First and early second trimester fetal heart screening

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First and early second trimester
fetal heart screeningSimcha Yagel, Sarah M. Cohen and Baruch Messing
Purpose of review

This review describes the recent advances in timing and

effectiveness of first and early second trimester fetal

echocardiography screening.

Recent findings

Fetal echocardiography can now be reliably performed from

11 weeks’ gestation owing to improvements in ultrasound

transducers and processors. Three-dimensional and four-

dimensional ultrasound modalities in image acquisition and

postprocessing analysis, including spatio-temporal image

correlation, rendering three-dimensional power Doppler

and high definition power flow Doppler, and B-flow have

further improved our capabilities in this area. Fetal nuchal

translucency measurement screening programs create a

new population of at-risk pregnancies that will be referred

for early fetal echocardiography. The majority of congenital

heart defects, however, still occur in low-risk patients.

Improved technology has lowered the gestational age at

which fetal cardiac anatomy scanning can be reliably

performed by properly trained and experienced examiners.

Summary

Early fetal echocardiography can be offered as a screening

examination to at-risk and low-risk patients, with the proviso

that it be repeated following screen-negative scans at

mid-gestation to exclude later developing lesions.

Keywords

developmental malformations, fetal echocardiography, fetal

heart, first trimester, four-dimensional ultrasound, prenatal

diagnosis, prenatal screening, spatio-temporal image

correlation, three-dimensional ultrasound

Curr Opin Obstet Gynecol 19:183–190. � 2007 Lippincott Williams & Wilkins.

Department of Obstetrics and Gynecology, Hadassah-Hebrew University MedicalCenters, Jerusalem, Israel

Correspondence to Professor Simcha Yagel, Department of Obstetrics andGynecology, Hadassah-Hebrew University Medical Centers, PO Box 24035, Mt.Scopus, Jerusalem, IsraelTel: +972 2 5844111; fax: +972 2 5815370; e-mail: [email protected]

Current Opinion in Obstetrics and Gynecology 2007, 19:183–190

Abbreviations

3VT th

opy

ree vessel and trachea
CHD c ongenital heart disease STIC s patio-temporal image correlation
� 2007 Lippincott Williams & Wilkins1040-872X

right © Lippincott Williams & Wilkins. Unauth

IntroductionHigh-frequency, high-resolution transvaginal and trans-

abdominal probes, along with substantial improvements

in magnification imaging and signal processing, have

dramatically increased our ability to visualize the devel-

oping fetal heart during the first and early second tri-

mesters of pregnancy, allowing detailed investigation of

fetal cardiac anatomy and diagnosis of cardiac defects

in that period.

Early fetal echocardiography has known potential

benefits: early confirmation of normal cardiac anatomy

in high-risk patients may relieve considerable anxiety;

and earlier diagnosis may allow for safer termination of

pregnancy or a longer time frame for fetal karyotyping

and genetic counseling for parents with affected fetuses.

Prompt initiation of pharmacological therapy or in certain

cases fetal surgical interventions can reverse or improve

conditions amenable to such interventions and ultimately

impact on prognosis. Prenatal diagnosis can improve

prognosis for surgical palliation or correction postnatally,

by improving neonatal conditions for surgery [1–3]. The

seminal study by Bonnet et al. [1] shows the effectiveness

of prenatal heart screening in improved neonatal

outcome.

Early fetal heart scanning has been performed since the

early 1990s [4–9]. Steady improvement in probes and

the increasing acceptance of the transvaginal approach

have made earlier scanning more widely available and

more feasible.

Early transvaginal and transabdominal sonography have

revealed developing structures once limited to the

embryologist or pathologist. The term ‘embryography’

[10] has been coined in this context. Embryonic devel-

opment, rather than technical obstacles, will eventually

be the limiting factor in early imaging and detection

of structural cardiac anomalies. The fetal heart is gen-

erally completely formed and the four-chamber structure

established by about 56 days after fertilization [11].

