Mild tricuspid regurgitation: a benign fetal finding at various stages of pregnancy

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1 Ultrasound Obstet Gynecol 2005; 26: Published online 7 October 2005 in Wiley InterScience ( DOI: /uog.1999 Mild tricuspid regurgitation: a benign fetal finding at various stages of pregnancy B. MESSING*, S. PORAT, T. IMBAR, D. V. VALSKY, E. Y. ANTEBY and S. YAGEL *Departments of Obstetrics and Gynecology, Beilinson Medical Center, Rabin Campus, Tel Aviv and Hadassah University Hospital, Mount Scopus, Jerusalem, Israel KEYWORDS: fetal echocardiography; prenatal diagnosis; screening; STIC; tricuspid regurgitation ABSTRACT Objective Tricuspid regurgitation (TR) may accompany various anatomical malformations and/or dysfunction of the fetal right heart. It may also appear in an anatomically healthy heart. With improved ultrasound modalities, more cases than the previously estimated prevalence of fetal TR in the low-risk population are being diagnosed. The objective of this study was to determine the prevalence of mild fetal TR in a low-risk obstetric population. Methods In 157 low-risk pregnant women (age range, years) undergoing both early second-trimester and mid-trimester targeted organ scanning, including complete fetal echocardiography according to the five transverse planes technique, the apical four-chamber view was visualized using gray-scale, color Doppler and spatiotemporal image correlation (STIC) ultrasound modalities, with optimal acquisition parameters. Results Mild-to-moderate TR was discovered in the early second-trimester scan in 131/157 (83.4%) fetuses. No cases of cardiac malformation were found. All fetuses showed normal flow in the ductus venosus, including in one case diagnosed with moderate TR. Only in 39 (24.8%) cases was mild TR still evident at the second, mid-trimester scan. Neonatal echocardiography revealed mild TR in eight (5.1%) cases. No cases of chromosomal anomalies were detected. Conclusion Mild TR is a benign finding of a temporal nature in early pregnancy. Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd. INTRODUCTION Mild tricuspid regurgitation (TR) is a frequent finding during Doppler echocardiography in neonates, children and adults. Some authors estimate a prevalence of detectable regurgitation of up to 80% in normal hearts 1 3. The prevalence of TR on fetal echocardiography has been reported to be approximately 7% 4,5. TR in fetal life may be associated with congenital heart defects, including Ebstein s malformation, tricuspid valve dysplasia, pulmonary atresia and atrioventricular canal malformation, as well as cardiomegaly, cardiac arrhythmia, non-immune hydrops, maternal diabetes or indomethacin exposure among others 1 3,6. Gembruch and Smrcek 5 found no association between fetal TR and intrauterine growth restriction (IUGR) in their 1997 study. The investigators performed echocardiographic evaluation of 289 appropriate for gestational age and 31 IUGR fetuses with color Doppler flow imaging and color Doppler M-mode in the fourchamber view. They found mild TR at a prevalence of 6.23% and 6.45%, respectively. Of these, most were isolated and transient findings. The authors concluded that while it may be indicative of underlying problems, TR is most likely a physiological finding. DeVore s 2000 study used a four-chamber view and color Doppler mapping to diagnose several cardiac markers for Down syndrome in women referred as highrisk 7. He found that 28.8% of Down syndrome fetuses had TR (though no description of classes or severity of the finding is provided) while only 1.7% of controls were found to have TR. None of the Down syndrome fetuses was reported to have isolated mild TR. A recent study by Huggon et al. 8 of fetuses at high risk for congenital heart disease and/or chromosomal anomaly referred for detailed echocardiography suggested that a careful search for TR is an important aspect of late first- and early second-trimester fetal evaluation, as this is frequently a marker for chromosomal defects even in the absence of structural heart disease. Correspondence to: Prof. S. Yagel, Department of Obstetrics and Gynecology, Hadassah University Hospital, Mount Scopus, Jerusalem, Israel ( syagel@hadassah.org.il) Accepted: 9 August 2005 Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER

Mild tricuspid regurgitation 607 Hitherto published studies methodologies diagnosed fetal TR by cross-sectional imaging and color flow mapping of the fetal heart, with specific attention to the

