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1. Introduction

prese(sponeart diciated

ularly in aortic coarctation, a prenatal diagnosis is associated withimproved survival and better preoperative clinical conditions.9 The

ight affect detec-hese include inad-ducer frequency,ime, and maternalraining also affect

etectable in earlygestation, or the heart anomalymight not be detectable in the four-chamber view.13 Indeed, late gestational age can also limit ultra-sound.15 High detection rates of CHD are more likely in severecardiac anatomic lesions.10 This might be because when the heartpresents as grossly abnormal in the four-chamber view, anomaliesare easier to detect.10

To assess the fetus in utero, the use of magnetic resonance im-aging (MRI) has been implemented over the last few years. MRI at1.5 T, after the rst trimenon,14 is already used in the clinical routine

* Corresponding author. Address: Department of Radiology, Medical University ofVienna/AKH, Waehringer Guertel 18-20, A-1090 Vienna, Austria. Tel.: 43 1 404004890; fax: 43 1 40400 4897.

E-mail address: vanessa.berger-kulemann@meduniwien.ac.at (V. Berger-

Contents lists available at

Seminars in Fetal &

journal homepage: www.e

Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297Kulemann).after preterm birth, the second most frequent cause of neonatalinfant death,5 although early mortality has been substantiallyreduced and long-term survival rates have improved.6

The prenatal detection of cardiac and vascular abnormalities al-lows a scheduled delivery in a stable environment, with preparedmanagement ofmother and fetus7 and proactive planning of furtheractions, including (postnatal) interventions and treatment.8 Partic-

45% to 74%.3,12 Chaoui13 discusses factors that mtion rates when using the four-chamber view; tequate examination, adjustment of transgestational age, insonation angle, examination tfactors. The operators expertise and level of tsensitivity for the detection of CHD.14

In addition, some lesions might not be dchromosomal anomalies.4

Cardiac abnormalities, including duct-dependent lesions, are,(ECG) is indicated.11

Prenatal detection of CHD by ECG (gold standard) varies fromper 1000 births,3 and is often assoCongenital heart disease (CHD) isbirths,1 not including missed birthstermination.2 Signicant congenital h1744-165X/$ e see front matter 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.siny.2013.05.006(MRI) has been implemented over the last several years and is already used in the clinical routine as asecond-line approach to assess fetal abnormalities. MRI of the fetal heart is still not routinely performed.Nevertheless, fetal cardiac MRI has the potential to complement ultrasound in detecting cardiovascularmalformations and extracardiac lesions. The present work reviews the potential of MRI to delineate theanatomy and pathologies of the fetal heart. This work also deals with the limitations and continuingdevelopments designed to overcome the current problems in cardiac imaging, including fast fetal heartrates, the lack of ECG-gating, and the presence of fetal movements.

2013 Elsevier Ltd. All rights reserved.

nt in eight of 1000 livetaneous abortion) andsease (sCHD) affects 3.6with extracardiac and

prenatal detection of CHD is also associatedwithdecreasedneonatalmorbidity10 and increased odds of a scheduled delivery and birthbefore the gestational age of 39 weeks.7

Ultrasound is routinely used in the rst and second trimester ofpregnancy. If risk factors are present, or the examination points toan anomaly of the fetal heart, targeted fetal echocardiographymaternal factors and the gestational age may lower the image quality. Fetal magnetic resonance imagingand gold standard by which cardiac malformations are dened. However, adequate examination by anexperienced healthcare provider with modern technical imaging equipment is required. In addition,Potential of magnetic resonance for ima

Alice Wielandner a, Elisabeth Mlczoch b, Daniela PraDepartment of Radiology, Medical University of Vienna, AKH, Vienna, AustriabDepartment of Pediatric and Adolescent Medicine, Pediatric Heart Center Vienna, Med

Keywords:Congenital heart diseaseFetal heartMagnetic resonance imaging

s u m m a r y

Signicant congenital heaextracardiac and chromosothe rate of long-term surviof neonatal infant death. Tparental counselling and pAll rights reserved.ng the fetal heart

er a, Vanessa Berger-Kulemann a,*

University of Vienna, AKH, Vienna, Austria

isease (sCHD) affects 3.6 per 1000 births, and is often associated withl anomalies. Although early mortality has been substantially reduced andas improved, sCHD is, after preterm birth, the second most frequent causeprenatal detection of cardiac and vascular abnormalities enables optimalnatal management. Echocardiography (ECG) is the rst-line examination

SciVerse ScienceDirect

Neonatal Medicine

lsevier .com/locate/s iny

l & Nas a second-line approach to assess the central nervous system,16

and is useful in detecting thoracic abnormalities and others.17e19

Although MRI of the fetal heart is still not routinely performed,and ECG remains the method of choice for the detection of fetalCHD,14,20e22 fetal cardiac MRI has the potential to complementultrasound in detecting cardiovascular malformations and extrac-ardiac lesions.