Technique and guidelinesGuidelines for the performance of fetal echocardiography

have been proposed by the International Society of

Ultrasound in Obstetrics and Gynecology [12�]. These

screening guidelines outline the elements required for a

complete fetal echocardiography examination. The

examination should include the following: general obser-

vation of normal cardiac situs, axis and position; that the

orized reproduction of this article is prohibited.

183

mailto:[email protected]

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184 Prenatal diagnosis

Figure 1 The five short-axis views for optimal fetal heart screen-

ing

The color image shows the trachea, heart and great vessels, liver andstomach, with the five planes of insonation superimposed (SVC, superiorvena cava; AO, aorta; T, trachea; DA, ductus arteriosus, PA, pulmonaryartery). Polygons show the angle of the transducer and are assigned tothe relevant gray-scale images. (I) The most caudal plane, showing thefetal stomach, cross section of the abdominal aorta, spine and liver.(II) The four-chamber view of the fetal heart, showing the right and leftventricles and atria, foramen ovale and pulmonary veins to the right andleft of the aorta. (III) The ‘five-chamber’ view, showing the aortic root, leftand right ventricles and atria and a cross section of the descendingaorta. (IV) The slightly more cephalad view showing the main pulmonaryartery and the bifurcation of left and right pulmonary arteries and crosssections of the ascending and descending aortae. (V) The three vesseland trachea plane of insonation, showing the pulmonary trunk, proximalaorta, ductus arteriosus, distal aorta, superior vena cava and the trachea[14]. Reproduced from Yagel et al. [13] with permission.

heart occupies one-third of the thorax, with the majority

of the heart in the left chest; and four cardiac chambers

should be present and no pericardial effusion or hyper-

trophy observed. In addition, the atria should be approxi-

mately equal in size with the foramen ovale flap in the left

atrium and the atrial septum primum present. The ven-

tricles should be about equal in size with no cardiac wall

hypertrophy. The moderator band should be observed at

the right ventricular apex, and the ventricular septum

should be examined apex to crux as intact. Both atrio-

ventricular valves should be observed to open and move

freely, the tricuspid valve leaflet inserting on the septum

closer to the cardiac apex compared with the mitral

valve.

The ‘extended basic’ fetal echocardiography examin-

ation proposed in the International Society of Ultrasound

in Obstetrics and Gynecology guidelines includes all of

the above and in addition examination of the right and

left outflow tracts. The examination should demonstrate

that normal great vessels of approximately equal size

cross each other at right angles from their origins as they

exit from their respective ventricular chambers [12�].

We recommend performance of early fetal echocardio-

graphic examination, whether transabdominally or trans-

vaginally, based on five transverse planes [13]. Our

approach is based on the established segmental approach

to cardiac evaluation, recently succinctly and cogently

elucidated as applied to the prenatal echocardiographic

diagnosis of congenital heart defects by Carvalho et al.[14]. This methodology streamlines visualization of the

planes that must be evaluated to meet the requirements

of the International Society of Ultrasound in Obstetrics

and Gynecology guidelines.

Examination begins from a transverse view of the fetal

upper abdomen, showing the spine, stomach and inferior

vena cava (Fig. 1). This view establishes fetal orientation

and is important for evaluating normal situ. Moving the

transducer cephalad, the next plane is the four-chamber

view. The third plane is sometimes called the five-

chamber view. Here the aortic root is visualized. The

fourth transverse plane reveals the bifurcation of the

pulmonary arteries. The three vessel and trachea

(3VT) plane of insonation is the fifth short-axis view in

fetal echocardiography. The 3VT is the most cephalad

transverse view, visualized on a plane crossing the fetal

upper mediastinum, and is easily obtained by moving the

transducer cephalad and slightly oblique from the four-

chamber view. The 3VT demonstrates the main pulmon-

ary artery in direct communication with the ductus

arteriosus. A transverse section of the aortic arch is seen

to the right of the main pulmonary artery and ductus

arteriosus. Cross sections of the superior vena cava, and

posterior to it the trachea, are visualized [13] (Fig. 1).

opyright © Lippincott Williams & Wilkins. Unautho

Venous system

Examination of the fetal venous system is important for

comprehensive understanding of the fetal cardiovascular

system, and indispensable in complete fetal echocardio-

graphy. The venous system develops from three paired

veins. At the end of the first trimester several abnormal

connections of the fetal venous system are recognized

and are classified as follows: pathologies of the cardinal

vein, umbilical veins, vitelline veins and anomalous

pulmonary venous connections. At the time of early fetal

cardiac scanning the venous system is also amenable to

evaluation; anomalies arising from the fetal central veins

and umbilical–portal system have also been described

[15�,16,17]. These anomalies are often associated with

cardiac and extracardiac anomalies, and may impact

significantly on prognosis.

rized reproduction of this article is prohibited.