2 Mild tricuspid regurgitation 607 Hitherto published studies methodologies diagnosed fetal TR by cross-sectional imaging and color flow mapping of the fetal heart, with specific attention to the pulsed Doppler flow profile in the tricuspid valve. Color Doppler scanning is the preferred modality to establish the presence of TR and to grade its severity. Severe lesions may produce a jet that appears to fill the right atrium; very small jets are diagnostic of minimal, trace, trivial or mild TR. Recently, Doppler spatiotemporal image correlation (STIC), a new three-dimensional (3D) technique, has been introduced to clinical practice. STIC technology acquires a volume of data from the fetal heart and displays a cine loop of a single cardiac cycle Since the advent of STIC technology, together with 3D color Doppler, surface rendering and multiplanar capabilities, the clinical impression is that mild TR is a much more common finding in the early second trimester than previously believed. These techniques were employed in the present study to assess the prevalence and clinical significance of mild TR in structurally normal fetuses during early secondand mid-trimester targeted organ scanning examinations of pregnancy and at postnatal follow-up. METHODS The study was approved by the institutional review board (Helsinki Committee) of the Hadassah Medical Centers. All patients signed informed consent. A prospective cohort study was conducted to establish the prevalence and clinical significance of mild TR at early secondand mid-trimester targeted organ scanning and at postnatal follow-up. The study group was enrolled over a period of 18 months from an obstetric population considered as low-risk for chromosomal or cardiac anomalies, presenting for either targeted organ scanning for fetal anomalies or during routine follow-up. Patients had previously undergone nuchal translucency (NT) screening with or without maternal biochemical testing or genetic testing (chorionic villus sampling). Overall, 157 gravidae fulfilled the following enrollment criteria: (1) known gestational age by first-trimester ultrasound or known date of last menstruation; (2) estimated fetal weight appropriate for gestational age; (3) NT measurement < 95 th centile for gestational age and/or calculated risk of Down syndrome < 1 : 300 by NT with maternal biochemical testing, or normal karyotype results; (4) structurally normal fetal heart on echocardiography; and (5) normal amniotic fluid volume. Exclusion criteria included multiple pregnancy, maternal or fetal disease such as maternal diabetes, family history of congenital heart disease, and fetal structural or chromosomal anomalies. Thus the study group was selected for its low risk of structural cardiac or chromosomal anomaly. Each patient was scanned twice during pregnancy, at weeks and at weeks gestation. Neonates were screened within 72 h of delivery; suspected cases of congenital cardiac anomalies or murmurs were followed clinically for up to 30 days, including echocardiography when cardiac malformation or dysfunction was suspected. Ultrasonography was performed using an abdominal 4 8-MHz curvilinear transducer or a vaginal 5 9-MHz transducer, as appropriate. The combined transabdominal (TAS) transvaginal (TVS) technique was employed as necessary, when the angle and position of the fetal heart required the TVS approach for optimal visualization. Fetal echocardiography was performed according to the five transverse planes technique as described previously 12, using the STIC modality to acquire the five planes, with and without color mapping. Each measurement was repeated twice in each fetus, and the mean value was determined. After the initial visualization of the fetal heart in the apical four-chamber view, a color and pulse Doppler sample was obtained at an optimal angle of 0 (uptoa maximum angle of 30 ) to the interventricular septum. Images generated from the volume datasets were viewed by multiplanar display, which allows dynamic images of the fetal heart to be simultaneously visualized in three orthogonal planes (Figure 1). When TR was identified by color Doppler scanning, pulse-wave Doppler was used to measure blood flow across the valve (Figure 2). Doppler settings were set to optimize visualization as follows: persistence low mid as appropriate, highpass filter low max as appropriate; pulse repetition frequency (PRF) 4 9 khz; and color Doppler settings: PRF 4 11 khz; size of the color box as small as possible; wall filter low mid, and persistence low med as appropriate. Neonatal echocardiography was performed with an HP-5500 machine (Hewlett-Packard, Palo Alto, CA, USA), using an 8-MHz transducer. TR was categorized according to the following three parameters: the length of the jet into the right atrium (RA), Figure 1 Multiplanar image generated from the volume dataset showing the fetal heart simultaneously visualized in three orthogonal planes, with reversed flow across the tricuspid valve (arrow).

