Archives of Disease in Childhood, 1988, 63, 1137-1145

Echocardiographic diagnosis of fetal heart defects inmid trimesterI A PARNESS,* S B YEAGER,t S P SANDERS,* B BENACERRAF,t S D COLAN,*AND R VANPRAAGHTDepartments of *Pediatrics and ¶Pathology, Harvard Medical School; *Department of Cardiology,Children's Hospital; and *Department of Obstetrics and Gynecology, Brigham and Women's Hospital,Boston, tDepartment of Pediatrics, West Virginia School of Medicine, Morgantown, and tDepartment ofPediatrics, University of Vermont School of Medicine, Burlington, USA

SUMMARY One hundred and thirty five consecutive fetuses of between 16 and 23 weeks'gestation that were considered to be at high risk of having structural heart defects were examinedprospectively to determine the reliability of echocardiography for diagnosing such defects in midtimester. Each echocardiogram was done in a standard manner and cardiac anatomy wasanalysed segmentally. Twelve fetuses were excluded from analysis because of lack of follow up.Of the remaining 123 fetuses, 109 had no evidence of heart disease when followed up. In thisgroup the prenatal echocardiogram was normal in 105 and technically inadequate in four; thusthere were no false positive diagnoses of heart disease in fetuses subsequently shown to havenormal hearts. Fourteen had heart defects at follow up. The serious defect was correctlydiagnosed prenatally in 10 of 14 cases, whereas in the other four the prenatal echocardiogram wasconsidered normal. Some errors were made in diagnosing associated segmental defectsparticularly if the heart disease was complicated. Therapeutic abortion was carried out in sevencases; in five of the fetuses the prenatally diagnosed heart defect was the sole or an importantcontributing reason for the abortion. We conclude that echocardiography is a reliable method fordiagnosing many heart defects in the mid trimester.

Ultrasonography has become a valuable and reliabletechnique for prenatal diagnosis of many fetalabnormalities.1 Techniques have been describedfor performing prenatal two dimensional,3-6 as wellas M mode,5-8 and Doppler9 10 echocardiography.These investigations have shown that prenatal echo-cardiography can identify normal cardiac anatomyat gestational ages ranging from about 17 weeks tofull term. Many structural heart defects have beendiagnosed in older fetuses'1-15 with echocardio-graphy, but there are few reports of the prospectivediagnosis of heart defects in fetuses of less than 24weeks' gestation.6 13 16-18 The accuracy of prenatalechocardiography has not been prospectively evalu-ated for the diagnosis of complex cardiac defectssegment by segment, yet management of pregnan-cies at high risk of congenital heart defects requiresdiagnostic methods that are reliable at a stage ofgestation when the option of terminating the preg-nancy is still available.We investigated the use of prenatal echocar-

diography for diagnosing structural heart defects infetuses of less than 24 weeks' gestation in apopulation considered at high risk of congenitalheart disease.

Subjects and methods

Between December 1982 and July 1986 we ex-amined 135 consecutive fetuses of less than 24weeks' gestation in 133 pregnancies. Eighty ex-aminations were done at the Children's Hospital,Boston, 41 were at West Virginia University Hos-pital (December 1982 to June 1985), and nine at theMedical Center Hospital of Vermont (July 1985 toJune 1986). Five fetuses underwent a second ex-amination either as a follow up for hydrops orbecause the first examination was technically in-adequate. Twelve fetuses were excluded from thestudy: nine were lost to follow up, two died in uteroand did not undergo necropsy, and one was thera-peutically aborted without necropsy. The gesta-

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1138 Parness, Yeager, Sanders, Benacerraf, Colan, and VanPraagh

tional ages of the 123 included in the study rangedfrom 16 to 23 weeks at the time of examination(mean 20.5).

Risk factors prompting referral for prenatal echo-cardiography included: family history of congenitalheart defect, 21 maternal diabetes,22 maternalexposure to teratogenic agents during early ges-tation,23 chromosomal abnormalities or multiplecongenital anomalies detected by prenatal screen-ing,24 a congenital heart defect suspected on obstetricultrasound examination, and fetal arrhythmias.