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Fetal heart screening Yagel et al. 185

Figure 2 The five chamber view (the third plane) [14] of the fetal

heart at 13 weeks derived from a spatio-temporal image corre-

lation acquisition

(a) The five chamber view (the third plane) of the fetal heart at 13 weeks (inthe upper left frame) derived from a spatio-temporal image correlationacquisition. RA, right atrium; LA, left atrium; RV; right ventricle; LV, leftventricle;PV,pulmonaryveins;dAodescendingaorta;LVOT, leftventricularoutflow tract. Note the reference dot placed on the ascending aorta; thereference dot position is stable in all three orthogonal views. (b) Thelongitudinal frame is seen: note the descending aorta in the long-axis view.

Figure 3 Spatio-temporal image correlation acquisition with

color Doppler at the three vessels and trachea plane in a fetus

diagnosed with severe tetralogy of Fallot with pulmonary atre-

sia at 14 weeks

The three vessels and trachea plane clearly shows the dilated aorta (Ao)with antegrade flow, the narrow main pulmonary artery (MPA) withreverse flow, antegrade flow in the azygos vein (Az) and the trachea(T). The superior vena cava (SVC) is visible as it drains the azygos vein.

Scanning approach

The transvaginal approach in fetal echocardiography

requires a substantial amount of experience. Certain

views may be limited by the fixed linear axis of the

transvaginal probe during the examination, and fetal

position often dictates the views that can be imaged.

Consequently, certain maneuvers and manipulations may

be needed to optimize results in a minimal examination

time. Nevertheless we continue to advocate the trans-

vaginal as superior to the transabdominal approach

for early fetal echocardiography owing to the higher

frequency and resolution of transvaginal ultrasound

probes. This was shown in a recent study comparing the

two approaches in early fetal cardiac studies [18�].

Emerging three-dimensional and four-dimensional

techniques in fetal cardiac scanning

The past several years have witnessed dramatic devel-

opments in three-dimensional and four-dimensional fetal

cardiac scanning. Spatio-temporal image correlation

(STIC) is a new three-dimensional modality for gated

volume acquisition. The methodology of STIC acqui-

sition and manipulation of the volume dataset have been

comprehensively described by Goncalves et al. [19��].

STIC technology acquires a volume of data from the fetal

heart and displays a reconstructed single cardiac cycle

[20–22]. A wedge-shaped scanning volume is acquired

from the fetal upper abdomen moving cephalad through

the fetal thorax by tilting the transducer through approxi-

mately 15–258; the five planes are acquired in a single

volume set. Acquisition speed varies from 7.5 to 15 s, and

is preferably performed with the fetus in a quiet state.

Slower scanning provides higher resolution but allows the

fetus more opportunity to move or breathe and compro-

mise scan quality. Thus younger fetal age shortens

examination time, making STIC an excellent tool for

three-dimensional–four-dimensional fetal heart scanning

in the first and early second trimesters (Figs 2 and 3).

Other researchers [23–26] have advocated varying meth-

odologies to optimize analysis of the STIC volume set to

obtain the scanning planes necessary for complete

fetal echocardiography.

Rendering capabilities in three-dimensional–four-

dimensional fetal echocardiography applications can be

employed to visualize virtual planes of the fetal heart that

may not be readily accessible in two-dimensional cardiac

scanning. Rendering modality is applied to an acquired

volume scan; the operator can move to any plane within

the volume. If a STIC volume was acquired, the operator

can navigate within the volume spatially, and a given

plane may be imaged at any stage of the cardiac cycle.

