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PRENATAL DIAGNOSIS Prenat Diagn 2004; 24: 1123–1129. Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/pd.1069 REVIEW Routine fetal cardiac screening: what are we doing and what should we do? Gurleen Sharland* Fetal Cardiology Unit, Guy’s Hospital, London, UK In many countries, ultrasound examination is used in the second trimester to look for congenital malformations as part of routine prenatal care. While tertiary centres scanning high-risk pregnancies have reported a high degree of accuracy in the detection of congenital heart disease, many studies have shown that cardiac abnormalities are commonly overlooked during routine obstetric evaluation and there still remains a huge variation between centres. The majority of babies with congenital heart disease are born to mothers with no identiable high-risk factors and so will not be detected unless there is widespread screening of the low-risk population. It is feasible to achieve widespread screening for fetal congenital heart disease in low-risk groups, but this does need commitment and effort from those performing the scans and those teaching them how to examine the heart. Staff performing routine obstetric ultrasound scans should learn a simple technique for examining the fetal heart and to use this in all patients. Links to a tertiary centre can provide support for checking scans of concern as well as for providing training and for obtaining feedback. In addition, an audit system needs to be established in each centre to trace false-positive and false-negative cases as well as to conrm true positives and true negatives. Copyright 2004 John Wiley & Sons, Ltd. KEY WORDS: heart defects prenatal; ultrasonography prenatal; screening prenatal INTRODUCTION Cardiac malformations are one of the commonest types of congenital abnormalities and remain a major cause of morbidity and mortality in infancy (Hoffman, 2002; Forfar, 1984). In a number of cases, the cardiac lesion is still not recognised during life (Abu Harb et al., 1994). It is now possible to detect most forms of major congenital heart disease (CHD), as well as some of the minor forms prenatally (Allan et al., 2000). Detection in early pregnancy allows parental choice and time for parents to be prepared for the likely course of events after delivery. However, examining the fetal heart during pregnancy can also be of great benet, if normality can be conrmed, in providing reassurance to parents at high risk of having a child with CHD. Even so, there has been much controversy about whether screening ultrasound is of benet. The conclusions of the RADIUS study published in 1993 (Ewigman et al., 1993) suggested that obstetric ultrasound screening did not improve perinatal mortality or morbidity and was not cost-effective. However, the Helsinki ultrasound trial demonstrated that in patients screened by ultrasound there was a signicant decrease in perinatal mortality, an increased rate of detection of malformations and a decrease in total health care costs (Saari-Kemppainen et al., 1990; Leivo et al., 1996). As far as the fetal heart is concerned, several reports have shown that in specic lesions an improved outcome is associated with prenatal *Correspondence to: Dr Gurleen Sharland, Fetal Cardiology Unit, 15th Floor Guy’s Tower, Guy’s Hospital, St Thomas Street, Lon- don SE1 9RT, UK. E-mail: [email protected] diagnosis (Bonnet et al., 1999; Andrews et al., 2001; Copel et al., 1997; Simpson and Sharland, 1998). In many countries, ultrasound examination is used in the second trimester to look for congenital malforma- tions as part of routine prenatal care. While tertiary centres have reported a high degree of accuracy in the detection of CHD, many studies have shown that cardiac abnormalities are commonly overlooked during routine obstetric evaluation and that there is a huge variation between centres in the same country, as well as differences between different countries (Bull, 1999; Garne et al., 2001; Buskens et al., 1996; Boyd et al., 1998; Hafner et al., 1998; Stumpen et al., 1996; Jaeggi et al., 2001; Tegnander et al., 1995; Klein et al., 1999; Hafner et al., 1998; Stoll et al., 1998; Ott, 1995). This is important because, currently, high-risk pregnancies are referred for specialist fetal echocardiography, but the majority of babies with CHD are born to mothers with no identiable high-risk factors. In order to detect these cases, screening of the low-risk population is needed to achieve a high prenatal detection rate for CHD. Thus, the initial identication of these cases will be dependent on the ability and expertise of sonographers and other personnel involved in routine obstetric ultrasound. Some sonographers have already reached an adequate level of expertise, but results show that the many have not. It has also been demonstrated that obstetric sonographers increase their ability to detect heart defects following a concentrated training programme (Sharland and Allan, 1992; Hunter et al., 2000; Rustico et al., 1995). If pre- natal detection of CHD is a real goal, then a widespread teaching and training programme needs to be established to ensure that a uniform standard of cardiac scanning is Copyright 2004 John Wiley & Sons, Ltd.

