at all levels of fetal medicine. It is time to request that the cardiac examination should not continue to be limited to the four-chamber view. It is the right of patients undergoing screening ultrasound to have a proper and complete scan, including of the heart. Many examiners are experienced in seeking subtle soft markers for chromosomal anomalies but avoid routine visualization of the great vessels. Achiron et al. 23 examined 5400 women in the second trimester, and reported a detection rate for CHDs of only 48% with the four-chamber view alone, compared with 78% with an extended cardiac examination. This is similar to the rate reported in a recent study by Carvalho et al. 24, who showed that the incorporation of ventricular outlet views at the routine fetal anomaly scan between 18 and 23 weeks achieved a detection rate of 75%. Routine use of color Doppler during cardiac scanning will also improve detection rates. This is more controversial than is the issue proposed above, and has been discussed in a recent review 22. It is not realistic to assume that color Doppler is available for every screening examination and in every country. On the other hand, it is difficult to accept that, in centers in which the screening examination is performed with high-resolution equipment with color Doppler facilities, this feature is not used routinely and is reserved only for those cases in which a heart anomaly is suspected. This review discusses the advantages of color Doppler and the information supplied on screening examination in increasing the speed and accuracy of the fetal cardiac scan 22. CONCLUSIONS There are sufficient studies and clinical experience to conclude that screening for fetal cardiac defects at the second-trimester ultrasound examination gives excellent results if performed properly. The effectiveness of screening for fetal heart defects should be evaluated according to the detection rate of major or critical CHDs, which influence mainly perinatal morbidity and mortality 21. Hints to achieve success include: Examination of the fetal heart should be carried out at every second-trimester screening examination. This should ideally be at weeks gestation, using a 5-MHz transducer.

7 Editorial 9 The image should be magnified and the cine-loop function used to analyze the different phases of the heart cycle. Evaluation of the four-chamber view alone is, of course, an excellent tool if performed properly, and above I have made suggestions to improve the accuracy of the examination and reduce pitfalls. The examiner who is increasingly involved in detailed analysis of the four-chamber view will soon move to the additional evaluation of the great vessels. This should be our aim for future training on how to achieve a complete heart examination by using different cross-sectional planes 35. The examiner should use a checklist and be familiar with possible abnormalities. If a third-trimester scan is performed, the heart should be evaluated at this time also, to detect anomalies which may have developed since, or were overlooked at, the previous scan. If color Doppler is available, it should be used routinely during the screening examination. REFERENCES 1. 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