These combined modalities have been applied to the

visualization of ‘virtual planes’ of the interventricular

septum, interatrial septum and the coronal atrioventri-

opyright © Lippincott Williams & Wilkins. Unauth

cular plane of the annuli of the cardiac valves, and have

been shown to have added value in the diagnosis of

ventricular septal defect, restrictive foramen ovale, align-

ment of the ventricles and great vessels, and evaluation of

the atrioventricular valves [27�] (Fig. 4).


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Figure 4 Normal four-chamber view of the fetal heart at

14 weeks derived from spatio-temporal image correlation acqui-

sition (a) and the same plane in rendering mode (b)

Note that the rendering plane displays texture and depth of the imagethat are lacking in the two-dimensional image on the left. (Right– leftorientation of the two images is reversed.)

Figure 5 Three-dimensional high definition power flow Doppler

of the normal heart and vascular anatomy in a 14 week fetus

Three-dimensional high definition power flow Doppler of the normal heartand vascular anatomy in a 14-week fetus showing the umbilical vein (UV),ductus venosus (DV), inferior vena cava (IVC), celiac artery (CA),descending aorta (Ao) and pulmonary veins (PV). Note that Dopplerflow directional information is reversed: the image was rotated in post-processing to heart-superior orientation while in the original scanningplane the fetus was in the vertex position.

Three-dimensional power Doppler provides three-

dimensional reconstruction of blood vessels based on

Doppler shift technology. Three-dimensional power

Doppler isolates and allows examination and evaluation

of the vascular tree; visualization of blood vessels using

this mode aids in the understanding of normal and

anomalous anatomy [15�,28,29]. It relieves the operator

from the necessity of visualizing the idiosyncratic course

of an anomalous vessel from a series of two-dimensional

images; the modality can provide a complete three-

dimensional reconstruction of the vessels under study

[15�] Most recently, high definition power flow Doppler

has been added to the technologies available to study

blood flow. It is adaptable to both static three-dimensional

and gated four-dimensional acquisition, and provides

high-resolution bidirectional color mapping (Fig. 5).

Inversion mode is yet another three-dimensional–four-

dimensional imaging modality that reverses the appear-

ance of echogenic (gray) and fluid-filled (black) voxels of

a scanned volume. This modality has been shown to be

useful in producing digital casts of blood vessels and the

cardiac chambers [29–32]. In addition, it has been

applied to quantification of ventricular [33] and other

volumes, which in turn may aid in heart function evalu-

ation (Fig. 6).

B-flow modality directly depicts blood echoes in gray-

scale presentation. As applied to fetal echocardiography,

this allows for evaluation of blood flow in the great

vessels, venous return or filling of the cardiac chambers

(Fig. 7). B-flow modality is the most sensitive for volume

measurement as it directly demonstrates blood flow and a

portion of the lumen of the target vessel [30,34].

Tomographic ultrasound imaging display mode com-

bined with STIC or static three-dimensional imaging is


a new analysis function that allows sequential planes of

the volume to be displayed on the screen simultaneously.

In fetal echocardiography, the operator can view

the several segments of the fetal heart scan together

[35–37]. Figure 8 shows a tomographic ultrasound

imaging display at the 3VT plane in a 14-week fetus

diagnosed with hypoplastic left heart.

FeasibilitySince the studies first published on transvaginal echo-

cardiographic diagnosis of congenital heart disease

(CHD) in the early 1990s [4–9] the field has seen

continuous improvement in probes and equipment,

and progressively earlier ages at diagnosis. Improvement

in abdominal probes has allowed for ever-earlier trans-

abdominal scanning. Several research teams have studied

the feasibility of early fetal echocardiography, using

either the transabdominal or transvaginal approach

(or both), to evaluate from what gestational week fetal

echocardiography may be reliably performed [16,38��,

39�,40–44].

Our center’s experience with early transvaginal cardiac

scanning has been favorable: we find that the full cardiac

anatomy is discernible in 95% of cases at 11–12 weeks,

and in 100% at 13–15 weeks’ gestation, with favorable

fetal lie.