3 608 Messing et al. Table 1 Characteristics of cases of tricuspid regurgitation (TR) Length of jet into atrium No TR Mild* Mild-to-moderate Moderate Early scan (n = 157) Mid-trimester scan Area of atrium covered < 25% > 25% Early scan Mid-trimester scan 39 0 Temporal appearance of jet in cardiac cycle Early systolic Early to mid-systolic Early scan Mid-trimester scan 39 0 *Length of jet < 1/3 of distance from tricuspid valve to opposite atrial wall. Length of jet between 1/3 and 2/3 of the distance to the opposite atrial wall. Length of jet > 2/3 of the distance but not reaching the opposite atrial wall. Table 2 Pregnancy outcome Vaginal delivery (n) 133 Cesarean delivery (n) 24 Gestational age at delivery (weeks) (range) 38.3 (27 42) Birth weight (g) (range) 3367 ( ) Figure 2 Typical pulse Doppler trace of mild tricuspid regurgitation. the area of the RA covered by the jet, and the temporal appearance of the jet in the cardiac cycle. The length of the jet into the RA was further classified into four degrees of severity: mild (length of jet < 1/3 of the distance to the opposite atrial wall); mild-to-moderate (length of jet between 1/3 and 2/3 of the distance to the opposite atrial wall); moderate (length of jet > 2/3 but not reaching the opposite wall) and severe (jet reaching the opposite atrial wall). The area of RA covered by the jet was estimated by operator s observation as the percentage of the area of the atrium. The temporal appearance of the jet during the cardiac cycle was further described as early systolic, mid-systolic (appearing at early systole and persisting to mid-systole) or holosystolic. Mild (or trivial or trace) TR was defined as those cases with jet length < 1/3 of the distance to the opposite atrial wall, with an area covered by the jet < 25% of the atrium, and temporal appearance during early to mid-systole. Statistics All data processing was performed using SPSS 9.0 for Windows (SPSS Inc., Chicago, IL, USA) and a value for P of 5% or less was considered statistically significant. RESULTS The mean maternal age of the cohort was 27.4 (range, 18 42) years and parity was 1.9 (range, 0 7). Using fetal echocardiography including the STIC technique revealed that while 131/157 (83.4%) cases demonstrated TR during the early scan, only 39 (24.8%) of these displayed TR during the mid-trimester scan. Measurement of the TR jet length into the RA and of the area of RA covered by the jet, as well as the temporal appearance of the jet in the cardiac cycle, showed that the majority of the TR cases were mild: 120/131 cases observed at weeks and all 39 cases that persisted to the mid-trimester scan (Table 1). Of the other 11 cases observed during the early scan, 10 were classed as mild-to-moderate and one as moderate. In 91/131 cases the TR was observed during early systole while 40 cases appeared during early to mid-systole at the early scan. Among the 39 cases of persistent mild TR, all were early systolic at the mid-trimester scan. Combined TAS TVS was used in one-third of cases, while TAS alone was used in two-thirds of cases. The proportion of TR-positive fetuses was similar in both examination groups. No cases of TR were diagnosed in the mid-trimester when the early scan was negative. Pregnancy outcome is presented in Table 2. While eight neonates demonstrated early mild TR, no anatomical or chromosomal anomalies were diagnosed. DISCUSSION In the present study using the STIC technique, we observed a high prevalence (83.4%) of mild TR during early scan with a significant decrease (24.8%) toward the midtrimester scan. The majority of cases diagnosed in the early scan were mild or mild-to-moderate; during the mid-trimester scan all persisting cases were classed as mild. In addition, while the majority of cases were early systolic and only the minority mid-systolic at the earlier scan, all the persisting cases were early systolic at the later scan. Eight (5.1%) neonates were observed to have mild TR.

