fetal ecocardiography text

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Carmina Comas Gabriel, Pilar Prats RodriguezREVIEW ARTICLE

Echocardiography in Early PregnancyCarmina Comas Gabriel, Pilar Prats RodrRRRRRguez

10.5005/jp-journals-10009-1281

ABSTRACT

Within the last decade, two significant events have contributedto the increasing interest in early fetal echocardiography. First,the introduction of high frequency vaginal ultrasound probesallows detailed visualization of cardiac structures at early stageof gestation, making early detection of fetal malformationspossible. Second, the close relationship observed between somefirst trimester sonographic and Doppler markers and congenitalheart defects allows an early identification of a high-risk groupat 11 to 14 weeks of gestation. In this context, from the early1990s, many authors have examined the potential role of thetransvaginal approach to obtain earlier diagnosis of fetal cardiacmalformations. Further studies have appeared in the literatureshowing that early transvaginal echocardiography inexperienced hand is a fairly sensitive investigative tool. Althoughsome malformations are detected as early as 11 weeks'gestation, the optimal gestational age to perform the early scanis at least 13 weeks' gestation. Transvaginal ultrasound is thepreferred approach, although most of the authors agree thatresults can be improved if transabdominal ultrasound is alsoincorporated. The further application of color Doppler enhancesvisualization. The sensitivity and specificity of early fetalechocardiography for the detection of heart anomalies isacceptable compared to the ones obtained by mid-gestationalechocardiography, showing a slight reduction in detection ratesand an increase in false positive and negative rates. The cardiacanomalies detected at this early stage of pregnancy are mainlydefects involving the four-chamber view, indicating that defectssolely affecting the outflow tracts are difficult to diagnose in thefirst trimester of pregnancy. Heart defects diagnosed early inpregnancy tend to be more complex than those detected later,with a higher incidence of associated structural malformations,chromosomal abnormalities and spontaneous abortions. Theneonate follow-up or postmortem examination in case oftermination of pregnancy (TOP) is essential to assess the actualrole of early fetal echocardiography. At present, early fetalechocardiography is a promising technique, which can be ofconsiderable value for patients at high-risk. This technique is,however, currently limited to a few specialized centers.

The aim of this review is to explore the possibilities ofexamining the fetal heart at this early stage of pregnancy. Thisarticle also present our experience in the first multicenter trial inearly fetal echocardiography performed in Spain. In accordancewith other studies, this experience stresses the usefulness ofearly echocardiography when performed by expert operatorson fetus specifically at risk for cardiac defects. Our review ofthese additional 48 cases contributes to the expanding literatureon the ability of transvaginal ultrasonography to detect fetal heartdefects in early pregnancy.

Keywords: Echocardiography, Early diagnosis, Earlypregnancy, Prenatal diagnosis, Early echocardiography.

How to cite this article: Gabriel CC, Rodriguez PP.Echocardiography in Early Pregnancy. Donald School JUltrasound Obstet Gynecol 2013;7(2):168-181.

Source of support: Nil

Conflict of interest: None declared

INTRODUCTION

Prenatal detection of fetal congenital heart defects (CHD)remains the most problematic issue of prenatal diagnosis.1

Major CHD are the most common severe congenitalmalformations, with an incidence of about 5 in a thousandlive births, whenever complete ascertainment is done andminor lesions are excluded.1,2 Congenital heart anomalieshave a significant effect on affected children’s life with upto 25 to 35% mortality rate during pregnancy and thepostnatal period, and it is during the first year of life, whenthe 60% of this mortality occurs. Moreover, major CHDare responsible for nearly 50% of all neonatal and infantdeaths due to congenital anomalies, and it is likely to besignificantly higher if spontaneous abortions are considered.Although CHD use to appear isolated, they are frequentlyassociated with other defects, chromosomal anomalies andgenetic syndromes. Their incidence is 6 times greater thanchromosomal abnormalities and 4 times greater than neuraltube defects.1-3

Most major CHD can be diagnosed prenatally bydetailed transabdominal second trimester echocardiographyat 20 to 22 weeks’ gestation.1,3-6 The identification ofpregnancies at high-risk for CHD needing referral tospecialist centres is of paramount importance in order toreduce the rate of overlooked defects.6,7 However, the mainproblem in prenatal diagnosis of CHD is that the majorityof cases take place in pregnancies with no identifiable riskfactors. Therefore, there is wide agreement that cardiacultrasound screening should be introduced as an integralpart of the routine scan at 20 to 22 weeks. When applied tolow-risk population, scrutiny of the four-chamber viewallows only the detection of 40% of the anomalies whileadditional visualization of the outflow tracts and the greatarteries increase the rate up to 60 to 70%.3-5

Recently, the finding of an increased nuchaltranslucency8,9 or an altered ductus venosus blood flow10,11

at 10 to 14 weeks’ gestation have been associated with ahigh-risk for CHD and their prevalence increaseexponentially with the thickness of nuchal translucency8

regardless of the fetal karyotype. Since earlier diagnosis ofcongenital malformations is increasingly demanded, theoption of an early fetal echocardiography must be takeninto account.12-14 The use of high-frequency vaginalultrasound probes along with substantial improvements inmagnification and processing of the imaging, together with

