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Imaging the first trimester heart: ultrasound correlation with morphology

Published online by Cambridge University Press:  27 August 2014

Fenna A. R. Jansen
Affiliation:
Department of Obstetrics, Leiden University Medical Center, Leiden, The Netherland
Emmeline E. Calkoen
Affiliation:
Department of Anatomy & Embryology, Leiden University Medical Center, Leiden, The Netherland Department of Paediatric Cardiology, Leiden University Medical Center, Leiden, The Netherland
Monique R. M. Jongbloed*
Affiliation:
Department of Anatomy & Embryology, Leiden University Medical Center, Leiden, The Netherland Department of Cardiology, Leiden University Medical Center, Leiden, The Netherland
Margot M. Bartelings
Affiliation:
Department of Anatomy & Embryology, Leiden University Medical Center, Leiden, The Netherland
Monique C. Haak
Affiliation:
Department of Obstetrics, Leiden University Medical Center, Leiden, The Netherland
*
Correspondence to: Dr M. R. M. Jongbloed, MD, PhD, Department of Anatomy & Embryology and Cardiology, Leiden University Medical Center Postal zone: S-1-P, P.O. Box 9600, 2300 RC, Leiden, The Netherlands. Tel: +31 71 526 9380; Fax: +31 71 526 8289; E-mail: m.r.m.jongbloed@lumc.nl

Abstract

First trimester sonography is a widely used technique to examine the foetus early in pregnancy. The desire to recognise complex anatomy already in early developmental stages stresses the need for a thorough knowledge of basic developmental processes as well as recognition of cardiac compartments based on their morphology. In this paper, we describe the possibilities and limitations of sonographic assessment of the foetal heart between 10 and 14 weeks of gestation and correlate this to morphology. Examples of the most commonly detected congenital anomalies are atrioventricular septal defects, transposition of the great arteries, and hypoplastic left heart, which are shown in this paper.

Type
Original Article
Copyright
© Cambridge University Press 2014 

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Footnotes

*

Both authors contributed equally.