This article reviews the current potential of fetal cardiac MRI tovisualize anatomy and detect pathologies. It does not concentrateon the functional assessment of the fetal heart.

2. Is MRI feasible as a complement to ultrasound?

Ultrasound is routinely used in the rst trimester of pregnancyto assess fetal biometric parameters, gestational age, and thenuchal transparency. The standard of care includes a second-trimester scan between the 19th and the 23th gestational weeksto evaluate the fetal anatomy (organ screening). In cases of sus-pected CHD, a fetal ECG is indicated.11

The second-trimester scan provides four-chamber and outow-tract views.23 A targeted fetal ECG includes an anatomic overview, abiometric examination, and detailed visualization of the cardiacanatomy and the great vessels.23 Flow proles are then examinedusing Doppler, with measurements of diameters and lengths ofanatomical structures.23 Examination of rhythm and heart rate canbe assessed by using the M-mode of atrial and ventricular wallmotion, and by Doppler examination of atrial and ventricular owpatterns.23 Three- and four-dimensional imaging yields informa-tion about cardiac motion and function.24

Ultrasound is the imaging modality of choice for routine preg-nancy evaluation due to its low cost, real-time capability, andoperator comfort and experience.14 However, there are some dis-advantages. Sensitivity is directly related to the operators expertiseand level of training.14 Maternal obesity25 and maternal abdominalwall scarring from previous abdominal or pelvic surgery can limitvisualization of the fetal anatomy.15,26 Fetal position, possible oli-gohydramnion, and ossication can inuence the images ob-tained.15,26 The limited time available during the clinical routinemight also prevent ultrasound from obtaining all the views in everyfetus, as it is not possible to wait until the fetus changes to anassessable position.13 Furthermore, some CHDs may develop in lategestation andmight subject to visualization at earlier stages.13 In upto 74% of patients, ECG can recognize CHDs in utero (in certainpathologies the detection rate is even higher).3 However, particu-larly for the detection of duct-dependent lesions, such as coarcta-tion of the aorta, the anatomy is very complex and several studieshave described a lack of adequate visualization.27

Factors that might limit ultrasound as mentioned above do notnecessarily compromise the image quality of MRI.28 It can beapplied in the second and third trimesters, to avoid any risk duringorganogenesis,29 and is already becoming part of the clinicalroutine in various centers.

Despite the advantages, image quality in MRI can be inuencedby severe oligohydramnion29 and fetal motion.22,29 The visualiza-tion of the heart is limited by heart rates of more than 150 bpm, andultimately by the small size of the heart.28 Fetal movements22 andrapid fetal heart rate30 also complicate delineation of the heart andthe great vessels. In our experience, ultrasound provides a betterimage resolution compared with MRI. Drawbacks include highcosts, limited availability, and MRI-specic contraindications, aswell as claustrophobia.28

Although several studies have described good agreement be-tween ultrasound and MRI (up to 100%21), ultrasound is recom-mended as the primary approach for the assessment of fetal

A. Wielandner et al. / Seminars in Fetastructures.14,20e22 However, cardiac MRI is already used in theclinical routine in children and adults to complement ultrasoundand assess the anatomy, pathology, and function of the heart.31e33

The continuous technical developments in cardiac MRI techniqueswill lead to more potential applications.

3. Technical aspects of fetal cardiac MRI

Fetal cardiac MRI examinations in human fetuses at our insti-tution are performed on a 1.5 T Siemens Trio (Siemens, Erlangen,Germany) or a 1.5 T Philips Gyroscan (Philips, Best, TheNetherlands), using an eight-element surface-phased array coil.The patient position is supine or slightly angular to prevent thevena cava compression syndrome. In the feet-rst position, thehead is outside the tube to prevent claustrophobia.28 There is noneed for preparations, such as 4 h fasting.26,28 In our experience,neither the mother nor the fetus requires sedation. Although arecent study advocates fetal sedation, this remains controver-sial.22,28 To achieve diagnostic image quality, cardiac fetal MRIshould be performed after gestational week 25. The examinationsof younger fetuses often suffer from temporal and spatial resolutionproblems.