Donald School Journal of Ultrasound in Obstetrics and Gynecology, April-June 2013;7(2):168-181 169

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Echocardiography in Early Pregnancy

the introduction of color Doppler, have extensivelycontributed to the development of the technique, allowingbetter visualization of cardiac structures earlier inpregnancy.12,15,16 Although most of the groups perform earlyfetal echocardiography between 13 and 16 weeks’ gestation,we can name it as so when performed before the 18th weekof gestation. Despite several studies that stated that fetalheart examination could be incorporated in first or earlysecond trimester examinations, its use is currently stilllimited to a few specialized centers.

TECHNICAL ISSUES

Regarding early fetal echocardiography, some institutionsuse predominantly the transvaginal approach14,17-22 whileothers prefer the transabdominal one.23-26 Most of theauthors reporting early fetal echocardiography prefer thetransvaginal approach due to its increased resolutionassociated with higher frequency transducers and alsobecause given that equivalent transducers frequencies, thetransvaginal probes provide better quality images.27

However, most importantly, authors with backgroundtraining as pediatric cardiologists are more likely to use thetransabdominal approach in contrast with most ofobstetricians, who are well used to the transvaginal route.The superiority of transvaginal sonography is usually wellaccepted before the 14th week. Between the 15th and 18thweek both transabdominal and transvaginal routes seem tooffer similar advantages and disadvantages, and beyond the18th week the transabdominal echocardiography seems toachieve better results.1,5,16,27,28

The combination of two-dimensional (2D) echocardio-graphy with color Doppler flow imaging proved generallyhelpful, in particular by visualization of blood flow on bothgreat arteries and of two divided ventricular inflows. Theaddition of color Doppler flow studies provides substantialimprovement in the diagnostic accuracy of earlyechocardiography, as was also shown by DeVore fortransabdominal sonography in the second-half ofpregnancy.29

When performing early fetal echocardiography, wefirstly recommend scanning by the transvaginal route,following the examination by the transabdominal probewhen a complete study is not possible. The highestfrequency must always be used, whatever the route ischosen. Obviously, a high resolution real-time ultrasoundhas to be used. For color Doppler evaluation, the energyoutput levels have to be lower than 50 mW/cm2 spatial peaktemporal average. Since color Doppler is dissipated over awide area of interest, thermal effects resulting from Dopplerinsonation should not be a matter of concern, unlike pulsed

Doppler in which the whole energy of the beam is focusedat a specific location. Besides, the embryonic developmentalof the heart has been completed by the time the scan isperformed.

ULTRASOUND ANATOMY OF THENORMAL HEART

Embryonic heart beat can be detected as early as the fifthweek of gestation, and normal development of its functionshows an increasing heart rate from 80 to 90 beats per minuteat 5 weeks’ gestation to 170 to 180 beats per minute at theend of the 9 to 10th week. As pregnancy progresses, thecontrol of the heart rate matures with increasing vagaldominance, and the baseline rate declines to 145 to 155beats per minute with the appearance of beat to beatvariation, most likely resulting from the functionaladaptation to the development of the heart and autonomicnervous system maturation, and remains more or lessconstant during the rest of intrauterine life.30,31

The structural development of the heart begins on day16 and it is finished by the 10th week. Early fetalechocardiography has the same goals that the standard oneand we advocate to perform it in a segmental approach.The first objective of the examination is to assess thenormality of the four-chamber view through a transversesection of the fetal chest: Normal situs solitus; normal sizeand axis of the heart in relation to the chest; both atria equalin size, with the foramen ovale flapping within the leftatrium; both ventricles equal in size and contractility; atrialand ventricular septa are of normal appearance; tricuspidand mitral valves are normally inserted, opening and closingtogether. Color and pulsed Doppler are particularly usefulto confirm normal inflow to the ventricles and to detectturbulent flow or jets suggesting valve regurgitation. It isuseful to assess the four-chambers in different views: apical,basal and long axis with the interventricular septumperpendicular to the ultrasound beam in order to visualizebetter the integrity of the septum. Then, the origin and doublecrossing of the great arteries must be correctly identified:the left ventricle outflow tract, with the continuity betweenthe interventricular septum and the anterior wall of theascending aorta; the right ventricle outflow tract, moresuperior, anterior, almost perpendicular to the axis of theascending aorta and connecting to the descending aorta inthe three vessels view. Color Doppler is also of help to bettervisualize the outflow tracts confirm anterograde flowthrough the semilunar valves and great arteries, and makeseasier the examination of both aortic and ductal archs andtheir confluence. Pulsed Doppler may be used to assessblood flow through the aortic and pulmonic valves in order

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Carmina Comas Gabriel, Pilar Prats Rodriguez

to confirm normal anterograde flow and to detect very highvelocities suggesting valve stenosis. Finally, color andpulsed Doppler are also very useful to identify normalsystemic and pulmonary venous return. Figures 1 to 10illustrates images obtained at early fetal scan by 2Dechocardiography and color Doppler in a structurally normalheart. In our experience, the average duration of thecomplete fetal cardiac scan is over 15 minutes. It essentiallydepends on the gestational age at the examination, and canbe even shorter if there is a favorable fetal lie. In our setting,a subsequent transabdominal echocardiography is scheduledfor all our patients at 20 to 22 weeks’ gestation.