Routine fetal cardiac screening: what are we doing and what should we do?

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PRENATAL DIAGNOSISPrenat Diagn 2004; 24: 1123–1129.Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/pd.1069

REVIEW

Routine fetal cardiac screening: what are we doing and whatshould we do?

Gurleen Sharland*Fetal Cardiology Unit, Guy’s Hospital, London, UK

In many countries, ultrasound examination is used in the second trimester to look for congenital malformationsas part of routine prenatal care. While tertiary centres scanning high-risk pregnancies have reported a highdegree of accuracy in the detection of congenital heart disease, many studies have shown that cardiacabnormalities are commonly overlooked during routine obstetric evaluation and there still remains a hugevariation between centres. The majority of babies with congenital heart disease are born to mothers with noidentifiable high-risk factors and so will not be detected unless there is widespread screening of the low-riskpopulation. It is feasible to achieve widespread screening for fetal congenital heart disease in low-risk groups,but this does need commitment and effort from those performing the scans and those teaching them how toexamine the heart. Staff performing routine obstetric ultrasound scans should learn a simple technique forexamining the fetal heart and to use this in all patients. Links to a tertiary centre can provide support forchecking scans of concern as well as for providing training and for obtaining feedback. In addition, an auditsystem needs to be established in each centre to trace false-positive and false-negative cases as well as toconfirm true positives and true negatives. Copyright 2004 John Wiley & Sons, Ltd.

KEY WORDS: heart defects prenatal; ultrasonography prenatal; screening prenatal

INTRODUCTION

Cardiac malformations are one of the commonest typesof congenital abnormalities and remain a major causeof morbidity and mortality in infancy (Hoffman, 2002;Forfar, 1984). In a number of cases, the cardiac lesionis still not recognised during life (Abu Harb et al.,1994). It is now possible to detect most forms of majorcongenital heart disease (CHD), as well as some of theminor forms prenatally (Allan et al., 2000). Detectionin early pregnancy allows parental choice and timefor parents to be prepared for the likely course ofevents after delivery. However, examining the fetalheart during pregnancy can also be of great benefit, ifnormality can be confirmed, in providing reassuranceto parents at high risk of having a child with CHD.Even so, there has been much controversy about whetherscreening ultrasound is of benefit. The conclusions ofthe RADIUS study published in 1993 (Ewigman et al.,1993) suggested that obstetric ultrasound screening didnot improve perinatal mortality or morbidity and wasnot cost-effective. However, the Helsinki ultrasound trialdemonstrated that in patients screened by ultrasoundthere was a significant decrease in perinatal mortality,an increased rate of detection of malformations and adecrease in total health care costs (Saari-Kemppainenet al., 1990; Leivo et al., 1996). As far as the fetal heartis concerned, several reports have shown that in specificlesions an improved outcome is associated with prenatal

*Correspondence to: Dr Gurleen Sharland, Fetal Cardiology Unit,15th Floor Guy’s Tower, Guy’s Hospital, St Thomas Street, Lon-don SE1 9RT, UK. E-mail: [email protected]

diagnosis (Bonnet et al., 1999; Andrews et al., 2001;Copel et al., 1997; Simpson and Sharland, 1998).

In many countries, ultrasound examination is used inthe second trimester to look for congenital malforma-tions as part of routine prenatal care. While tertiarycentres have reported a high degree of accuracy inthe detection of CHD, many studies have shown thatcardiac abnormalities are commonly overlooked duringroutine obstetric evaluation and that there is a hugevariation between centres in the same country, as wellas differences between different countries (Bull, 1999;Garne et al., 2001; Buskens et al., 1996; Boyd et al.,1998; Hafner et al., 1998; Stumpflen et al., 1996; Jaeggiet al., 2001; Tegnander et al., 1995; Klein et al., 1999;Hafner et al., 1998; Stoll et al., 1998; Ott, 1995). This isimportant because, currently, high-risk pregnancies arereferred for specialist fetal echocardiography, but themajority of babies with CHD are born to mothers withno identifiable high-risk factors. In order to detect thesecases, screening of the low-risk population is needed toachieve a high prenatal detection rate for CHD. Thus,the initial identification of these cases will be dependenton the ability and expertise of sonographers and otherpersonnel involved in routine obstetric ultrasound. Somesonographers have already reached an adequate level ofexpertise, but results show that the many have not. Ithas also been demonstrated that obstetric sonographersincrease their ability to detect heart defects following aconcentrated training programme (Sharland and Allan,1992; Hunter et al., 2000; Rustico et al., 1995). If pre-natal detection of CHD is a real goal, then a widespreadteaching and training programme needs to be establishedto ensure that a uniform standard of cardiac scanning is

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attained in all obstetric ultrasound units. Such a pro-gramme would have widespread implications and con-sequences, which may prove difficult to address.