All examinations were done by three of theauthors (IAP and SPS at the Children's Hospital,Boston, and SBY at West Virginia UniversityHospital and the Medical Center Hospital of Ver-mont). Prenatal echocardiograms were done with anATL Mark 600 or Hewlett Packard cardiac imagerequipped with a short or medium focus 5 0 mHztransducer. Two dimensional echocardiographic im-aging was supplemented by two dimensionaldirected M mode or Doppler cardiography, or both,in patients with abnormal rhythms or anatomy.Examinations were recorded on 1/2" video cassettetape for review in real time, slow motion, and stopframe modes.The examination was done with the mother

supine or in a lateral decubitus position. If theposition of the fetus was unfavourable for cardiacimaging, the mother was asked to change position orwalk about the laboratory. If the position could notbe improved, the patient was asked to return onanother day for examination.Each examination was done in a standard

manner. The position and orientation of the fetuswas determined using long and short axis scans ofthe fetal trunk.3 The fetal cardiovascular anatomywas then analysed segment by segment as previouslydescribed in neonates.2927 Visceroatrial situs wascalculated from a transverse view of the abdomennear the diaphragm by evaluating the respectivepositions of the inferior vena cava, the descendingaorta, and the spine, as well as the pattern of thevenous connections (fig 1).28 Long and short axisviews of the trunk were used to provide short andlong axis views, respectively, of the fetal heart.3 Amodified long axis view of the trunk was used tovisualise the aortic arch.3 Using these views, theveins, atriums, atrial septum, atrioventricular valves,ventricles, ventricular septum, semilunar valves,and great arteries were sequentially scanned in atleast two orthogonal planes.The recorded examination was reviewed and an

anatomical diagnosis assigned using the nomencla-ture proposed by VanPraagh et al.29 If any examina-tion failed to visualise any cardiac segment ad-equately, the study was considered technically

Fig 1 Transverse sections of the fetal trunk at the level ofthe diaphragm showing the relative positions ofthe aorta,inferior vena cava and spine. a-Case 2. Note the rightanterior position of the inferior vena cava and the leftposteriorposition oftheaorta. b-Case8 (heterotaxy).A dilated azygos vein isposteriorto theaorta associated withabsence ofthe renalto hepaticsegmentofthe inferiorvenacava. c-Case 9. Because ofa left diaphragmatichernia, theaortaand inferior vena cava arejuxtaposed to the leftofthespine (similarto asplenia). Ao: aorta, Az: azygos vein, IVC:inferiorvena cava, 1: left, r: right, Sp: spine, andp.posterior.

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Echocardiographic diagnosis of fetal heart defects in mid trimester 1139

inadequate. Because, however, it was often difficultto see pulmonary venous connections and the aorticisthmus clearly, studies that defined these structuresindistinctly were considered technically adequate.Technically inadequate examinations are reportedas such and were not excluded from analysis.The result of each prenatal echocardiogram was

discussed with the parents, the referring obstetri-cian, and (if concerned) the paediatric cardiologist.The presumed limitations of the test, specifically forthe diagnosis of atrial septal defect, ventricularseptal defect, patent ductus arteriosus, coarctationof the aorta, and minor abnormalities of the valveswere discussed with the parents before the examina-tion and again afterward in those cases in which noabnormality was detected.

If a cardiac defect was diagnosed, the nature ofthe defect including anatomy, physiology, prog-nosis, and possible postnatal treatment was ex-plained to the parents and physicians. The parentsand primary physicians were encouraged to contactus again after the examination if questions arose.The decision to continue or terminate the pregnancywas made by the parents in consultation with theprimary physician. If the pregnancy was continuedthe parents were referred to a paediatric cardiologistwho made appropriate plans for perinatal manage-ment.The outcome of live births was found out by

telephone interview with a parent or primaryphysician, or both, one month to one year post-natally. The infant was considered normal if therewere no findings suggestive of a congenital heartdefect at routine paediatric physical examination(n= 109). All infants with clinically suspectedcardiac defects were examined by a paediatriccardiologist. The results of clinical examination, twodimensional echocardiography, cardiac catheteri-sation, and angiography or surgical inspection, orboth, were obtained in these eight cases. Necropsyreports were obtained in all 10 cases in which theexamination was performed.