Most of the authors agree that the best window of timeto perform the early echocardiography is between the 13

and 16 weeks of gestation, since a complete cardiacexamination is rarely achieved before the 13th week ofgestation.14,17,18,20-22,26 Articles on early fetal echocar-diography demonstrate an increase in visualization rates ofthe four-chamber view and the outflow tracts in the lastdecade, with visualization rates greater than 90% at 13weeks’ gestation.28 To maximize the reduction of uninter-pretable examinations, early fetal echocardiography shouldbe preferably performed at 13 completed weeks’ gestation.Using current technology, the four-chamber view and theoutflow tracts are often demonstrated by 2D echocardio-graphy only, but color Doppler imaging enhances and makesthe identification of the structures faster, increasing thesuccess rate of the examination and allows even earlieridentification of the structures.

Figs 1A and B: Early fetal echocardiography by 2D in a structurallynormal heart. Situs visceral: Abdominal (A) and cardiac situs (B).Left: Fetal stomach, cross section of the abdominal aorta, spineand liver. Right: 4 chambers view. Heart axis pointing left, heartoccupies one third of the thorax, majority of heart in left chest—RV:right ventricle; LV: left ventricle; RA: right atrium; LA: left atrium;AAo: aorta abdominal; St: stomach; Sp: spine

Fig. 2: Early fetal echocardiography by 2D in a structurally normalheart. The 4 chambers view: Normal situs solitus; normal size andaxis of the heart in relation to the chest; both atria equal in size,with the foramen ovale flapping within the left atrium; both ventriclesequal in size and contractility; atrial and ventricular septa are ofnormal appearance; tricuspid and mitral valves are normallyinserted. RV: right ventricle; LV: left ventricle; RA: right atrium;LA: left atrium; FO: foramen ovale; DAo: descending aorta

Fig. 3: Early fetal echocardiography by 2D in a structurally normalheart. Color Doppler in the 4-chamber view is particularly useful toconfirm normal inflow to the ventricles and to detect turbulent flowor jets suggesting valve regurgitation. RV: right ventricle; LV: leftventricle; RA: right atrium; LA: left atrium

Figs 4A and B: Early fetal echocardiography by 2D and ColorDoppler in a structurally normal heart. (A) 4-chamber view—2D.(B) 4-chamber view—2D and color Doppler. RV: right ventricle;LV: left ventricle; RA: right atrium; LA: left atrium; FO: foramen ovale;DAo: descending aorta


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Figs 5A and B: Early fetal echocardiography by 2D and color Doppler and bi-flow in a structurally normal heart. The 4-chamber view. (A)4-chamber view—2D and color Doppler. (B) 4-chamber view—2D and bi-flow. RV: right ventricle; LV: left ventricle; RA: right atrium;LA: left atrium; FO: foramen ovale; DAo: descending aorta

Fig. 6: The 5-chamber view: Left ventricle outflow tract in the longaxis view showing the continuity between the interventricular septumand the anterior wall of the ascending aorta. RV: right ventricle;LV: left ventricle; RA: right atrium; LA: left atrium; AAo: ascendingaorta; DAo: descending aorta; IVS: interventricular septum

Fig. 7: Early fetal echocardiography by 2D in a structurally normalheart. The 3 vessels view: Cross-sections of the pulmonary artery,ascending aorta and superior vena cava in a transverse view ofupper mediastinum. In normal conditions, the structures in the 3vessels view are in descending order of size from left to the right.PA: pulmonary artery; Ao: aorta; SVC: superior vena cava

Figs 8A to C: Early fetal echocardiography by 2D, color Doppler and bi-flow in a structurally normal heart. Color Doppler is particularlyuseful to demonstrate the normal V confluence of the ductal and aortic archs (V sign). Note that normally the trachea is located behindthe aortic arch (A) 3 vessels view by 2D, (B) 3 vessels view by 2D and color Doppler, (C) 3 vessels view by 2D and bi-flow

DIAGNOSIS OF CHD

The first diagnosis of a CHD by early echocardiographywas reported by Gembruch et al32 in 1990. A completeatrioventricular canal defect, with complete heart block and

atrioventricular valve regurgitation was diagnosed at 11weeks + 4 days’ gestation using a 5 MHz transvaginal probe.The same year, Bronshtein et al33 reported the diagnosis ofa ventricular septal defect with overriding aorta and a further

