The Normal Offset of the Tricuspid Septal Leaflet in the Fetus
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1 Article The Normal Offset of the Tricuspid Septal Leaflet in the Fetus Ivana M. Vettraino, MD, Raywin Huang, PhD, Christine H. Comstock, MD Objective. To quantify the normal distance between the insertion of the medial leaflets of the mitral valve and tricuspid valve in the fetal heart. This mitral valve tricuspid valve distance was compared with the distance from known cases of Ebstein anomaly. Methods. An apical 4-chamber view was obtained at end diastole in fetuses between 18 and 41 weeks gestation. Calipers were placed parallel to the ventricular septum, with 1 caliper on the medial insertion of the mitral valve and a second caliper on the medial insertion of the tricuspid valve. The distance recorded was plotted against gestational age. Statistical analysis was performed by descriptive and linear regression techniques. Results. One hundred forty-five fetuses were studied. The mean ± SD mitral valve tricuspid valve distance in the second trimester was 2.8 ± 0.9 mm with a range of 1.2 to 5.0 mm; in the third trimester it was 4.6 ± 1.1 mm with a range of 2.2 to 6.9 mm. Regression analysis showed that with each 1-week increase in gestational age, there was an increase of 0.15 mm in separation between the medial leaflets of the mitral valve and tricuspid valve (β = 0.15 ± 0.011). Conclusions. A positive correlation between mitral valve tricuspid valve distance and advancing gestational age was found. The reference range described allows for the identification of a fetal heart with normal variation in the mitral valve tricuspid valve distance. Further downward displacement of the medial tricuspid cusp suggests the possibility of Ebstein anomaly. Key words: Ebstein anomaly; fetal echocardiography; tricuspid valve. Abbreviations AV, atrioventricular; MTD, mitral valve tricuspid valve offset distance Received March 27, 2002, from the Department of Obstetrics and Gynecology, Division of Fetal Imaging, William Beaumont Hospital, Royal Oak, Michigan (I.M.V., C.H.C.); Division of Biostatistics, The Research Institute, Royal Oak, Michigan (R.H.); and Department of Obstetrics and Gynecology, Wayne State University, Detroit, Michigan (C.H.C.). Revision requested April 11, Revised manuscript accepted for publication May 23, Address correspondence and reprint requests to Ivana M. Vettraino, MD, Department of Obstetrics and Gynecology, Division of Fetal Imaging, William Beaumont Hospital, 3601 W Thirteen Mile Rd, Royal Oak, MI The prenatal evaluation of fetal anatomic structures includes a 4-chamber view of the fetal heart. In the normal fetal heart, the tricuspid valve and mitral valve are offset; the tricuspid valve has an apical displacement in relation to the mitral valve. The relationship of the atrioventricular (AV) valves in the fetal heart is evaluated in a subjective manner. Occasionally, there can be difficulty in determining whether the observed displacement is within a normal range. In Ebstein anomaly, the medial leaflet and sometimes the posterior leaflet of the tricuspid valve are located closer to the apex of the heart than normal. 1 4 Although this cardiac anomaly is rare, it can lead to heart failure in the antenatal period and can be difficult to repair. 5 8 Prenatal suggestion of this anomaly can facilitate a more detailed evaluation in the prenatal and neonatal periods and can allow for the education of parents to the potential implications of Ebstein anomaly by the American Institute of Ultrasound in Medicine J Ultrasound Med 21: , /02/$3.50