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Figure 6 Inversion mode applied to a normal fetal abdomen and

umbilical vein at 15 weeks (a) and a case of persistent right

umbilical vein at 15 weeks (b)

The persistent right umbilical vein (UV) is seen coursing right of the gallbladder. Note that the fluid-filled stomach (St) and gall bladder (GB)appear white in this mode while surrounding normally echogenic tissuenow appears black. DV, ductus venosus.

Figure 7 Anterior view of a normal heart fetal heart at 14 weeks

scanned in B-flow modality, showing the brachocephalic trunk

(BT), the left common carotid (LCC) and the left subclavian

artery (LSA) projecting from the aortic arch (AoA)

The inferior vena cava (IVC) is indicated.

Figure 8 Tomographic ultrasound imaging displays a number of

sequential parallel planes of the region of interest simul-

taneously

The upper panel (a) shows the acquired volume in the far left, with theplanes shown to the right marked with white lines. The green asteriskmarks the zero or ‘home’ plane; others are marked sequentially. In thiscase of hypoplastic left heart at 14 weeks, the upper panel shows theheart in diastole with normal filling on the right and absent on the left. Thelower panel (b) shows the heart in systole with ejection from the rightventricle but none from the hypoplastic left ventricle.

We analyzed over 6000 cases that underwent early

(13–16 weeks) transvaginal fetal echocardiography

repeated transabdominally at mid-trimester and com-

pared them with more than 15 000 patients that were

scanned only at mid-trimester. We found that transvagi-

nal sonography was feasible for early second-trimester

fetal echocardiography and approached the sensitivity of

transabdominal sonography at mid-trimester [45].

Most recently, Smrcek et al. [18�] compared the two

approaches. They showed that while complete cardiac

evaluation was impossible at 10 weeks’ gestation, it could

be reliably performed by 12 weeks [18�].

Accuracy of early fetal echocardiographyAs early fetal echocardiography has been used in more

centers, data have been accrued on the accuracy of

these programs. In our study [45], 42 malformations

(64%) were detected at the first transvaginal sonography

examination, and 11 (17%) only at mid-trimester, while

three additional anomalies (4%) were found during the


third trimester, and 10 malformations (15%) postnatally.

In the mid-trimester group, 80 malformations (78%) were

detected at the initial transabdominal sonography scan,

and seven more (7%) at the third trimester scan whereas


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15 (15%) were diagnosed postnatally. Overall, 85% of the

affected babies were diagnosed prenatally. The majority

of missed lesions belonged to the category of develop-

mental CHD. This study demonstrated the most import-

ant proviso to early fetal heart screening: the necessity of

repeating examinations later in pregnancy to exclude

developmental CHD [45].

Becker and Wegner [38��] evaluated 3094 fetuses at

11–14 weeks’ gestation from a medium-risk population.

The prevalence of CHD in this population was 1.2%, and

the detection rate of major cardiac anomalies at the early

scan was 84%; the detection rate was increased when

nuchal translucency measurement was �2.5 mm.

Smrcek et al. [39�] evaluated the detection rate of early

fetal echocardiography and the in-utero development

of CHD. A total of 2165 cases were analyzed that under-

went fetal echocardiography between 11 and 14 weeks’

gestation. Twenty cases were diagnosed during the early

scan, an additional nine in the second and another two in

the third trimester, for a cumulative detection rate of

87%. Six cases were detected postnatally. The authors

concluded that early fetal echocardiography is feasible

but must be followed by mid-trimester scanning [39�].

McAuliffe et al. [40] studied fetuses referred for fetal

echocardiography from 11–15þ6 weeks’ gestation, and

repeated the scans at 18 weeks. They found that overall,

early scans were feasible 95% of the time. In this referral

cohort, 14/20 cardiac defects were identified in the earlier

scans while six more were detected at the later scans,

giving a sensitivity and specificity of early fetal echocar-

diography of 70% and 98%, respectively [40].

In contrast with these studies, Westin et al. [46] random-

ized over 39 000 women to receive either a 12-week or an

18-week targeted anomaly scan, with fetal echocardio-

graphy when indicated according to findings in the

anomaly scan. They reported a detection rate of 11%

in the 12-week scan group and 15% in the 18-week group

[46].