4 Mild tricuspid regurgitation 609 Our results differ from those of other researchers in several respects, foremost in the much higher prevalence of TR in our low-risk fetal population as compared to the 2 6.8% prevalence of earlier studies 4,5,7. We speculate that this marked difference reflects the higher sensitivity of the STIC technique vs. two-dimensional color flow mapping of the fetal heart. Great care was taken to maintain an angle of insonation of 0 30 to the interventricular septum. Furthermore, this technique allows frame-by-frame review of the recorded cardiac cycle loop, so that very early and very brief regurgitation jets can be detected. We included only cases of isolated mild-to-moderate TR, while other studies may not have included all mild cases. Respondek and colleagues 4 suggested that TR might indicate physiological abnormality such as increased preload or afterload, myocardial impairment or arrhythmia. Huggon and colleagues 8 recently reported a high prevalence of TR in their study of 262 fetuses referred for detailed echocardiography for increased NT, suspected cardiac or extracardiac malformation, or a family history of cardiac malformation. In this high-risk fetal population the prevalence of TR was 27%, of which 83% proved to have karyotype anomalies, while of those without TR 35% were found to have karyotype anomalies. It has also been proposed that a finding of fetal TR increases the risk of Down syndrome 7. However, the populations studied and the severity of the findings in these studies differed from the present study. TR in the fetus may be an indication of a variety of structural and functional abnormalities, some of which may evolve during the course of pregnancy and beyond. The present study examined the prevalence of mild TR in early and mid-gestation, an apparently innocuous finding, and a discrete entity from severe TR and its apparent association with chromosomal or cardiac anomalies 8. Despite its clinical insignificance, mild TR warrants notice because of the danger of over-treatment for supposed increased risk of aneuploidy or cardiac malformations, interventions that may be indicated in the presence of severe TR. The enigma of mild fetal TR, namely that it is common in early gestation, decreases in severity and prevalence during gestation, and reappears during the neonatal period and childhood remains. It may be related to changes in pulmonary resistance or myocardial compliance; larger observational studies might shed light on this issue. However, the high prevalence of mild TR found in the present study suggests that this phenomenon may reflect a normal physiological finding during early fetal development, which decreases in prevalence and severity over the course of pregnancy. REFERENCES 1. Brand A, Dollberg S, Keren A. The prevalence of valvular regurgitation in children with structurally normal hearts: a color Doppler echocardiographic study. Am Heart J 1992; 123: Choong CY, Abascal VM, Weyman J, Levine RA, Gentile F, Thomas JD, Weyman AE. Prevalence of valvular regurgitation by Doppler echocardiography in patients with structurally normal hearts by two-dimensional echocardiography. Am Heart J 1989; 117: Singh JP, Evans JC, Levy D, Larson MG, Freed LA, Fuller DL, Lehman B, Benjamin EJ. Prevalence and clinical determinants of mitral, tricuspid, and aortic regurgitation (the Framingham Heart Study). Am J Cardiol 1999; 83: Respondek ML, Kammermeier M, Ludomirsky A, Weil SR, Huhta JC. The prevalence and clinical significance of fetal tricuspid valve regurgitation with normal heart anatomy. Am J Obstet Gynecol 1994; 171: Gembruch U, Smrcek JM. The prevalence and clinical significance of tricuspid valve regurgitation in normally grown fetuses and those with intrauterine growth retardation. Ultrasound Obstet Gynecol 1997; 9: Hornberger LK, Sahn DJ, Kleinman CS, Copel JA, Reed KL. Tricuspid valve disease with significant tricuspid insufficiency in the fetus: diagnosis and outcome. J Am Coll Cardiol 1991; 17: DeVore GR. Trisomy 21: 91% detection rate using secondtrimester ultrasound markers. Ultrasound Obstet Gynecol 2000; 16: Huggon IC, DeFigueiredo DB, Allan LD. Tricuspid regurgitation in the diagnosis