Results

In 109 cases there was no evidence of congenitalheart disease at follow up. In 105 of these theprenatal echocardiogram was normal, and in theother four cases the examination was technicallyinadequate.

Fourteen of 123 (11%) were confirmed to haveheart defects either at clinical follow up or atnecropsy. A cardiac defect had been diagnosedprenatally in 10 of the 14 cases. Six of these 10 weretherapeutically aborted and one fetus died in uteroat 33 weeks' gestation with severe hydrops fetalis.

Of the remaining three infants who were born alive,two died in the neonatal period-one of the heartdefect and the other of neonatal hepatitis. The thirddied at the age of 2/2 months after a viral infection.Necropsy confirmed the serious heart defects di-agnosed by prenatal echocardiography in all 10cases. Serious defects that were diagnosed were:Ebstein's anomaly (n=1), tricuspid regurgitation(n=1), pulmonary stenosis with hypoplastic rightventricle (n=1), tetralogy of Fallot with pulmonaryatresia and complete common atrioventricular canal(n=1), hypoplastic left heart syndrome (n=2), andcomplex heart disease with heterotaxy (n=3) (table1).

Defects were not diagnosed prenatally in four ofthe 14 fetuses that were subsequently found to havecongenital heart defects (table 2). The lesions inthose four cases were: patent ductus arteriosus(n=1), moderate sized apical muscular ventricularseptal defect (n=1), midmuscular ventricular septaldefect (n= 1), short segment coarctation of the aorta(n=1), and atrial septal defect secundum (n=1). Inthe infant with persistent patent ductus arteriosusspontaneous closure occurred when a few weeksold. The infant with coarctation and ventricularseptal defect had the coarctation repaired when 3weeks old, and the ventricular septal defect subse-quently closed spontaneously. The other infant witha ventricular septal defect (age 12 months) does notat the time of writing seem to require operation. Theatrial septal defect secundum was an incidentalfinding at necropsy following therapeutic abortionfor other abnormalities.The parents of four fetuses with prenatally di-

agnosed heart defects chose to continue the preg-nancies after counselling. Two of these fetuses(cases 4 and 7) were born alive but died in theneonatal period despite management of the heartdefects. A third fetus (case 6) died in utero at 33weeks' gestation of fetal hydrops. The remainingfetus (case 10) was born at full term and underwentpalliative ligation of patent ductus arteriosus andpulmonary artery banding. The infant subsequentlydeveloped pneumonia and died when 21/2 monthsold.

Discussion

In our study, adequate two dimensional echocardio-grams were obtained in 97% of fetuses before 24weeks' gestation. We correctly excluded structuralheart defects in all fetuses that were subsequentlyfound to be normal and in which technicallyadequate echocardiograms could be obtained; nonormal fetus was diagnosed as having a structuralheart defect by prenatal echocardiography.

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1140 Parness, Yeager, Sanders, Benacerraf, Colan, and VanPraagh

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1142 Parness, Yeager, Sanders, Benacerraf, Colan, and VanPraagh

Table 2 Heart defects not diagnosed prenatally

Case Gestational Indication for Echocardiographic diagnosis Final diagnosis and method of confirmationNo age (weeks) examination

11 20 Previous child with Born alive (angiography, echocardio-congenital heart graphy, clinical observation)disease 1 {S,D,S}* 1 {S,D,S}*

2 No structural heart defects 2 Moderate midmuscular ventricular septaldefect

3 Severe short segment coarctation ofaorta

12 20 Previous child with Born alive (echocardiography, clinicalcongenital heart observation)disease 1 {S,D,S}* 1 {S,D,S}*