A region of interest is typically placed in the center of the coil. Ascout scan is acquired to assess the position of the fetus. Manydifferent sequences are used to evaluate the anatomy of the fetus.To assess the position of the fetus and the thoraco-abdominal situs,T2-weighted HASTE (half-Fourier single-shot turbo spin echo) se-quences are used. To visualize the anatomy and pathologies of theheart, a balanced steady-state free precession (SSFP, Philips) or trueFisp (Siemens) sequence are acquired in the dened heart planes ofthe fetus, based on thewhite blood technique: mixed signal (T1 andT2) where owing blood has a hyperintense signal. Dark blood T2-weighted, single-shot fast spin echo is also possible. The use ofthese techniques is in line with other studies, which investigatedthe potential of MRI to visualize the fetal heart.21,22,26,28,30,34,35

Metric optimized gating (vector ECG) of the fetus could be bene-cial, and is currently under investigation.36 ECG-gating of the fetalheart is not yet possible, and, due to rapid heart movement, it isdifcult to capture the fetal heart without blurring. To accomplishthe delineation of the heart, our institution uses a modiedapproach where the sequences are accelerated according to thematernal heart cycle.

The visualization of the fetal heart function allows an estimationof the ejection fraction.

The mean duration of the entire examination of the fetal heartvaries from 5 to 30 min and may be prolonged if additional se-quences are required.22,34

4. General considerations

Assessment of the images often includes visualization of theplanes and traditional views known from ultrasound imageacquisition.28,30 However, since MR provides multiplanar imageacquisition, the identication of structures is not necessarilydependent on traditional views. A segmental approach to assessCHD by Carvalho et al.37 was successfully modied by Saleem26 forapplication in MRI. This method can be used to summarize the MRIndings for the visualization of cardiac anatomy and the detectionof CHD in fetuses. A distinction was made between direct and in-direct signs of CHDs according to Manganaro et al.30 Volumetricabnormalities of the heart, the cardiac chambers, abnormalities ofthe structure, thickness, and signal intensity of the myocardial wall,anomalies of the cardiac axis orientation, defects of the ventricularand atrial septa, and anomalies of the origin, size, and course of thegreat arteries were rated as direct signs of CHD.28,30 Indirect signs

eonatal Medicine 18 (2013) 286e297 287were dened as difculties in recognizing a normal anatomical

postnatal assessments were later included. Due to those pre-requisites, the calculations for sensitivity and specicity are of greatvalue, even though fetal sedation was used in some cases.

It should be noted that the following summary is based onndings by radiologists who were highly experienced in the eval-uation of fetal MRI and who were equipped with state-of-the-arttechniques. In addition, not all of the examiners were blinded tothe results of prior ultrasound examinations.30,34

5. Visualization of fetal cardiac structures using MRI

5.1. Viscero-atrial situs

5.1.1. Visualized anatomyThe situs is assessed in relation to the bronchi. According to

Saleem et al.,28 the left bronchus is long, with no early division, andruns under the left pulmonary artery. The right bronchus is short,closer to vertical, and runs behind the right pulmonary artery.26,28

Assessment of the fetal position and evaluation of the regularityof the viscero-atrial situs was feasible in all fetuses in severalstudies (Fig. 1).26,28,35

Fig. 1. Viscero-atrial situs; gestational week 34. SSFP sequences were used to obtainimages in the coronal plane to assess the viscero-atrial situs. (A) Bronchi, liver on the

A. Wielandner et al. / Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297288structure in the reference projections, an increase in vascular sizebefore a vascular stenosis, the presence of cardiomegaly, andpericardial effusion.34

The following overview refers to the ndings from several in-dependent studies in fetuses using cardiac MRI from the 16th to the38th gestational week. Techniques similar to those described in theTechnical aspects section above were used in these studies. Thestudies included from 10 to 83 pregnant women/fetuses; mostwere prospective, and one study described ndings within a rangeof 298 cases.21,22,26,28,30,34,35

One study used fetal sedation but no other preparations wereused.22 The absence of fetal movements was in line with bettervisualization of the structures.22 However, additional scans wereapplied in one study when the visualization of some structures wasnot feasible.30 Most studies reported postnatal assessment of thefetuses to conrm the suspected diagnosis.22,26,30,34