Embryonic and fetal heart rateQuantitative evaluation of embryonic and fetal heart rate

(HR) at early fetal echocardiography is both feasible and

important. Early evidence of disordered HR may indicate

poor prognosis. Abnormal HR, especially when observed

with increased nuchal translucency measurement, raises

suspicion of CHD, and may also indicate fetuses at higher

risk for spontaneous abortion [47–49]. Nomograms for

HR aid in the diagnosis of dysrhythmias in the first

trimester; early dysrhythmia is an indication for a detailed

anatomic evaluation [47–48]. Significant fetal tachycardia

(>95% confidence interval) may result in cardiac decom-

pensation, hydrothorax and ascites. We presented a case


of tachycardia diagnosed at nuchal translucency screen-

ing at 13 weeks. The fetal HR responded to treatment

with digoxin and flecainide; hydrops resolved in eight

days [50]. Early diagnosis of fetal tachycardia or arrhyth-

mia is feasible and provides the possibility for medical

treatment for patients who desire to continue the

pregnancy.

Nuchal translucency and the early detection of CHD

Nuchal translucency measurement has been shown to be

an effective tool in the identification of fetuses at high

risk for CHD, with or without associated anatomic or

chromosomal anomaly. Nuchal translucency screening

programs will refer 3–5% of screened patients for com-

prehensive fetal echocardiography. Many groups have

examined the association between nuchal translucency

and cardiac defects. The evidence supports the notion

that the risk of cardiac defect increases as nuchal trans-

lucency thickness rises above the median for gestational

age. In addition, detection rates of CHD seem to increase

as nuchal translucency thickness increases. It is now

feasible to perform fetal echocardiography at the time

of nuchal translucency screening [38��,39�,51–55].

Natural course and in-utero development of CHD

Delayed or missed diagnoses in some cardiac malfor-

mations occur despite detailed echocardiographic exam-

ination by experienced operators. The normal echocar-

diographic appearance of the heart at any gestational age

does not always mean that subsequent development can

be assumed to be normal, and cannot completely rule out

subsequent diagnosis of structural heart disease in late

gestation, or even in the postnatal period [45].

Possible causes for delayed diagnosis fall into three

main categories: limited resolution, which may be

related to both instrumentation and fetal size and

position, progression of lesions in utero, leading to late

onset of CHD, and errors in diagnosis. Isolated ven-

tricular septal defects are perhaps the most commonly

missed CHD during prenatal sonographic scanning, and

this is probably the result of a combination of limited

ultrasound resolution and erroneous diagnosis. Lesions

that may evolve and progress in utero are of major

interest. Examples of such lesions include major vessel

stenosis and ventricular outflow tract obstruction.

Abnormal pressure gradients may result in focal hypo-

plasia and structural remodeling.

Although the fetal heart will have established its four-

chamber structure by 10 gestational weeks [11], an

apparently normal appearance of the heart at early scan

does not exclude major CHD. In addition, serious defects

may develop even after mid-trimester. Follow-up exam-

inations are indispensable and should be performed

throughout pregnancy, especially in high-risk patients.


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ConclusionEarly transvaginal or transabdominal echocardiography

can provide a comprehensive assessment of the fetal

heart by 12–15 weeks’ gestation, and in expert hands

achieve high rates of sensitivity and specificity. Nuchal

translucency screening programs will refer more patients

for fetal echocardiography, increasing the demand for

these services. Practitioners must keep in mind the

developmental nature of many heart defects, and there-

fore the necessity of repeating fetal echocardiography at

mid-trimester.

References and recommended readingPapers of particular interest, published within the annual period of review, havebeen highlighted as:� of special interest�� of outstanding interest

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27

�Yagel S, Benachi A, Bonnet D, et al. Rendering in fetal cardiac scanning: theintracardiac septa and the coronal atrioventricular valve planes. UltrasoundObstet Gynecol 2006; 28:266–274.

Demonstrates one of the most valuable aspects of three-dimensional ultrasound,visualization of virtual planes not accessible in two-dimensional scanning.