CURRENT ORGANISATION OF FETALECHOCARDIOGRAPHY

High-risk pregnancies

High-risk pregnancies are referred to tertiary centres forevaluation of the fetal heart. Pregnancies at increasedrisk of CHD include those with the following:

1. Maternal factors identified at booking:(a) A family history of CHD (Gill et al., 2002).(b) Maternal diabetes (Meyers-Wittkopf et al., 1996).(c) Exposure to teratogens in early pregnancy.

2. Fetal high-risk factors:(a) The detection of an extra-cardiac fetal anomaly

on ultrasound (Allan et al., 1991; Copel et al.,1986).

(b) Fetal arrhythmias, particularly complete heartblock.

(c) Non-immune fetal hydrops (Skoll et al., 1991;Kleinman et al., 1982).

(d) Increased nuchal translucency in the first trimester(Hyett et al, 1999).

Low-risk groups

The majority of cases of fetal CHD will occur in a low-risk population, even though it is the high-risk groupsthat are referred for specialist fetal echocardiography.This is illustrated in Figure 1, which shows that outof a total of 2758 cases of prenatal CHD, 80% werereferred as a result of screening the low-risk population.Thus, in order to detect a large number of cases of majorCHD prenatally, there must be a system of screening thefetal heart in the low-risk population. This means that allultrasound examinations performed in low-risk pregnantwomen, with the view of detecting fetal malformation,must include examination of the fetal heart.

0

500

1000

1500

2000

2500

?CHD FH Fabn Farr Fhyd Diabetic other

Figure 1—Referral reasons in 2758 cases of congenital heart diseaseseen in the fetal cardiology unit at Guy’s Hospital, London.?CHD,suspected heart abnormality during obstetric scan; FH, family history;Fabn, extra-cardiac fetal abnormality; FARR, fetal arrhythmia; Fhyd,fetal hydrops; diabetic, maternal diabetes; other, other high-riskindications

The concept of prenatal screening for CHD wasintroduced in the United Kingdom in 1986 (Allanet al., 1986), following the results of a French study(Fermont et al., 1986), which proposed that the four-chamber view of the heart be incorporated into theroutine obstetric scan performed at 18 to 22 weeksof gestation. Following this, a concentrated screeningprogramme was set up in 10 obstetric centres in thesouth-east Thames region in 1988 (Sharland and Allan,1992). This study showed that screening for some of themajor forms of CHD can be implemented prenatally bythose performing the routine obstetric scan if the four-chamber view of the heart is correctly examined. In a2.5-year period, 77% of all the cardiac abnormalitiesthat would be associated with an abnormal appearanceof the four-chamber view of the heart, were detected inthe 10 obstetric scanning centres, following appropriateteaching of the personnel involved in scanning. In67% of cases, the heart defects were detected as aresult of four-chamber view screening, and, in a further10%, there were associated high-risk factors, whichprompted referral for detailed fetal echocardiography.More recently, however, a collaborative study on behalfof the British Paediatric Cardiac Association has shownthat only 23.4% of major forms of heart disease weredetected prenatally in the United Kingdom during thestudy period (Bull, 1999). However, this study did notdifferentiate between cases that had and those that hadnot undergone a second-trimester anomaly scan thatincluded a four-chamber view. Thus, it is difficult tointerpret the data, but the detection rate for abnormalitiesassociated with an abnormal four-chamber view wasmuch higher than that for great artery abnormalities, with66% of cases of hypoplastic left heart syndrome and38% of atrioventricular septal defects being detected,compared with 3% of simple transpositions and 11% ofconotruncal abnormalities. This is not surprising becausethe four-chamber view was introduced as the first stepfor screening for heart defects with progression toinclude views of the great arteries later. However, evenfor the four-chamber abnormalities, this study showedthat there was a huge regional difference in prenataldetection rates with many detectable abnormalities stillbeing overlooked. The variation in detection rates maybe a reflection of differences in screening policy aswell as different levels of training to examine the heart.The success of prenatal screening for CHD is relatedto the expertise and experience of the ultrasonographersperforming the scans; and this is clearly not uniform.This variation in the ability to detect CHD is reflectedin many other reported studies (Stumpflen et al., 1996;Tegnander et al., 1995; Garne et al., 2001; Buskenset al., 1996; Montana et al., 1996).