In the approach by Votino et al.,22 in addition to a time limit of

right side, and stomach on the left side. (B, C) Heart; the arrow in (C) highlights theapex pointing to the left side.5 min per cardiac MRI examination, the observers were blinded tothe results of prior ultrasound examinations, but these results and

Fig. 2. Situs inversus, heterotaxia, polysplenia; gestational week 28. Axial SSFP images showand polysplenia (mp, multiple spleens).5.1.2. Visualized pathologiesUncommon variants, such as situs inversus totalis, can be visu-

alized,28 as well as a combination of cardiac, vascular, and visceralabnormalities, such as the heterotaxy syndrome.28 Left-sided or-gans are paired and right-sided structures might be absent in leftatrial isomerism. Fetal MRI can detect dextrocardia, central liver,and polysplenia (Fig. 2).28

5.2. Cardiac position, cardiac axis, cardiac size

5.2.1. Visualized anatomyA normal-sized heart occupies a third of the thorax, withmost of

it positioned on the left side, and can be measured by calculatingthe cardio/thoracic (C/T) ratio.26,28,35 The median C/T ratio reportedis 0.34 (range: 0.21e0.36).35 In our experience, visualization of thecorrect cardiac position is possible in the majority of fetuses. Thecardiac axis is dened by the angle between the true sagittal plane(a line from the spine to the anterior chest wall) and the line alongthe interventricular septum.26,28 The mean cardiac axis reportedvaries from 37.25 to 44 (Fig. 3).26,35ing a fetus with situs inversus and heterotaxy syndrome. Median position of the liver

cases.22,30

ventricular walls at mid-cavity are described to be feasible.35 Dif-ferences in signal intensity can be assessed when evaluating the

Fig. 3. Assessment of the heart size, position, and axis; gestational week 39. (A, B)Axial T2-weighted images of the fetal thorax. The aorta (AO), the right ventricle (RV),and the right atrium (RA), as well as the left ventricle (LV) and the left atrium (LA) canbe seen. The median arrow points from the spine to the anterior chest, and, based onthis median, the heart axis can be measured (smaller arrow). Normal range from 37.25

(Saleem26) to 44 (Manganaro et al.35).

A. Wielandner et al. / Seminars in Fetal & NNormally, the left atrium is the closest chamber to the fetalspine. The atria should be of equal size, and the relative size of theventricles should be similar.26,28 Volume measurements of thecardiac chambers suggest that the right ventricle in the fetus islarger than the left ventricle, up until the 32nd week of gestation;however, the atria were of similar or equal size.30 The distinction5.2.2. Visualized pathologiesAn unusual axis of the heart might be associated with an

increased risk of heart malformation, as well as abnormal intra-thoracic anatomy.38 Ectopia cordis may be visualized.28

Measuring the C/T ratio was useful in suspected cardiomegaly(Fig. 4).34

5.3. Cardiac chambers

5.3.1. Visualized anatomyVisualization of the cardiac chambers, especially the four-

chamber view (Figs 5 and 6), is feasible21,26,35 in almost allbetween right and left cardiac chambers is apparent in more than

Fig. 4. Single left ventricle; gestational week 24. Axial (SSFP) magnetic resonanceimage of large single left ventricle.two-thirds of fetuses,30 and is based on direct evidence of thepresence of the moderator band at the right ventricle apex,28,30 oron the left ventricle morphology, which is deeper in the portioncomprising the apex than the right ventricle.30

In our experience, visualization of the chordal attachments ofthe arterial valves, as applied in ultrasound,37 is not yet possiblewith MRI in human fetuses due to the lower resolution of theimages.

The interventricular septum can be imaged in every fetus withMRI.30 The inter-atrial septum can be visualized in only about one-third of all fetuses.30 The foramen ovale lies in between both atria,and detection rates vary widely.35,26 The ap of the foramen ovalefrom right to left is barely detectable,30 and the atrial septal ap isdetectable in over one-third.26

Anatomic measurements of the atria and the ventricles (area,length), as well as of the ventricular septum (thickness) and the

Fig. 5. Assessment of the cardiac chambers: four-chamber view; gestational week 39.Axial SSFP image. The four cardiac chambers, left atrium (LA), right atrium (RA), leftventricle (LV), right ventricle (RV), and the aorta (AO) are well delineated. IVS, inter-ventricular septum; spine.

eonatal Medicine 18 (2013) 286e297 289myocardial wall.30 The left ventricle demonstrates a stronger signalhypodensity compared with the right ventricle in most examina-tions, independent of gestational age.30 The opening and closing ofthe triscuspid valve and the mitral valve is detectable in the dy-namic sequences.30

The tricuspid valve lies apically in relation to the mitral valve.39

The pulmonary valve lies cranially and anterior to the aortic valve.4

The mitral and tricuspid valves are visible in most fetuses.35 In ourexperience, delicate structures such as the chordal attachmentscannot be detected (Figs. 7 and 8).