2 Normal Offset of the Tricuspid Septal Leaflet in the Fetus The upper limits of the normal offset of the medial leaflets of the AV valves have been published for autopsy specimens, neonates, pediatric patients, and adults To our knowledge, a range of values for this distance has not yet been published for the fetus. The objective of this study was to investigate the relationship between gestational age and the distance between insertion of the medial leaflets of the mitral valve and tricuspid valve (MTD) in fetuses without abnormalities. A nomogram for the MTD in the second- and third-trimester fetal heart was developed. The MTD from known cases of Ebstein anomaly was compared with the developed MTD nomogram. Materials and Methods The Human Investigation Committee approved this study. The apical 4-chamber view is routinely obtained in second- and third-trimester sonograms performed in the Fetal Imaging Unit. A power analysis revealed that a sample size of at least 95 fetuses would be sufficient to have 80% confidence in detecting a relationship of at least 0.30 at P.05 between valve displacement at various gestational ages. During the study period, an apical 4-chamber axial view of the fetal heart was obtained at end diastole in fetuses between 18 and 40 weeks gestation. The apex of the fetal heart was at the top in all study fetuses. The cine loop feature on the sonography machine permitted scrolling through the image to obtain the point in the cardiac cycle at or very near end diastole. End diastole was chosen to optimize the accuracy and reproducibility of the measurement. 10 Each fetus studied was referred in the second or third trimester for fetal growth assessment. The fetuses included had normal-appearing cardiac anatomic structures and no apparent abnormal anatomic findings or known or suspected chromosomal abnormalities. Birth information and discharge summaries were reviewed for postnatal findings suggesting anatomic or chromosomal abnormalities. When applicable, karyotype and neonatal echocardiographic reports were reviewed. The sonographic equipment used during the study included an updated XP/10 OB system (Acuson, a Siemens Company, Mountain View, CA), a Sequoia system (Acuson), and a Voluson 730 system (GE Medical Systems, Milwaukee, WI). Experienced sonographers were instructed in obtaining the view and placing the calipers. The images obtained were reviewed by the physician and sonographer for inclusion or exclusion because of technique. The physician and sonographer independently measured the MTD. Calipers were placed parallel to the ventricular septum, with 1 caliper on the superior portion of the medial insertion of the tricuspid valve and a second caliper on the inferior portion of the medial insertion of the mitral valve, as shown in Figure 1. This technique has been described previously. 10 This distance was recorded. The distance of separation was plotted against gestational age. Linear regression analysis was used to examine the relationship between estimated gestational age and the MTD. Tests for normal distribution of the data were performed. Descriptive statistics were used to summarize the data. Interobserver reliability between the sonographer and physician was evaluated. For comparison, cases of a documented Ebstein anomaly were obtained through search of the sonography database. Still images of the 4- chamber view were obtained from the recorded sonograms, and the MTD was measured as described above. Figure 1. Normal second-trimester 4-chamber view with calipers placed for MTD. Arrow indicates tricuspid valve; arrowheads, mitral valve; LV, left ventricle; and RV, right ventricle J Ultrasound Med 21: , 2002
3 Vettraino et al Results The MTDs from 145 fetuses were included in this study. These 145 fetuses had normal neonatal examination findings and discharge summaries. Of the fetuses that underwent karyotype analysis, all had normal karyotypes. Five fetuses with a documented Ebstein anomaly were identified from the database. Images from the original prenatal sonographic examinations were reviewed. The results are summarized in Figures 2 4 and Table 1. Figure 2 represents the frequency distribution of valve distances in the second- and third-trimester fetuses as well as the entire population. Figure 3 is a scatterplot of the gestational age versus valve distance. Table 1 shows the results of the descriptive analysis of the MTD observations in our population without abnormalities. In summary, the MTD for second-trimester fetuses had mean ± SD of 2.8 ± 0.9 mm and a range of 1.2 to 5.0 mm. The MTD for third-trimester fetuses had mean of 4.6 ± 1.1 mm and a range of 2.2 to 6.9 mm. Correlation analysis showed a positive relationship between MTD and gestational age (r = 0.61 [0.64, corrected for attenuation]; P <.001), indicating that valve distances increase with gestational