28 Lee W, Kalache KD, Chaiworapongsa T, et al. Three-dimensional powerDopplerultrasonographyduringpregnancy.JUltrasoundMed2003;22:91–97.

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31 Lee W, Goncalves LF, Espinoza J, Romero R. Inversion mode: a new volumeanalysis tool for 3-dimensional ultrasonography. J Ultrasound Med 2005;24:201–207.

32 Espinoza J, Goncalves LF, Lee W, et al. A novel method to improve prenataldiagnosis of abnormal systemic venous connections using three- and four-dimensional ultrasonography and ‘inversion mode’. Ultrasound Obstet Gy-necol 2005; 25:428–434.

33 Messing B, Rosenak D, Valsky DV, et al. 3D inversion mode combined withspatio-temporal image correlation (STIC): A novel technique for fetal heartventricle volume quantification (abstract). Ultrasound Obstet Gynecol 2006;28:397.

34 Volpe P, Campobasso G, Stanziano A, et al. Novel application of 4Dsonography with B-flow imaging and spatio-temporal image correlation(STIC) in the assessment of the anatomy of pulmonary arteries in fetuseswith pulmonary atresia and ventricular septal defect. Ultrasound ObstetGynecol 2006; 28:40–46.

35 Goncalves LF, Espinoza J, Romero R, et al. Four-dimensional ultrasonographyof the fetal heart using a novel tomographic ultrasound imaging display.J Perinat Med 2006; 34:39–55.

36 Paladini D, Vassallo M, Sglavo G, et al. The role of spatio-temporal imagecorrelation (STIC) with tomographic ultrasound imaging (TUI) in the sequen-tial analysis of fetal congenital heart disease. Ultrasound Obstet Gynecol2006; 27:555–561.


C


37 Devore GR, Polanko B. Tomographic ultrasound imaging of the fetal heart: anew technique for identifying normal and abnormal cardiac anatomy.J Ultrasound Med 2005; 24:1685–1696.

38

��Becker R, Wegner RD. Detailed screening for fetal anomalies and cardiacdefects at the 11–13-week scan. Ultrasound Obstet Gynecol 2006;27:613–618.

A large and well designed prospective study of the effectiveness of early ultra-sound screening for all anomalies and cardiac anomalies in a moderate-riskpopulation.

39

�Smrcek JM, Berg C, Geipel A, et al. Detection rate of early fetal echocardio-graphy and in utero development of congenital heart defects. J UltrasoundMed 2006; 25:187–196.

A careful study of one of the most important aspects of early fetal heart scanningwith important medico-legal implications: the in-utero development of congenitalheart disease.

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45 Yagel S, Weissman A, Rotstein Z, et al. Congenital heart defects: naturalcourse and in utero development. Circulation 1997; 96:550–555.


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51 Hyett JA, Perdu NL, Sharland GK, et al. Increased nuchal translucency at 10–14 weeks of gestation as a marker for major cardiac defects. UltrasoundObstet Gynecol 1997; 10:242–246.

52 Hyett JA, Perdu M, Sharland GK, et al. Using fetal nuchal translucency toscreen for major congenital cardiac defects at 10–14 weeks of gestation:population based cohort study. BMJ 1999; 318:81–85.

53 Haak MC, Bartelings MM, Gittenberger-De Groot AC, Van Vugt JM. Cardiacmalformations in first-trimester fetuses with increased nuchal translucency:ultrasound diagnosis and postmortem morphology. Ultrasound Obstet Gy-necol 2002; 20:14–21.

54 Makrydimas G, Sotiriadis A, Huggon IC, et al. Nuchal translucency and fetalcardiac defects: a pooled analysis of major fetal echocardiography centers.Am J Obstet Gynecol 2005; 192:89–95.

55 Lopes LM, Brizot ML, Lopes MA, et al. Structural and functional cardiacabnormalities identified prior to 16 weeks’ gestation in fetuses with increasednuchal translucency. Ultrasound Obstet Gynecol 2003; 22:470–478.


First and early second trimester fetal heart screening

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