5.3.2. Visualized pathologiesThe four-chamber view assessed with MRI yielded a sensitivity

of 88% and a specicity of 96% for the detection of pathologies.22

Direct signs, such as a reduction in the size of a chamber or anabnormal increase in a cardiac chamber, can lead to the detection ofhypoplastic left heart syndrome (reduction of size of the leftchamber) and a trilocular biventricular heart (one atrium, twoventricles).34 In Ebsteins anomaly and partial anomalous pulmo-nary venous drainage, an increase in the size of the cardiac cham-bers (dilatation of the right atrium) was identied.28 Yet, to ourknowledge, no fetal MRI study in human fetuses has as yetdescribed the Ebstein anomaly in detail.

Fig. 6. Four-chamber view; gestational week 39. (A) SSFP sequence, axial plane, to visualize the four-chamber view compared with (B) the four-chamber-view using ultrasound. AO,aorta; LA, left atrium; LV, left ventricle; RV, right ventricle; RA, right atrium; IVS, interventricular septum; spine.

Fig. 7. Assessment of the two-chamber view; gestational week 33. Sagittal images(SSFP sequences) of the left atrium (LA) and the left ventricle (LV), in between themitral valve (MV).

Fig. 8. Outow vessels; gestational week 28. Axial images of SSFP sequences: right ventricular outow tract (RVOT), aortic valve (AO valve), superior vena cava (SVC), and left atrium(LA). (B) Amplication of (A) to illustrate the Mercedes star-shaped tricuspid AO valve.

Fig. 9. Tuberous sclerosis presenting with rhabdomyoma; gestational week 28. Axial(SSFP) magnetic resonance image of a rhabdomyoma within the septum (A) andsubependymal nodules (C and D). (B) T2-weighted hypointense and T1-weightedhyperintense alteration of the structure.

A. Wielandner et al. / Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297290

Fig. 10. Pericardial teratoma with pericardial effusion; gestational week 28. Coronal mageffusion (AeF: arrowhead).

A. Wielandner et al. / Seminars in Fetal & NIn addition, some cardiac tumors can be recognized by delin-eation of hypodense nodular lesions in the myocardial thickness,34

such as rhabdomyomas (Fig. 9), and visualization of pericardialeffusion is feasible (Fig. 10).34 Detection of spongious cardiomy-opathy and hypertrophy of the myocardium is achieved byanalyzing thickness, structure, and signal intensity (low) of themyocardium (Fig. 11).34

Defects in the interventricular septum can be visualized whilethe delineation of large defects of the atrial septum is very difcultdue to the presence of the physiological foramen ovale.34

Indirect signs help to detect pathologies as well,30 and areespecially useful in the detection of abnormal vessel diameters andabnormalities of the valves (aortic coarctation, pulmonary atresia/stenosis, mitraleaortic disease, tricuspid atresia). Stenosis can bedetected through the dilatation of the cardiac chambers proximalFig. 11. Hypertrophic cardiomyopathy (CMP), pericardial effusion; gestational week23. SSFP in the sagittal plane. Fetus with hypertrophic CMP, septal thickening (septum),and moderate pericardial effusion (PE).to the stenosis and post-stenotic dilatation of the vessel.30 In ourexperience, decreased size of the left ventricle can be an indirectsign of aortic coarctation.

Duct dependency of the systemic circulation can present as anincrease in the vascular caliber of the pulmonary artery and of theductus arteriosus.34

When optimal resolution and conditions were provided, wewere able to observe delineation of arch hypoplasia in fetusesstarting at the age of 30 weeks of gestation. Votino et al.22 reportedthat abnormalities of the aortic arch were demonstrable in two-thirds of subjects in their study.22

A pulmonary valve stenosis can be recognized through thepresence of severe dilatation of the right atrium, right ventricle, andductus arteriosus.34