age. The evaluation of interobserver reliability for MTD readings showed an intraclass correlation of 0.90 (95% confidence interval, ). Further regression analysis indicated that with each increase of 1 week in gestational age, there was an increase of 0.15 mm of MTD per week (β = 0.15 ± 0.011; P <.001). Figure 4 illustrates the difference in the proposed normal values of MTD and documented cases of Ebstein anomaly. Discussion Figure 2. Frequency distribution of MTD. A, Second trimester (18 28 weeks). B, Third trimester (>28 weeks). C, Study group. Asterisks indicate Kolmogorov- Smirnov test of normal distribution. A B C Sonographic imaging of the 4-chamber view is an important part the second- and thirdtrimester fetal anatomic evaluation. Specifically, examination of the crux for the characteristic offset of the AV valves can be useful in identifying the presence of a cardiac anomaly. Lack of the typical apical displacement of the tricuspid valve may indicate the presence of an AV septal defect, whereas exaggerated displacement of the tricuspid valve may be indicative of Ebstein anomaly. 1,2,12 14 Either finding can have considerable clinical importance. The AV septal defect is associated with fetal trisomy 21. The prenatal diagnosis of Ebstein J Ultrasound Med 21: ,
4 Normal Offset of the Tricuspid Septal Leaflet in the Fetus Figure 3. Relationship between valve offset for fetuses without abnormalities and gestational age: scatterplot and regression analysis. Stars indicate 95% and 5% confidence limits of the point estimates; and asterisks, 95% and 5% confidence limits of the average of the point estimates. anomaly appears to be associated with a less favorable prognosis than the diagnosis in the neonatal or pediatric groups. 5,11,15 17 In addition, follow-up for hydrops and arrhythmias would be important if this diagnosis were suspected. 2,5 The displacement of the mitral and tricuspid valves in the fetus is most often evaluated in a subjective manner. 10,17 Previous studies have evaluated various ratios such as the cardiothoracic ratio, right and left atrial heights, valve annulus diameters, and others. 9,12,16 20 The quantitative evaluation of mitral and tricuspid Figure 4. Cases of documented Ebstein malformation superimposed on a scatterplot of the normal reference range. Single asterisk indicates case 1;, case 2; #, case 3; open circle, case 4; +, case 5; stars, 95% and 5% confidence limits of the point estimates for normal MTD; and double asterisk, 95% and 5% confidence limits of the average of the point estimates for normal MTD. valve displacement by echocardiography has been studied in the pediatric and adult populations. 9,10 Studies in adult and pediatric groups have also correlated the degree of apical displacement or absence of the septal leaflet of the tricuspid valve with clinical outcome. 6,9,18 The quantitative evaluation of mitral and tricuspid valve displacement has not been studied for the live fetus without abnormalities. In this study, we quantitatively evaluated the distance between insertion of the mitral and tricuspid valves in the fetal heart in the second and third trimesters. The manner selected in this study was based on review of previous reports, ease of obtaining the measurement, and good intraobserver reliability. The MTD from our study population approximates a normal distribution, adding statistical strength to the validity of the range of normal values developed. In the second trimester, the mean MTD was 2.8 ± 0.9 mm. In the third trimester, the mean MTD was 4.6 ± 1.1 mm. For the late-thirdtrimester fetus, the MTD correlates well with numbers reported for neonates with normal hearts. 9 Our results also show a positive correlation between the MTD and gestational age. This has been suggested previously on the basis of subjective observation of the fetus at various gestational ages but, to our knowledge, had not been quantified. 10,17 Figure 4 shows the MTD distances obtained from documented cases of Ebstein anomaly from our unit. The MTDs from these cases were above the 95th percentile for the developed nomogram. Thus, the MTDs from these fetuses were outliers and if compared with the developed reference range would raise the suggestion of Ebstein anomaly. The information presented allows for evaluation of the expected normal variation in MTD at various gestational ages. One may encounter those cases for which the subjective assessment of the tricuspid valve displacement is difficult or the findings are uncertain. The reference ranges presented may permit quantitative assessment to identify potential outliers. This in turn should facilitate discussions with the patient and family regarding the potential for a fetal cardiac abnormality and the need for a more detailed prenatal evaluation and neonatal follow-up J Ultrasound Med 21: , 2002