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case of an isolated ventricular septal defect with pericardialeffusion, both cases at 14 weeks’ gestation. Since then, anincreasing number of case reports and series on the earlydiagnosis of CHD have been reported, both in high-risk andlow-risk population. Tables 1 and 2 summarizes some ofthe largest and most significant studies on the detection ofCHD using early fetal echocardiography in high-risk andlow-risk pregnancies.14,17-22,24-26,34-46 Obviously, studies inunselected population report less encouraging results, withlower visualization rates and detection rates. The largestseries was published by Bronshtein et al.20 They report thediagnosis of 173 cases of CHD over 36,323 fetuses evaluatedby transvaginal ultrasound at 11 to 17 weeks’ gestation overa 14-year period of time, with 99% of scans performed at14 to 16 weeks’ gestation and 86% of them in low-riskpopulation. Two institutions went further and reported theirexperience performing the echocardiography as early asbetween 10 and 13 weeks’ gestation.22,26

The most frequent fetal heart anomalies diagnosed atearly echocardiography are summarized in Table 3 (truepositive cases).14,18-21,24-26,34,35,37,39-42,45,46 Note that only themain anomaly for each fetus is presented in the table, eventhough some fetuses had several cardiac anomalies. It shouldbe noted that defects such a small isolated ventricular septaldefect or valvular stenosis are not reported in these studies.Table 4 summarizes the published cases of cardiacanomaly not detected in early pregnancy (false negativecases).14,19-21,24-26,34-37,39-42,45,46

The results of these studies support the use of early fetalechocardiography to detect the majority of major CHD inboth low-risk and high-risk population, during the first andearly second trimester of pregnancy. The cardiac anomaliesdetected at this early stage of pregnancy are mainly defects

Table 1: Results of early fetal echocardiography to diagnose cardiac defects in high-risk population(only series with at least 10 cardiac defects diagnosed)

Author, year Route GA Success Risk N Cases 11-16 ws 20-22 ws

Gembruch, 9314 TV 11-16 90.3% High 114 13 92% 100%Zosmer, 9924 TA 13-17 — High 323 27 89% 96.3%Simpson, 0025 TA 12-15 98.7% High 229 17 76% 94%Huggon, 0226 TA 10-14 86.8% High 478 68 94% —Haak, 0222 TV 10-13 95.5% High 45 13 54% —Bronshtein, 0220 TV 11-17 >99% High 6175 46 >90% —Comas, 0221 TV 12-17 94.6% High 337 48 79% 96%Lopes, 0339 TV 12-16 94,9% High 275 37 89% —Weiner, 0240 TV 11-14 97% High 392 19 58.3% —Carvalho, 0441 TA 10-16 96% High 230 14 91.3% —McAuliffe, 0542 TV 11-16 95% High 160 20 70% —Smrcek, 0643 TV 11-14 NR High 2165 35 63% —Weiner, 0845 TV 11-14 94% High 200 19 68% —

Route: Main approach; TV: transvaginal; TA: transabdominal; GA: range of gestational age at scan (in weeks); Success: visualizationsuccess rate for the complete early fetal echocardiography; N: total number of pregnancies scanned; Cases: total number of cardiacdefects (pre- and postnatal); 11-16 ws: percentage of the cardiac defects identified at early echocardiography; 20-22 ws: percentage ofthe cardiac defects identified at mid-trimester echocardiography; NR: no reported

Fig. 9: Early fetal echocardiography by 2D and bi-flow in astructurally normal heart. Bi-flow is particularly useful to demonstratethe crossing of the great arteries. Ao: aorta; PA: pulmonary artery

Fig. 10: Early fetal echocardiography by 2D in a structurally normalheart. The short axis view showing an anterior right ventricle and aposterior left ventricle. RV: right ventricle; LV: left ventricle


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involving the four-chamber view, such as large ventricularseptal defects, atrioventricular septal defects andmalformations resulting in asymmetry of the ventricles,indicating that defects solely affecting the outflow tractsare difficult to diagnose in the first trimester of pregnancy.Heart defects diagnosed early in pregnancy tend to be morecomplex than those detected later, with a higher incidenceof associated structural malformations, chromosomalabnormalities and spontaneous abortions. It is widelyaccepted that the spectrum of CHD diagnosed during

prenatal life is different from that observed in postnatalseries, with a higher incidence of associated extracardiaclesions and a significant relationship with chromosomalabnormalities in comparison with postnatal life.3-5,17

Furthermore, when the cardiac defects are detected duringthe early pregnancy, they use to be even more complex,probably corresponding to the most severe spectrum of thedisease21,25,26 and use to cause more severe hemodynamiccompromise in the developing fetus. A common finding isthe presence of an hygroma or hydrops associated with

Table 2: Detection rate of cardiac defects at early ultrasound to screen for congenital malformations in low-risk population

Author, year GA Success Risk Normal Cases 11-16 ws(%) 20-22 ws(%)