Aorticemitral atresia can be detected due to the prior detectionof a hypoplastic left heart.34

netic resonance image (SSFP) of a pericardial teratoma (AeF: arrow) and pericardial

eonatal Medicine 18 (2013) 286e297 2915.4. Systemic and pulmonary veins

5.4.1. Visualized anatomyNormally, the superior (SVC) and inferior venae cavae (IVC)

connect to the right atrium, and, when four pulmonary veins arepresent, two right and two left pulmonary veins connect to the leftatrium.28 Visualization of the SVC and the IVC (Fig. 12) is possible inthe majority of fetuses.26

In many fetuses, at least one pulmonary vein is visible; mostly,the right upper pulmonary vein.26 The systemic venous return canbe visualized in most fetuses, in the absence of fetal movements.22

5.4.2. Visualized pathologiesInow vessel abnormalities, such as a persistent left SVC

(Fig. 13), as well as anomalous pulmonary venous drainage, can bevisualized.28

5.5. Great arteries

5.5.1. Visualized anatomyThe left and right ventricular outow tracts (aorta and pulmo-

nary arteries) are usually equal in relative size and their relativeposition in relation to each other should be a spiral relationshipwith regard to their origin.26,28

l imltra

A. Wielandner et al. / Seminars in Fetal & N292Currently, MRI can visualize the left ventricular outow tract(LVOT) in only half of examinations,22,26 but the right ventricularoutow tract (RVOT) can be seen in almost every examination(Fig. 14).22,26,30

The pulmonary arteries, although very small structures, are seenin about one-quarter of fetuses, although this is limited by spatialresolution (Fig. 15).30 The bifurcation of the main pulmonary arteryis visible in half of the fetuses by combining several planes.26 Theductus arteriosus (Fig. 16), similar in diameter compared with theSVC, can be seen in over two-thirds of cases (see also Figs. 8, 12, 14,16, 17).30 The aortic origin, seen in the long axis, can be assessed inone-third of fetuses.35

Therewereonly slight differences in vessel diameter,with regardto the pulmonary artery, aorta, and the SVC.30 However, beginningwith the largest median diameter to the smallest, the followingsequence was described: pulmonary artery > aorta > SVC.30

In our experience, the image resolution of cardiac ultrasoundexaminations of the great arteries is much higher compared with

Fig. 12. Inow vessels: vena cava and pulmonary tract; gestational week 28. (A) Coronavena cava (IVC). (B) IVC and the ductus venosus (Duct.venosus). (C) SVC and the IVC (uthe resolution of fetal cardiac MR. Further technical improvements,e.g. the introduction of ECG-gating, might improve current visual-ization rates.

Fig. 13. Bilateral superior venae cavae (SVC); gestational week 30. Axial image (SSFPsequences) with bilateral SVC.5.5.2. Visualized pathologiesWhen LVOT is visible, defects have been detected with a sensi-

tivity of 63%, and a specicity of 100% with MRI. The sensitivity fordetecting abnormalities of the RVOT was 59% and the specicity97%.22

Fetal cardiac MRI is feasible to detect conotruncal abnormalities,including the transposition of the great arteries, truncus arteriosus,tetralogy of Fallot, and coarctation of the aorta.28

Abnormalities of aortic origin (transposition, overriding aorta,truncus arteriosus) have been visualized. Hypoplasia of the aorticarch and pulmonary artery demonstrate as reduced in size in thecontext of the surrounding vessels.30

Aortic aneurysms and pulmonary artery aneurysms can bedetected (Figs. 18 and 19).

5.6. Ventriculo-arterial concordance

age obtained with SSFP sequences shows delineation of the superior (SVC) and inferiorsound). RA, right atrium; trachea.

eonatal Medicine 18 (2013) 286e2975.6.1. Visualized anatomyThe standard aorta arises from the left ventricle, continuing to a

regular arch with the three neck vessels. The pulmonary arteryusually starts in the morphologic right ventricle and dividesdistally.26,28

The left ventricular outow tract, which continues to a normalaortic arch, is well detectable (Figs. 17 and 20). The ductus arte-riosus is visible in the three-vessel transverse view in half of allfetuses.26 The ductal arch and the descending aorta can be welldetected in most fetuses (Fig. 20).26 If the arch and ductus arte-riosus are present in one image (Fig. 16), a size comparison ispossible. The origin of the head and neck vessels is visible in90%.35