Although the four-chamber view examination hasbeen shown to be an effective method of detecting someof the severe forms of cardiac malformation in utero, thiswill not detect all major forms of CHD (Sharland andAllan, 1992; Fermont et al., 1986; Vergani et al., 1992;Comstock, 2000). Including examination of the arterialconnections of the heart will improve the detectionrate (Wigton et al., 1993; Kirk et al., 1994), but thepracticality and feasibility of this in the setting of

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routine obstetric scanning is still not clear. There is nodoubt, however, that in order to detect fetal CHD thesonographer performing the scan must learn to examinethe fetal heart, whether this includes four-chamber viewsalone, or in conjunction with views of the great arteries.

A SIMPLE APPROACH TO EXAMINE THE FETALHEART DURING ROUTINE SCREENING

Many previous publications have described in detail themethods of examining the fetal heart (Allan et al., 2000;Allan, 1986). A systematic approach will enable theconfirmation of normality easily, and make it easier torecognise congenital heart malformations.

A simple stepwise method can be used by startingwith the four-chamber view (Figure 2) and making aseries of horizontal sections moving more cranially toview initially the aorta arising from the left ventricle(Figure 3). Angulating the transducer cranially from thefour-chamber view towards the right shoulder demon-strates the aorta arising in the centre of the chest fromthe left ventricle. From here, a horizontal section cra-nial to this plane will demonstrate the pulmonary artery(Figure 4). This artery arises anteriorly, close to thechest wall and is directed straight back towards thespine. More cranial to this is the so-called three-vesselview, which demonstrates the aorta, pulmonary arteryand superior vena cava (Figure 5). In this view, the aortaand pulmonary artery should appear of approximatelyequal size. In this ‘sweep’ of sections can be included atransverse section of the abdomen to view the positionof the stomach, the descending aorta and the inferior

Figure 2—Normal four-chamber view of the fetal heart

Figure 3—Aorta arising from the left ventricle and directed towardsthe baby’s right shoulder

Figure 4—Pulmonary artery arising beneath the anterior chest walland directed towards the fetal spine

vena cava (Figure 6). The fetal stomach and the fetalheart should both lie on the left side.

Important features of a four-chamber view are thefollowing:

1. The heart occupies about a third of the thorax andthe apex points out of the left anterior thorax.

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Figure 5—The three-vessel view showing the pulmonary artery, aortaand superior vena cava

Figure 6—A view of the abdominal arrangement of the descendingaorta, inferior vena cava and stomach

2. There are two atria of approximately equal size.3. There are two ventricles of approximately equal size

and thickness. Both show equal contraction in themoving image.

4. The atrial and ventricular septa meet the two atri-oventricular valves (mitral and tricuspid) at the cruxof the heart forming an offset cross. This offset crossappearance is because the septal leaflet of the tri-cuspid valve inserts slightly lower in the ventricularseptum than the mitral valve.

5. The two atrioventricular valves (mitral and tricuspid)are seen to open equally in the moving image.

6. The inter-atrial defect, the foramen ovale is patent infetal life. It is usually guarded by the foramen ovaleflap valve, which can usually be seen flickering inthe left atrium.

7. The interventricular septum should appear intact.8. The pulmonary venous connections to the back of the

left atrium should be identified.

The two most common abnormalities detected onfour-chamber view examination are hypoplastic leftheart syndrome and atrioventricular septal defect. Anexample of each is shown in Figures 7 and 8.

The following features of the great arteries allowmajor anomalies of the great vessels to be excluded:

1. Two arterial valves should always be seen.2. The aorta arises from the centre of the chest and is

wholly committed to the left ventricle. It gives rise tothe aortic arch, which can be identified by head andneck vessels.

3. The pulmonary artery arises from the right ventricleand is a branching vessel, which gives rise to thebranch pulmonary arteries and the arterial duct.

4. The great arteries are similar in size, but the pul-monary artery at the valve ring may be slightly biggerthan the aorta.