Achiron, 9418 13-15 98% Low 660 6 50 50Hernadi, 9734 12 — Low 3991 3 33 100D’Ottavio, 9735 13-15 — Low 3490 8 25 80Yagel, 9717 13-16 99% Low 6924 66 64 81Economides, 9836 12-13 — Low 1632 3 0 33Whitlow, 9937 11-14 — Low 6443 10 40 60Guariglia, 0038 10-16 — Low 3592 11 18 56Rustico, 0019 13-15 <50% Low 4785 41 10 32Bronshtein, 0220 11-17 99% Low 30148 127 97 99Becker, 0644 11-14 — Low 3094 86 84.2 94Volpe, 1146 11-14 — Low 4445 42 62 93

GA: range of gestational age at scan (in weeks); Success: visualization success rate for the extended cardiac examination (4 chamber +outflow tracts); Normal: Total number of pregnancies screened; Cases: total number of cardiac defects (pre- and postnatal); 11-16 ws:percentage of the cardiac defects identified at early scan; 20-22 ws: percentage of the cardiac defects identified at mid-trimester scan

Table 3: Fetal heart anomalies diagnosed at early echocardiography (true positive cases at early fetal echocardiography)

True + A B C D E F G H I J K L M N O P Q R S Overall

Gembruch, 9314 — — — 6 — 1 1 — — — 2 — 2 — — — — — — 12Zosmer, 9924 — — 3 3 2 1 4 2 3 1 — — 4 — — — 1 — — 24Rustico, 0019 — — — 2 — 1 1 1 — — — — — — — — — — — 5Simpson, 0025 — — 3 2 — — — 3 2 — — — 2 1 — — — — — 13Huggon, 0226 — — 5 29 — 12 9 1 — — 1 — — 1 1 1 — — — 60Bronshtein,0220 4 1 4 13 2 9 25 — 31* 22 5 — 18 — 17 3 2 13 — 169Comas, 0221 — — 4 8 — 10 4 1 3 — 2 2 1 — — 3 — — — 38Achiron, 9418 — — — 2 — — — — 2 — 1 — — — 1 1 1 — — 8Hernadi, 9734 — — — — — 1 — — — — — — — — — — — — 1D’Ottavio, 9735 — — — — — — 2 — — — — — — — — — 2 — — 4Whitlow, 9937 — — — — 1 — 1 — — — — — — — — 1 — — — 3Rustico, 0019 — 1 — — — — 2 — 1 — — — — — — — — — — 4Lopes, 0339 — — 2 6 — 11 5 1 1 1 1 3 2 — — — — — — 33Weiner, 0240 — — — 4 — 1 1 — 2 2 2 — — — — — — — 1 13Carvalho 0441 — — 1 3 1 1 1 2 — 1 — — — 3 — 1 — — — 14McAuliffe, 0442 — — — — 2 2 2 — — — — 1 — 2 — 2 1 — 2 14Weiner, 0845 — — — 4 — 1 2 — 2 1 2 — — — — — — — 1 13Volpe, 1146 — — 1 7 — 4 7 1 2 1 — — 2 — — — — — 1 26

Overall 4 2 23 89 8 59 67 12 49 29 16 6 31 7 19 12 7 13 5 374

A: abnormal venoatrial connections; B: atrial septal defects; C: tricuspid atresia or dysplasia; D: atrioventricular septal defect;E: single ventricle; F: ventricular septal defects; G: aortic atresia, aortic stenosis, mitral stenosis, hypoplastic left heart; H: pulmonaryatresia or stenosis; I: tetralogy of fallot; J: transposition of great arteries; K: truncus; L: double outlet right ventricle; M: aortic archanomalies; N: isomerism; O: myocardiopathy; P: ectopia cordis; Q: complex cardiac defect, others; R: vascular ring; S: hypoplastic rightheart; *This series includes cases with tetralogy of fallot and double outlet right ventricle

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CHD, whereas this is not so when the diagnosis is donelater in pregnancy.1,5,21 As a result, many of these fetusesare not going to survive long into the second trimester, butthis does not argue against early diagnosis. Indeed, whenthe intrauterine demise of the fetus occurs days or weeksbefore the delivery, the pathological examination is certainlymore difficult to perform. All these considerations shouldbe taken into account when counseling the parents aboutcomplex CHD.

We have previously published our experience in the firstmulticenter trial in early fetal echocardiography performedin Spain21 (Figs 11 to 15). In accordance with other studies,

this experience stresses the usefulness of early echocardio-graphy when performed by expert operators on fetusspecifically at risk for cardiac defects. Our review of theseadditional 48 cases contributes to the expanding literatureon the ability of transvaginal ultrasonography to detect fetalheart defects in early pregnancy. Figures 16 to 23 showearly fetal echocardiography in structurally abnormal heart.