5.6.2. Visualized pathologiesDirect visualization of the origin and course of the great

vessels for the detection of possible pathologies is feasible withMRI.34 Complete transposition of the great arteries, with anabnormal origin of the pulmonary artery from the left ventricleand of the aorta from the right ventricle, can be visualized.34 Theoverriding aorta is visualized in more than half of all fetuses witha tetralogy of Fallot.34 A single great artery overriding the ven-tricles can represent a truncus arteriosus, but, in our experience,this can only be determined in the context of the surroundinganatomy.34

(A) S

A. Wielandner et al. / Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297 2935.7. Side of the aortic arch

5.7.1. Visualized anatomyThe regular side of the aortic arch is determined with regard to

the main bronchus. Normally the aorta crosses in the back of themediastinum, across the main bronchus.21,26,28 Visualization of theaortic arch is successful in almost every case without severe fetalmovements.22

5.7.2. Visualized pathologiesIn a recent study, the sensitivity for detecting an abnormality of

the aortic arch (e.g. right-sided aortic arch, Fig. 21) was 58%, and thespecicity 99% using MRI.22 Detection of a right-sided aortic arch ispossible.22 However, with a sensitivity and specicity of almost100% for the detection of a dextro-transposition of the great ar-teries, ultrasound is superior to fetal MRI in human fetuses.40Fig. 14. Outow vessels: right ventricular outow tract (RVOT); gestational week 32.image that delineates the RVOT. RV, right ventricle.5.8. Traditional sonographic views assessed using MRI

The four-chamber view (Figs. 5 and 6) and the left-ventricularshort-axis view are feasible in almost every fetus.22,30 The three-

Fig. 15. Outow vessels: pulmonary arteries; gestational week 28. (A) Sagittal image of SSFPAxial image delineates the ascending aorta (asc. AO), the superior vena cava (SVC), the rigartery.vessel-view may be obtained in more than one-third,30 the ve-chamber view in half of the fetuses and the long axis view inabout one out of two.30

6. Limitations

In the majority of cases, limited visualization of anatomicstructures is associated with a high fetal heart rate, fetal move-ments, and artifacts.21,22,26,35

Early gestational age limits visualization of views, most likely dueto the smaller size of the vessels, combinedwith greater fetalmotion.Cardiac outow vascular structures can be difcult to visualize.30

Severe malrotations make recognition of both anatomical andpathological structures more complicated and time-consuming.34

7. The future

agittal image (SSFP sequences). (B) Sagittal ultrasound image. (C) Sagittal ultrasoundThe applicability of fetal MRI is expanding; however, future usein cardiac imaging in utero depends on the ability to improve theimage resolution of cardiac structures and to overcome currentlimitations. These include fetal movement, the lack of

sequence shows the right ventricle (RV) and the main pulmonary artery (main PA). (B)ht pulmonary artery (RPA), the descending aorta (desc. AO), and the main pulmonary

Fig. 16. Outow vessels: ductus arteriosus; gestational week 28. (A, B) Sagittal magnetic resonance images of the ductus arteriosus (Duct. Art.) (SSFP sequences). (C) Ultrasoundimage of the ductus arteriosus (desc. AO, descending aorta).

Fig. 17. Outow vessels: left ventricular outow tract (LVOT); gestational week 27. (A) Sagittal image (SSFP sequences) of the ascending aorta (asc. AO) and the aortic valve (AOvalve). (B) Ascending aorta (asc. AO) (ultrasound).

Fig. 18. Aortic aneurysms; gestational week 23. (A, B) Coronal images (SSFP) of aortic aneurysms. (C) Aortic aneurysms, sagittal view.

A. Wielandner et al. / Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297294

electrocardiography-gating, high fetal heart rates, and the smallsize of the structures.22,28,30

Our current knowledge of fetal electrocardiography triggering isbased on results from animal studies, mostly in sheep. A promisingnon-invasive triggering method to assess the morphology andfunction of fetal hearts, using modied CTG transducers, has beenreported.41,42 Despite maximum heart rates up to 240 beats perminute, scanning of the heart was feasible,42 and visualization atfetal heart rates from 130 to 160 without sampling artifacts wasalso described.41 A magnetic eld strength of 3.0 T was associated

In addition to the assessment of the morphologic features of thefetal heart, it is also possible to evaluate contractions, visualize theaortic valves (both closed and open) without artifacts, and identifythe mitral valves, tricuspid valves, atrial septum, and foramenovale.41 Quantitative assessment of the heart has been achieved(measurement of the thickness of the left ventricular myocardiumin diastole/systole, as well as septum and volume measurements ofthe left ventricle), and, based on those results, stroke volume andejection fraction were calculated.41 There was no undue heating ofthe transducer or the sheep.42

Fig. 19. Pulmonary artery aneurysm; gestational week 28. Magnetic resonance image (SSFP) delineating a pulmonary artery aneurysm (PAA). (A) Coronal, (B) sagittal, (C) axial.