References

1.Hove, JR, Koster, RW, Forouhar, AS, Acevedo-Bolton, G, Fraser, SE, Gharib, M. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 2003; 421: 172177.Google Scholar
2.Broekhuizen, ML, Hogers, B, DeRuiter, MC, Poelmann, RE, Gittenberger-de Groot, AC, Wladimiroff, JW. Altered hemodynamics in chick embryos after extraembryonic venous obstruction. Ultrasound Obstet Gynecol 1999; 13: 437445.Google Scholar
3.Vermot, J, Forouhar, AS, Liebling, M, et al. Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol 2009; 7: e1000246.Google Scholar
4.Slough, J, Cooney, L, Brueckner, M. Monocilia in the embryonic mouse heart suggest a direct role for cilia in cardiac morphogenesis. Dev Dyn 2008; 237: 23042314.Google Scholar
5.Allan, L, Benacerraf, B, Copel, JA, et al. Isolated major congenital heart disease. Ultrasound Obstet Gynecol 2001; 17: 370379.Google ScholarPubMed
6.Carvalho, JS. Fetal heart scanning in the first trimester. Prenat Diagn 2004; 24: 10601067.Google Scholar
7.Gittenberger-de Groot, AC, Poelmann, RE. Normal and abnormal cardiac development. In: Moller JH, Hoffman JIE (eds). Pediatric Cardiovascular Medicine. Churchill Livingstone, Philadelphia, 2000: 320.Google Scholar
8.Larsen, WJ. Development of the heart. In: Sherman LS, Potter SS, Scott WJ (eds). Human Embryology. Churchill Livingstone, New York, 1999: 157180.Google Scholar
9.Schoenwolf, GC, Bleyl, SB, Brauer, PR, Francis-West, PH. Larsen’s Human Embryology. Churchill Livingstone, New York, 2008.Google Scholar
10.Cook, AC, Yates, RW, Anderson, RH. Normal and abnormal fetal cardiac anatomy. Prenat Diagn 2004; 24: 10321048.Google Scholar
11.Anderson, RH, Yen Ho, S. Sequential segmental analysis – description and categorisation for the millennium. Cardiol Young 1997; 7: 98116.CrossRefGoogle Scholar
12.Timor-Tritsch, IE, Farine, D, Rosen, MG. A close look at early embryonic development with the high-frequency transvaginal transducer. Am J Obstet Gynecol 1988; 159: 676681.Google Scholar
13.Timor-Tritsch, IE, Peisner, DB, Raju, S. Sonoembryology: an organ-oriented approach using a high-frequency vaginal probe. J Clin Ultrasound 1990; 18: 286298.Google Scholar
14.D’Amelio, R, Giorlandino, C, Masala, L, et al. Fetal echocardiography using transvaginal and transabdominal probes during the first period of pregnancy: a comparative study. Prenat Diagn 1991; 11: 6975.Google Scholar
15.Blaas, HG, Eik-Nes, SH, Kiserud, T, Hellevik, LR. Early development of the abdominal wall, stomach and heart from 7 to 12 weeks of gestation: a longitudinal ultrasound study. Ultrasound Obstet Gynecol 1995; 6: 240249.Google Scholar
16.Allan, LD, Santos, R, Pexieder, T. Anatomical and echocardiographic correlates of normal cardiac morphology in the late first trimester fetus. Heart 1997; 77: 6872.Google Scholar
17.Johnson, P, Sharland, G, Maxwell, D, Allan, L. The role of transvaginal sonography in the early detection of congenital heart disease. Ultrasound Obstet Gynecol 1992; 2: 248251.Google Scholar
18.Carvalho, JS, Moscoso, G, Ville, Y. First-trimester transabdominal fetal echocardiography. Lancet 1998; 351: 10231027.Google Scholar
19.Simpsom, JM, Jones, A, Callaghan, N, Sharland, GK. Accuracy and limitations of transabdominal fetal echocardiography at 12–15 weeks of gestation in a population at high risk for congenital heart disease. BJOG 2000; 107: 14921497.Google Scholar
20.Huggon, IC, DeFigueiredo, DB, Allan, LD. Tricuspid regurgitation in the diagnosis of chromosomal anomalies in the fetus at 11–14 weeks of gestation. Heart 2003; 89: 10711073.Google Scholar
21.Carvalho, JS, Moscoso, G, Tekay, A, Campbell, S, Thilaganathan, B, Shinebourne, EA. Clinical impact of first and early second trimester fetal echocardiography on high risk pregnancies. Heart 2004; 90: 921926.CrossRefGoogle ScholarPubMed
22.Persico, N, Moratalla, J, Lombardi, CM, Zidere, V, Allan, L, Nicolaides, KH. Fetal echocardiography at 11–13 weeks by transabdominal high-frequency ultrasound. Ultrasound Obstet Gynecol 2011; 37: 296301.Google Scholar
23.Bellotti, M, Fesslova, V, De, GC, et al. Reliability of the first-trimester cardiac scan by ultrasound-trained obstetricians with high-frequency transabdominal probes in fetuses with increased nuchal translucency. Ultrasound Obstet Gynecol 2010; 36: 272278.CrossRefGoogle ScholarPubMed