ADVANTAGES AND LIMITATIONS

The first benefit of performing early fetal echocardiographywould be an early reassurance of normality in order torelieve anxiety and reduce emotional trauma to the parents

Figs 11A and B: Early fetal echocardiography by 2D in a structurally normal heart. The left sagittal view of ductal (A) and aortic arch(B). RV: right ventricle; LV: left ventricle; PA: pulmonary artery; DA: ductus arteriosus; DAo: descending aorta; AAo: ascending aorta

Table 4: Fetal heart anomalies not detected at early echocardiography (false-negative cases at early fetal echocardiography)

False – A B C D E F G H I J K L M N Overall

Gembruch, 9314 — — — — 1 — — — — — — — — — 1Hernadi, 9734 1 — — 1 — — — — — — — — — — 2D’Ottavio 9735 1 — — — 3 2 — — 1 — — — — — 7Economides, 9836 1 — — — — 1 1 — — — — — — — 3Whitlow, 9937 2 1 — — — 2 1 1 — — — — — — 7Zosmer, 9924 — — — — 1 1 — — 1 — — — — — 3Rustico, 0019 1 — — — 4 1 2 — 1 — — — — — 9Simpson, 0025 3 — — — — — — — — 1 — — — — 4Comas, 0221 4 1 — — 3 1 1 — — — — — — — 10Huggon, 0226 2 — 2 — — 1 — — 2 — — — — — 7Bronshtein, 0220 — — — — 1 1 — 1 1 — — — — — 4Lopes, 0339 3 — — — — — — 1 — — — — — — 4Weiner, 0240 3 — — — 1 — 1 — — — — — 1 — 6Carvalho 0441 1 — — — — — — — — — — 1 — — 2McAuliffe, 0442 3 — — — — — — 2 — 1 — — — — 6Becker, 0644 — — — — 1 — 1 2 — — 1 — 1 1 7Weiner, 0845 2 — — — 1 — 1 — 1 — 1 — — — 6Volpe, 1146 7 1 — — 2 1 1 1 1 — — 1 — — 15

Overall 34 3 2 1 18 11 8 8 8 2 2 2 2 1 61

A: ventricular septal defects; B: atrial septal defects; C: abnormal venoatrial connections; D: tricuspid atresia or dysplasia;E: atrioventricular septal defect; F: aortic atresia, aortic stenosis, hypoplastic left heart; G: tetralogy of fallot; H: transposition of greatarteries; I: aortic arch anomalies; J: myocardiopathy; K: absent pulmonary valve, pulmonary stenosis; L: mitral dysplasia; M: pulmonarystenosis; N: total anomalous pulmonary venous drainage


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Fig. 12: Early fetal echocardiography by 2D in a structurally normalheart. Systemic venous return to the right atrium throws the superiorand inferior vena cava. SVC: superior vena cava; IVC: inferior venacava

Fig. 13: Early fetal echocardiography by 2D and color Doppler in astructurally normal heart. Color Doppler is particularly useful todemonstrate the aortic arch. DAo: descending aorta

Fig. 14: Early fetal echocardiography by 2D and power Doppler.Normal mitral wave flow by power Doppler

Fig. 15: Early fetal echocardiography by 2D and power Doppler.Normal tricuspid wave flow by power Doppler

Figs 16A to E: Atrioventricular septaldefect detected at 13 weeks’ gestation ina fetus affected by cystic hygroma andtrisomy 21. Note the abnormal reversed Awave in the ductus venosus (A). Note theventricular septal defect (B and C). D andE illustrate the mitral and tricuspid diastolicflow respectively

Atrioventricular septal defect

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Figs 18A to C: Atrioventricular septal defect with unbalanced right ventricle dominance and double outlet right ventricle at 15 weeks’gestation. Note: The abnormal reversed A wave in the ductus venosus (A), the color Doppler flow through the atrioventricular septaldefect with atrioventricular regurgitation (B) and the double outlet right ventricle with unbalanced right ventricle dominance (C)

Figs 19A to E: Hypoplastic left heart at 14 weeks’ gestation. Note: The identification of markers of CHD: increased nuchal translucency(A) and abnormal ductus venosus flow (B). Reverse flow at the 3 vessels view (C), hypoplastic left ventricle with reverse flow with colorDoppler (D), reversed flow in aortic arch (E)

Figs 17A to E: Tetralogy of fallot detectedat 16 weeks’ gestation. Note the reverse awave in ductus venosus flow (A). Note theleft ventricular septal defect (B), thedominance of the aorta compared with thesmall pulmonary artery at the 3 vessels viewin the upper mediastinum (C), cardiacdeviation (D) and aortic misalignment (E)


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Figs 20A to C: Hypoplastic left heart and aortic stenosis at 17 weeks’ gestation in a Turner syndrome. Note: The left cardiac axisdeviation (A), the severe reduction of the aortic outflow tract compared to the main pulmonary artery (B) and the opposite color flow in theV sign at the upper mediastinum level (C)

Figs 21A to C: Myocardial fibroelastosis and stenotic atresia at 12 weeks’ gestation. Note: Aortic reverse flow in3 vessels view (A), mitral regurgitation (B) and myocardial fibroelastosis (C)

Figs 22A to D: Myocardial fibroelastosis and stenotic atresia at 12 weeks’ gestation. Note: The mitral regurgitation and thefibroelastosis (A) and the reverse flow in pulmonary veins (B), myocardial fibroelastosis in 2D (C) and color Doppler (D)

at high-risk for CHD. Early prenatal diagnosis of CHD willallow us to optimize the genetic counseling to the parentsby permitting further testing such as fetal karyotyping andin those cases with severe defects it may provide the parentswith the option of an earlier and safer TOP.13,14,17 In selectedcases, there is the possibility of pharmacologic therapy.