A. Wielandner et al. / Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297 295with an increase in sensitivity with regard to artifacts fromelectrocardiography recordings.42 Manual control of the amplitudeand time parameters is still required.41,42Fig. 20. Ventriculo-arterial concordance: aortic arch, three vessels; gestational week 27. (A)(asc. AO), aortic arch (AO arch), descending aorta (desc. AO), and trachea. (B) Sagittal ultrasA study by Wedegaertner43 describes the assessment of fetal O2saturation with MR oximetry in sheep, which might becomeessential in high-risk fetuses with intrauterine growth restriction.43Sagittal image of SSFP sequences, showing the inferior vena cava (IVC), ascending aortaound image delineating the aortic arch with the branches and the descending aorta.

Postmortem studies were able to visualize the heart situs andthe four-chamber view beyond the gestational age of 16 weeksusing 1.5 and 3.0 T.44 The outow tract was only delineatedbeginning at 19.5 weeks when using 3.0 T.44 In-vivo 3.0 T fetal MRImight be applicable in future examinations.

Further developments of the techniques proven in animal studiesmay lead to application in human fetuses in the coming years, andhelp to overcome current limitations in visualizing the fetal heart.

3. Levy DJ, Pretorius DH, Rothman A, et al. Improved prenatal detection ofcongenital heart disease in an integrated health care system. Pediatr Cardiol2013;34:670e9.

Fig. 21. Right-sided aortic arch; gestational week 22. (A) Coronal magnetic resonance imageweighted, single-shot fast spin echo sequences).

l & NCardiac fetal MRI is already practical as an important second-lineapproach after ultrasound, and bears great potential for the future.

Practice points

Prenatal detection of cardiac and vascular malforma-tions provides essential information for the perinatalmanagement and further treatment of the newborn.

Further technical developments in fetal cardiac MRI,A. Wielandner et al. / Seminars in Feta296Conict of interest statement

None declared.

Funding sources

None.

Research directions

Supply overview of the potential for fetal cardiac MRI. Introduction of fetal cardiac MRI into clinical practice asa second-line approach.

Development of fetal electrocardiography-gatingmethods.

e.g. the introduction of ECG-gating, are necessary tosupply complementary information about fetal cardiacstructures when ultrasound is limited.4. Allan L. Technique of fetal echocardiography. Pediatr Cardiol 2004;25:223e33.5. Anagnostou K, Messenger L, Yates R, Kelsall W. Outcome of infants with pre-

natally diagnosed congenital heart disease delivered outside specialist paedi-atric cardiac centres. Arch Dis Child Fetal Neonatal Ed 2013;98:F218e21.

6. Eskedal L, Hagemo PS, Eskild A, Aamodt G, Seiler KS, Thaulow E. Survival aftersurgery for congenital heart defects: does reduced early mortality predictAcknowledgments

We thank our excellent radiological technician, Barbara Hoche,for her essential input regarding the technical part of this paper.

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A. Wielandner et al. / Seminars in Fetal & Neonatal Medicine 18 (2013) 286e297 297

Potential of magnetic resonance for imaging the fetal heart1 Introduction2 Is MRI feasible as a complement to ultrasound?3 Technical aspects of fetal cardiac MRI4 General considerations5 Visualization of fetal cardiac structures using MRI5.1 Viscero-atrial situs5.1.1 Visualized anatomy5.1.2 Visualized pathologies

5.2 Cardiac position, cardiac axis, cardiac size5.2.1 Visualized anatomy5.2.2 Visualized pathologies

5.3 Cardiac chambers5.3.1 Visualized anatomy5.3.2 Visualized pathologies

5.4 Systemic and pulmonary veins5.4.1 Visualized anatomy5.4.2 Visualized pathologies

5.5 Great arteries5.5.1 Visualized anatomy5.5.2 Visualized pathologies

5.6 Ventriculo-arterial concordance5.6.1 Visualized anatomy5.6.2 Visualized pathologies

5.7 Side of the aortic arch5.7.1 Visualized anatomy5.7.2 Visualized pathologies

5.8 Traditional sonographic views assessed using MRI

6 Limitations7 The futureConflict of interest statementFunding sourcesAcknowledgmentsReferences