2 No structural heart defects 2 Moderate apical muscular ventricularseptal defect

13 23 Fetal arrhythmia Born alive (clinical observation)1 {S,D,S}* 1 {S,D,S}*2 No structural heart defects 2 Patent ductus arteriosus

14 20 Amniocentesis 46,3p- Therapeutic abortion (necropsy)Other abnormalities 1 {S,D,S}* 1 {S,D,S}*

2 No structural heart defects 2 Atrial septal defect secundum3 Renal and skeletal abnormalities

*Segmental notation described by VanPraagh et al.29

Our results also show that many forms of con-genital heart disease, including complex defects, canbe diagnosed in fetuses before 24 weeks' gestationusing two dimensional echocardiography. Thus theinformation necessary to make rational decisionsabout continuing or terminating pregnancies at highrisk of congenital heart defects can be obtained innearly all patients. In five of our cases the know-ledge that the fetuses had severe heart defects wasinfluential in the decision to terminate the preg-nancy. In the three cases in which severe cardiacdefects were diagnosed prenatally and the preg-nancies were carried to full term, the family andresponsible physician were prepared for the birth ofan infant with congenital heart disease.The three complex cases of heterotaxy illustrate

both the potential for accurate segmental diagnosisand the potential for error in such an analysis. Incase 8 a complex defect was correctly diagnosed innearly all details. Persistent left superior vena cavaand ipsilateral pulmonary venous connection werenot seen prenatally (figs 1 and 2, and table 2). Incase 9, though double outlet single right ventriclewas correctly diagnosed, several errors were madein the segmental diagnosis. The inferior vena cavaand descending aorta were to the left of the spine atthe diaphragm suggesting visceroatrial heterotaxy(fig lc). Displacement of the liver to the left by theleft diaphragmatic hernia disorted the relationshipbetween the inferior vena cava and spine in thisfetus with normal visceroatrial situs. The anomalouspulmonary venous connection to the left verticalvein was not recognised prenatally. The hypoplastic

left atrium with mitral atresia could not be seenadequately, and the dilated right atrium and tricuspidvalve were misinterpreted as a common atrium andcommon atrioventricular valve. Functionally, themost important error was in mistaking the enlargedpulmonary artery and ductus arteriosus for a largeaorta. We believe that this was partly a result of ourheightened suspicion of asplenia (which is commonlyassociated with malposition of the great arteries andpulmonary stenosis), and partly because of theinability to resolve as separate structures the hypo-plastic aorta and the ductus arteriosus (fig 3). Inretrospect a branch pulmonary artery could be seenarising from the anterior vessel, identifying it as thepulmonary trunk. Though in this case the errors indiagnosis did not influence the management appre-ciably, some of the errors might be important if theheart disease were an isolated abnormality.

In case 10, our failure to identify the inferior venacava led us to suspect that there was an interruptedinferior vena cava with azygous continuation, butthis was not so. As in case 9, a hypoplastic leftatrium was not recognised, and a dilated rightatrium was misinterpreted as a common atrium.Visualisation of the atrioventricular valve and ven-tricular morphology was not good enough to identifythe ventricular loop, and a posterior muscularventricular septal defect was mistaken for anatrioventricular canal defect. In two additionalfetuses (cases 1 and 2), tricuspid regurgitationseemed to restrict the excursion of the pulmonaryvalve resulting in an overestimation of the degree ofobstruction.

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Echocardiographic diagnosis of fetal heart defects in mid trimester 1143

Fig 3 Case 9. Parasagittal view in fetus with double outletsingle right ventricle showing how the main pulmonaryartery and ductus arteriosus can look like the aortic arch.Note the leftpulmonary artery arisingfrom the mainpulmonary artery. BCA: brachiocephalic arteries, Dsc Ao:descending aorta, LPA: leftpulmonary artery, MPA:main pulmonary artery, s: superior, RV: right ventricle, anda: anterior.