Furthermore, the correct timing and place for delivery maybe planned and arranged well in advance.

However, there are certain disadvantages of the earlyscanning which reduce its diagnostic accuracy comparedwith the conventional examination at 20 to 22 weeks’gestation.1,5,13,14,17 The transvaginal technique requires a

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substantial amount of operator experience, yet it cannot belearned from the second trimester examination as the earlytransabdominal scan. Unfavorable fetal position or limitedangles of insonation due to the less mobile capacity of thetransvaginal probe may not overcome. Also, spatialorientation can be challenging by the transvaginal scan. Insuch cases, we recommend a transabdominal scan that willhelp us to quickly asses the situs and obtain a good spatialorientation. The small size of the fetal heart is an importantlimiting factor to obtain an optimal sonographicvisualization, and also to obtain a successful pathologicalexamination, particularly before the 13th week of gestation.At 13 to 14 weeks of gestation the transverse diameter ofthe heart at the four-chamber view ranges between 5 and8 mm, and the great artery diameter at the level of thesemilunar valves ranges between 0.8 and 1.8 mm.5

Moreover, this exploration is more time consuming andrequires a high level of training of the examiner. Finally,the biggest disadvantage of first-trimester echocardiographyis the later manifestation of structural and functional changesin some CHD. Some cardiac lesions are progressive innature, such as mild pulmonary and aortic stenosis or

coarctation and even hypoplastic left heart syndrome. Someobstructive lesions, as a result of a reduced blood flow, mayincrease the severity of the lesions, resulting in a restrictedgrowth in chambers or arteries. This may be the biggestdisadvantage of performing the early scan. Progressionusually is toward a more severe form of lesion that may besometimes only discernible in the second or even in thethird trimester, although in some rare cases a regression toa less severe form may be observed. In this sense, the falsenegative cases published in literature are particularlyinstructive demonstrating these limitations. Anotherdisadvantage of early fetal echocardiography is the possibledetection of defects that could resolve spontaneously in laterpregnancy, such as muscular ventricular septal defects,resulting in unnecessary anxiety in the parents.

Therefore, a normal early examination does not precludea subsequent abnormal heart development at the secondtrimester ultrasound, or even in the third trimester or thepostnatal period. After a normal early fetal echocardio-graphy, a conventional transabdominal echocardiographyat 20 to 22 weeks of gestation is strongly recommended.

Figs 23A to D: Tetralogy of fallot at 16 weeks. Note: Abnormal ductus venosus flow (A), the ventricular septal defect (B), aortamisalignment and reverse flow in pulmonary artery (C) and dilatation of the aorta (D)


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PATHOLOGICAL CONFIRMATION

Pathological confirmation in the case of an early TOP orperinatal death is particularly important in those areas whereultrasound diagnosis is most challenging. Only a completediagnosis will make an individual genetic counselingpossible and will validate the accuracy of early fetalechocardiography as a diagnostic technique. Therefore, weadvocate that a precise pathological report have to becompulsory for an adequate assessment of the reliability ofearly fetal echocardiography. This is still a major drawbackin most of the studies.1,5,21,26

TOP is an option only before 22 weeks of gestation inour country. Whenever a termination takes place, it is ofvital importance to obtain permission for autopsy in orderto confirm the diagnosis and to search for any otherassociated malformations. Ideally this should be performedby a pathologist who is familiar with the small size of thespecimen and with special examination techniques such asdissection microscopy.5,21,22 Current methods of terminatingearly pregnancies others than using prostaglandins are lessrecommended because do not usually allow the retrieval ofsuitable specimens for appropriate examination to correlateultrasound and pathological findings. This method allowsa more gentle extraction of the embryo or fetus so that apathological examination for verification of the prenatallydiagnosed malformation can be performed. A pathologicalinvestigation after TOP following the diagnosis of a CHDshould be always recommended, preferably in referrallaboratories, being of paramount importance to validateearly echocardiography. In particular semilunar valve andaortic arch defects are usually underdiagnosed. We areaware of some cases in which Doppler findings, suchturbulent flow and very high velocities, are more reliableto diagnose valve stenosis than pathological examination,even during the second trimester. Indeed, this is a problemand a major challenge not only for ultrasonographers butalso for pathologists.