of chromosomal anomalies in the fetus at weeks of gestation. Heart 2003; 89: Goncalves LF, Lee W, Chaiworapongsa T, Espinoza J, Schoen ML, Falkensammer P, Treadwell M, Romero R. Fourdimensional ultrasonography of the fetal heart with spatiotemporal image correlation. Am J Obstet Gynecol 2003; 189: DeVore GR, Falkensammer P, Sklansky MS, Platt LD. Spatiotemporal image correlation (STIC): new technology for evaluation of the fetal heart. Ultrasound Obstet Gynecol 2003; 22: Chaoui R, Hoffmann J, Heling KS. Three-dimensional (3D) and 4D color Doppler fetal echocardiography using spatio-temporal image correlation (STIC). Ultrasound Obstet Gynecol 2004; 23: Yagel S, Cohen SM, Achiron R. Examination of the fetal heart by five short-axis views: a proposed screening method for comprehensive cardiac evaluation. Ultrasound Obstet Gynecol 2001; 17:

5 610 Messing et al. Excerpts from Reviewers Comments The authors of this paper claim to have demonstrated a very high incidence of tricuspid valve regurgitation in normal fetuses, especially at weeks of gestation. Previous papers have suggested a significant association between mild tricuspid regurgitation (TR) and chromosomal abnormality. If the findings of Messing et al. are valid, the incidence of TR in the normal fetal population would be too high for the finding of TR to be of any value in the detection of chromosomal abnormality. A major weakness of this study is that it relies on a new technique, color STIC, in circumstances in which it has not been validated as a suitable method. Some degree of flow reversal in early systole is inevitable in order to bring about closure of an atrioventricular valve. The mere presence of flow reversal at the tricuspid valve on color Doppler (STIC or conventional) is therefore not in itself sufficient to diagnose TR. Most cardiologists would avoid diagnosing TR on color Doppler in the absence of any clear aliasing of the signal and Figure 1 does not demonstrate aliasing. A new figure, Figure 2, has been introduced in the revised manuscript and is labeled as a typical example of mild TR. It is not clearly stated whether the pulsed wave Doppler trace in Figure 2 is from the same examination as that in Figure 1 or a different one. Figure 2 actually shows only a normal tricuspid valve closure artifact (with the gain turned up higher than appropriate) and not TR, an interpretation with which, I believe, just about every trained cardiologist would agree. I think that this paper may inadvertently mislead many readers because its definition of TR clearly includes examples that most operators would consider artifact. In particular most, if not all, of the cases in the study would not fit the inclusion criteria for significant TR in papers demonstrating an association with chromosomal abnormality. I. Huggon Harris Birthright Research Centre, King s College Hospital, London, UK ( ian.huggon@btinternet.com) The authors should perform a validation study of pulsed Doppler at a minimum to compare with this new technique. Figure 1 does not show TR. The velocities going into the atrium should be aliased to be TR and those in the figure are not. The authors are capturing the low velocity result of normal tricuspid valve closure and falsely identifying that as tricuspid valve regurgitation. It is well known that non-holosystolic TR can be simulated by the closure sound of the TV and the associated movements of blood nearby. The duration of these sounds aids in differentiating a TV closure click noise and TR. Previous work has used the criterion of a duration of at least 70 milliseconds to define trace TR. The authors include no data concerning the criteria for TR. Low velocity, non-aliased color Doppler should not be accepted as TR. J. Huhta Department of Pediatrics, University of South Florida College of Medicine, St. Petersburg, FL, USA ( huhfam@aol.com)

Relationship Between Isolated Mild Tricuspid Valve Regurgitation in Second-Trimester Fetuses and Postnatal Congenital Cardiac Disorders

ORIGINAL RESEARCH Relationship Between Isolated Mild Tricuspid Valve Regurgitation in Second-Trimester Fetuses and Postnatal Congenital Cardiac Disorders Jizi Zhou, MD, PhD, Yun Zhang, MD, Yonghao Gui,