Fig 2 Case 8 (heterotaxy). a-Four chamber view oftheheart showing common atrium, common atrioventricularvalve, and right ventricular dominance. b-Short axis viewofthe ventricles showing large right ventricle andhypoplastic left ventricle. c-Transverse cut through thegreat arteries showing large aorta and hypoplasticpulmonary arteries. a: anterior, CA: common atrium,i: inferior, LV: left ventricle, PA: pulmonary artery, RV:right ventricle, Ao: aorta, r: right, and p: posterior.

In summary, diagnostic errors were made in theevaluation of each cardiac segment. Systemic andpulmonary venous anomalies, were particularlydifficult to visualise in fetuses of less than 24 weeks'gestation, though improved resolution and newtechniques (such as colour flow Doppler) mayimprove the sensitivity. On two occasions a smallatrial chamber was not recognised and this led to afalse diagnostic impression of a single atrium. In one

case the presence of mitral atresia led to themisdiagnosis of a single common atrioventricularvalve, and on two occasions imaging was not goodenough to see ventricular looping. Evaluation of theinfundibular and semilunar valve segments of theheart was largely successful, though in two cases thepresence of severe tricuspid regurgitation influencedthe assessment of the pulmonary valve.Our experience suggests that some additional

defects are unlikely to be diagnosed consistently byprenatal echocardiography, at least before 24 weeks'gestation. We missed muscular ventricular septaldefects and coarctation of the aorta largely becauseof limitations in resolution of the imaging devices.None of these defects could be definitely diagnosed,even in retrospect. Other defects that might not bedetected for the same reason include abnormalitiesof the valves such as bicommissural aortic valve orcongenital mitral stenosis. Normal fetal physiologyresults in a widely patent foramen ovale, preeluding-reliable prenatal diagnosis of atrial septal defectsecundum (fig 4). Prenatal echocardiography cannotpredict postnatal patency of the ductus arteriosus,and in some cases coarctation of the aorta maydevelop postnatally in association with closure of theductus arteriosus. 1

Because a fetus with a normal two dimensionalechocardiogram was not re-examined again, wecannot exclude the possibility that some defectsmissed at the first examination might be detected

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1144 Parness, Yeager, Sanders, Benacerraf, Colan, and VanPraagh

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C,

Fig 4 Four chamber views ofthe heart illustrating thedifficulty in diagnosing atrial septal defect secundum.a-Case 12 with intact atrial septum atfollow up,and b-Case 14 with secundum atrial septal defect atnecropsy. LA: left atrium, and RA: right atrium.

later in gestation. None the less, most of the defectsthat might be difficult or impossible to diagnoseusing prenatal echocardiography can be treatedsurgically with low risk. It seems unlikely thatparents would choose to terminate a pregnancybecause of detection of one of these lesions.Though the postnatal clinical evaluation used to

establish normality in our patients is not proof of theabsence of a heart defect, it is the most common wayof detecting such defects. Abnormalities that may bemissed by routine clinical examination in younginfants include atrial septal defects, mild coarctationof the aorta, and minor valvular defects, all of whichwould be unlikely to be diagnosed by fetal echocar-diography. Thus the clinical examination seemsadequate to diagnose those lesions that one hopes todetect by prenatal echocardiography.

The high yield of cardiac defects in our series isthe result of the highly selected nature of our patientpopulation. The disproportionate number of fetuseswith unusual and severe anomalies was largelybecause of referral after routine obstetric ultrasoundexamination had suggested the presence of a heartdefect. Similar skewing of the distribution towardsmore severe lesions was noted in the series reportedby Allen et al.32Though prenatal echocardiography is a promising

and useful technique, its limitations should berecognised. Reliable diagnosis of structural heartdefects, especially complex lesions, in utero requiresextensive knowledge of normal and pathologicalcardiac anatomy. Despite meticulous use of asegmental approach to prenatal echocardiographicdiagnosis of structural heart defects we have beenunable to achieve the diagnostic accuracy attainablepostnatally. We hope that as techniques improveprenatal diagnosis will become as accurate aspostnatal diagnosis.This study was supported in part by training grant No 5T32HLO752-03 from the National Institutes of Health.

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Accepted 26 May 1988

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