5 Vettraino et al Table 1. Summary of Descriptive Statistics for MTD by Trimester for Fetuses Without Abnormalities Quartile Percentile Trimester Mean 95% CI SD Range 25th 75th Median 10th 95th n 2nd (18 28 wk) rd (>28 wk) All groups CI indicates 95% confidence interval. References 1. Bianchi DW, Crombleholme TM, D Alton ME. Ebstein anomaly. In: Bianchi DW, Crombleholme TM, D Alton ME (eds). Fetology: Diagnosis and Management of the Fetal Patient. 1st ed. New York, NY: McGraw-Hill; 2000: Sharland G. Tricuspid valve abnormalities. In: Allan L, Hornberger LK, Sharland G (eds). Textbook of Fetal Echocardiography. 1st ed. London, England: Greenwich Medical Media Ltd; 2000: Dearani JA, Danielson GK. Congenital heart surgery nomenclature and database project: Ebstein s anomaly and tricuspid valve disease. Ann Thorac Surg 2000; 69:S106 S Rusconi PG, Zuberbuhler JR, Anderson RH, Rigby ML. Morphologic-echocardiographic correlates of Ebstein s malformation. Eur Heart J 1991; 12: 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: Chavaud S. Ebstein s malformation: surgical treatments and results. Thorac Cardiovasc Surg 2000; 48: Schreiber C, Cook A, Ho SY, Augustin N, Anderson RH. Morphologic spectrum of Ebstein s malformation: revisitation relative to repair. J Thorac Cardiovasc Surg 1999;117: Knott-Craig CJ, Overholt ED, Ward KE, Razook JD. Neonatal repair of Ebstein s anomaly: indications, surgical technique, and medium term follow-up. Ann Thorac Surg 2000; 69: Shiina A, Sward JB, Edwards WD, Hagler DJ, Tajik AJ. Two-dimensional echocardiographic spectrum of Ebstein s anomaly. J Am Coll Cardiol 1984; 3: Gussenhoven EJ, Stewart PA, Becker AE, Essed CE, Ligvoet KM, De Villeneuve VH. Offsetting of the septal tricuspid leaflet in normal hearts and in hearts with Ebstein s anomaly: anatomic and echographic correlation. Am J Cardiol 1984; 53: Oberhoffer R, Cook AC, Lang D, et al. Correlation between echocardiographic and morphological investigations of lesions of the tricuspid valve diagnosed during fetal life. Br Heart J 1992; 68: Frescura C, Angellini A, Daliento L, Thiene G. Morphological aspects of Ebstein s anomaly in adults. Thorac Cardiovasc Surg 2000; 48: Ammash NM, Warnes CA, Connolly HM, Danielson GK, Seward JB. Mimics of Ebstein s anomaly. Am Heart J 1997; 134: Anderson RH, Silverman NH, Zuberbuhler JR. Congenitally unguarded tricuspid orifice: its differentiation from Ebstein s malformation in association with pulmonary atresia and intact ventricular septum. Pediatr Cardiol 1990; 11: Celermajer DS, Bull C, Till JT, et al. Ebstein s anomaly: presentation and outcome from fetus to adult. J Am Coll Cardiol 1994; 23: Pavlova M, Fouron JC, Drblik SP, et al. Factors affecting the prognosis of Ebstein s anomaly during fetal life. Am Heart J 1998; 135: Roberson DA, Silverman NH. Ebstein s anomaly: echocardiographic and clinical features in the fetus and neonate. J Am Coll Cardiol 1989; 14: Nihoyannopoulos P, McKenna WJ, Smith G, Foale R. Echocardiographic assessment of the right ventricle in Ebstein s anomaly: relation to clinical outcome. J Am Coll Cardiol 1986; 8: J Ultrasound Med 21: ,
6 Normal Offset of the Tricuspid Septal Leaflet in the Fetus 19. Celermajer DS, Dodd SM, Greenwald SE, Wyse RK, Deanfield JE. Morbid anatomy in neonates with Ebstein s anomaly of the tricuspid valve: pathophysiology and clinical implications. J Am Coll Cardiol 1992; 19: Therrien J, Henein MY, Li W, Somerville J, Rigby M. Right ventricular long axis function in adults and children with Ebstein s malformation. Int J Cardiol 2000; 73: J Ultrasound Med 21: , 2002
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