INDICATIONS OF EARLY FETALECHOCARDIOGRAPHY

Since most CHD are detected in low-risk pregnancies, andknowing the high prevalence of heart defects in anonselected population (incidence of CHD in low-riskpopulation 1\238),20 some authors suggest that an earlydetailed cardiac examination should be performed in allpregnant women.17,20 Indeed, very few cardiac defects havebeen identified in the pregnancies in which a family historywas the main indication for the early fetal echocardiography,which is consistent with the recurrence rate of 2 to 3% for

siblings. The main value of the early scan in such family-risk cases lies in the reassurance that it gives to the parents.As we have previously stated, in most of the studies theearly echocardiography is somewhat less reliable and mayresult in a higher false-negative and false-positive resultsin comparison with the 20 to 22 weeks transabdominalechocardiography. Besides, early echocardiography is mosttime-consuming and requires a high level of expertise ofthe examiner. Therefore, it is difficult to offer this scan as ascreening test to the general population. In this context, theidentification of a high-risk collective is of paramountimportance.

Currently, the importance of the aforementionedlimitations of early fetal cardiac examination justifiesrestriction of its use to fetuses at high-risk of having cardiacanomalies.5,10,14,18,21,22,26,47

The indications proposed for early fetal echocardio-graphy are as follows:• Increased nuchal translucency (>95th or 99th percentile)

is the main indication of referral in all recently reportedstudies

• Abnormal ductus venosus blood flow, regardless themeasurement of the nuchal translucency

• Fetuses affected by other structural malformations:Hygroma, hydrops, omphalocele, situs inversus,arrhythmia

• Monochorionic placentation in multiple gestation• Suspected cardiac anomalies at screening ultrasound• Pregestational diabetes of the mother• High-risk family, with a previously affected child, a first-

degree relative affected by a congenital heart disease ora genetic disease in which CHD are common

• Women at high-risk of chromosomal abnormalitydeclining invasive test for karyotyping

• Pregnancies affected by a chromosomal abnormality.Currently, as long as the sensitivity, specificity and

predictive value of early echocardiography are still unclear,this examination should be generally reserved for patientsat high-risk for CHD. However, only the accumulation ofresults from carefully collaborative studies as the presentseries will clear define the role of early transvaginalechocardiography.

CONCLUSION

Fetal echocardiography performed by expert operators isreliable for an early reassurement of normal cardiacanatomy.1. Transvaginal sonography enables good visualization of

fetal heart earlier in gestation. The four-chamber view

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and the extended examination to the great vessels canbe imaged in almost 100% at 13 to 14 weeks of gestation.Less than 5% of patients will need a repeated scanbecause of inadequate visualization.

2. The combination of transvaginal and transabdominalroutes and the application of color Doppler enhancevisualization.

3. Most CHD are detected in low-risk population. As wecan not perform a targeted fetal echocardiography as ascreening test, we need to improve the identification ofhigh-risk group pregnancies. Increased nuchaltranslucency at 10 to 14 weeks’ scan and, may be, ductusvenosus blood flow assessment seem to be the newestand most promising risk factors for fetal CHD, and maybe particularly useful during the first trimester.

4. Currently, early fetal echocardiography should beoffered to high-risk pregnancies. Some authors advocateroutine early extended cardiac examination in low-riskpregnancies. At present, as long as the sensitivity,specificity and predictive value of early echocardio-graphy is still unclear, this examination should begenerally reserved for patients at high-risk for CHD.

5. Whenever a normal heart is diagnosed in the early scan,it has to be supplemented with the conventional trans-abdominal examination at 20 to 22 weeks’ gestation.Fetal echocardiography performed by expert operators

is reliable to diagnose most major structural heart defectsin the first and early second trimester of pregnancy.1. Cardiac defects diagnosed early in pregnancy tend to

be more complex than those detected later on and use tocause more severe hemodynamic compromise in thedeveloping fetus.

2. Many CHD can be detected at the beginning of thesecond trimester.

3. The incidence of associated structural malformations,chromosomal abnormalities and spontaneous abortionsis significantly high.

4. A complete work-up including pathological andkaryotype evaluation should be warranted in order toprovide parents with a proper genetic counseling, whichis extremely difficult to obtain if spontaneous loss ofthe pregnancy occurs.

5. The small size of specimens at this time of gestationrenders pathological examination difficult and requireshigh expertise and careful inspection, irrespective of thetechnique used for termination.

6. Clinical follow-up in the neonate and postmortemexamination if TOP is undertaken are essential to assessthe actual role of early fetal echocardiography.

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ABOUT THE AUTHORSCarmina Comas Gabriel

Fetal Medicine Unit, Obstetrics Service, Department of Obstetrics,Gynecology and Reproduction Medicine, Hospital UniversitarioQuiron Dexeus, Barcelona, SpainCorrespondence Address: C/ Gran Via de Carles III, 71-75, Barcelona08028, Spain, Phone: 0034 932274706, Fax: 0034 934187832e-mail: [email protected]

Pilar Prats Rodríguez

Fetal Medicine Unit, Obstetrics Service, Department of Obstetrics,Gynecology and Reproduction Medicine, Hospital UniversitarioQuiron Dexeus, Barcelona, Spain

fetal ecocardiography text

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