5. The pulmonary valve is anterior and cranial to theaortic valve.

Figure 7—The four-chamber view in hypoplastic left heart syn-drome showing a diminutive echogenic left ventricle and a dominantright ventricle

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Figure 8—An example of an atrioventricular septal defect

Figure 9—In this example of transposition of the great vessels, thefour-chamber view was normal. However, examination of the greatvessels revealed parallel orientation of the two great arteries with theaorta arising from the right ventricle and the pulmonary artery fromthe left ventricle

6. The great arteries cross over at their origin.

Common cardiac abnormalities that can be detected byexamining the great vessels, but missed on four-chamberview examination are transposition of the great arteriesand tetralogy of Fallot. An example of each is shown inFigures 9 and 10.

Figure 10—An example of a ventricular septal defect with aortic over-ride, as seen in tetralogy of FallotLA, left atrium; RA, right atrium;LV, left ventricle; RV, right ventricle; Ao, aorta; PA, pulmonary artery;SVC, superior vena cava; IVC, inferior vena cava; des Ao, descend-ing aorta

Practicality of routine screening

In 1997, a report from the Royal College of Obstetri-cians and Gynaecologists (RCOG) of screening for fetalabnormalities (RCOG, 1997) identified that one of theproblems with screening scans was the variable way inwhich they were conducted throughout the country. Asupplementary report published in 2000 (RCOG, 2000)provided a standard format for a 20-week anomaly scan.In this report, the minimum standard for a 20-weekanomaly scan includes examination of the four-chamberview of the fetal heart. The optimal standard for the20-week anomaly scan includes examination of the car-diac outflow tracts. However, the optimal scan can onlybe achieved in Trusts where resources allow, as thistakes additional time, may require some women to attendfor additional review and requires additional training.Thus, as far as the fetal heart is concerned, all unitsperforming ‘anomaly scans’ should include the four-chamber view as a minimum in the examination. Evenso, published data suggests that a uniform standard offour-chamber screening has not yet been reached and, inmany instances, cardiac abnormalities associated with anabnormal four-chamber view are being overlooked dur-ing anomaly scans. The Royal College report suggeststhat examination of the arterial connections should bepart of an optimal anomaly scan. However, with someunits still not being successful with four-chamber viewexamination, this may not yet be realistic for all units.Currently, it is for individual units to decide whetherthey are able to include views of the outflow tracts aspart of the examination. Whatever the level of scanning,it is vital for each unit to have a clear outline of whatcan and what cannot be achieved, both for the pregnant

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women and the staff. Many of the women being screenedmay have unrealistic expectations and may believe thatscreening tests have a perfect sensitivity and specificity.It is important that they are given information prior tothe scan about possibility of detecting a problem andalso be made aware of what can and cannot be detected.

How can we improve the detection rate ofcongenital heart disease prenatally?

The success of individual units in the detection of majorCHD during routine obstetric scanning has not beenextended to all. This is a key area of weakness inestablishing effectual screening for prenatal CHD. Inorder to achieve a uniform standard of cardiac scan-ning in the routine obstetric setting, there needs to bewidespread teaching and training for appropriate per-sonnel, the majority of whom will be sonographers. Thismust include practical hands on training as well as fac-tual information disseminated through lectures/seminars.The training needs to be a continuing process with sup-port and feedback being provided by specialist centres.Realistically, this is a huge task, but potentially possible.

In addition to learning to look at the heart correctly, itis important to keep accurate records and audit activity,so that all the staff in individual units is aware of all thecorrect diagnoses made as well as all the false positivesand false negatives. For these reasons, links to a tertiarycentre may prove beneficial for several reasons. Firstly,this provides support for checking scans where there isconcern about the fetal heart, and a system for feedingback information on true positives and false positivescan be established. Secondly, a system of continuoustraining could be established if there are links in placewith a specialist centre.

SUMMARY/CONCLUSIONS

Staff performing routine obstetric ultrasound scans needadequate training and support to examine the fetalheart. It is feasible to achieve widespread screening forfetal CHD in low-risk groups. However, this does needcommitment and effort from those performing the scansand those teaching them how to examine the heart. Itis important to learn a simple technique for examiningthe fetal heart and to use this in all patients scanned.Patience, experience and determination will improve thedetection rates of CHD prenatally. In addition, an auditsystem needs to be established to trace false-positive andfalse-negative cases as well as to confirm true positivesand true negatives.

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