24.Rasiah, SV, Publicover, M, Ewer, AK, Khan, KS, Kilby, MD, Zamora, J. A systematic review of the accuracy of first-trimester ultrasound examination for detecting major congenital heart disease. Ultrasound Obstet Gynecol 2006; 28: 110116.Google Scholar
25.Gembruch, U, Shi, C, Smrcek, JM. Biometry of the fetal heart between 10 and 17 weeks of gestation. Fetal Diagn Ther 2000; 15: 2031.Google Scholar
26.DeVore, GR, Steiger, RM, Larson, EJ. Fetal echocardiography: the prenatal diagnosis of a ventricular septal defect in a 14-week fetus with pulmonary artery hypoplasia. Obstet Gynecol 1987; 69: 494497.Google Scholar
27.Gembruch, U, Knopfle, G, Chatterjee, M, Bald, R, Hansmann, M. First-trimester diagnosis of fetal congenital heart disease by transvaginal two-dimensional and Doppler echocardiography. Obstet Gynecol 1990; 75: 496498.Google Scholar
28.Bronshtein, M, Siegler, E, Yoffe, N, Zimmer, EZ. Prenatal diagnosis of ventricular septal defect and overriding aorta at 14 weeks’ gestation, using transvaginal sonography. Prenat Diagn 1990; 10: 697702.Google Scholar
29.Dolkart, LA, Reimers, FT. Transvaginal fetal echocardiography in early pregnancy: normative data. Am J Obstet Gynecol 1991; 165: 688691.Google Scholar
30.Allan, LD, Crawford, DC, Chita, SK, Tynan, MJ. Prenatal screening for congenital heart disease. Br Med J (Clin Res Ed) 1986; 292: 17171719.Google Scholar
31.Copel, JA, Pilu, G, Green, J, Hobbins, JC, Kleinman, CS. Fetal echocardiographic screening for congenital heart disease: the importance of the four-chamber view. Am J Obstet Gynecol 1987; 157: 648655.Google Scholar
32.Haak, MC, Van Vugt, JM. Echocardiography in early pregnancy: review of literature. J Ultrasound Med 2003; 22: 271280.Google Scholar
33.Votino, C, Jani, J, Verhoye, M, et al. Postmortem examination of human fetal hearts at or below 20 weeks’ gestation: a comparison of high-field MRI at 9.4T with lower-field MRI magnets and stereomicroscopic autopsy. Ultrasound Obstet Gynecol 2012; 40: 437444.Google Scholar
34.Timor-Tritsch, IE, Fuchs, KM, Monteagudo, A, D’alton, ME. Performing a fetal anatomy scan at the time of first-trimester screening. Obstet Gynecol 2009; 113: 402407.Google Scholar
35.Scherptong, RW, Jongbloed, MR, Wisse, LJ, et al. Morphogenesis of outflow tract rotation during cardiac development: the pulmonary push concept. Dev Dyn 2012; 241: 14131422.Google Scholar
36.Sklansky, MS, Berman, DP, Pruetz, JD, Chang, RK. Prenatal screening for major congenital heart disease: superiority of outflow tracts over the 4-chamber view. J Ultrasound Med 2009; 28: 889899.Google Scholar
37.Haak, MC, Twisk, JW, Van Vugt, JM. How successful is fetal echocardiographic examination in the first trimester of pregnancy? Ultrasound Obstet Gynecol 2002; 20: 913.Google Scholar
38.McAuliffe, FM, Trines, J, Nield, LE, Chitayat, D, Jaeggi, E, Hornberger, LK. Early fetal echocardiography – a reliable prenatal diagnosis tool. Am J Obstet Gynecol 2005; 193: 12531259.Google Scholar
39.Blyth, M, Howe, D, Gnanapragasam, J, Wellesley, D. The hidden mortality of transposition of the great arteries and survival advantage provided by prenatal diagnosis. BJOG 2008; 115: 10961100.Google Scholar
40.Sharland, G. Fetal cardiac screening: why bother? Arch Dis Child Fetal Neonatal Ed 2010; 95: F64F68.Google Scholar
41.Westin, M, Saltvedt, S, Bergman, G, et al. Routine ultrasound examination at 12 or 18 gestational weeks for prenatal detection of major congenital heart malformations? A randomised controlled trial comprising 36,299 fetuses. BJOG 2006; 113: 675682.Google Scholar
42.Volpe, P, Ubaldo, P, Volpe, N, et al. Fetal cardiac evaluation at 11–14 weeks by experienced obstetricians in a low-risk population. Prenat Diagn 2011; 31: 10541061.Google Scholar
43.Grande, M, Arigita, M, Borobio, V, Jimenez, JM, Fernandez, S, Borrell, A. First-trimester detection of structural abnormalities and the role of aneuploidy markers. Ultrasound Obstet Gynecol 2012; 39: 157163.Google Scholar
44.Syngelaki, A, Chelemen, T, Dagklis, T, Allan, L, Nicolaides, KH. Challenges in the diagnosis of fetal non-chromosomal abnormalities at 11–13 weeks. Prenat Diagn 2011; 31: 90102.Google Scholar
45.Rissanen, A, Niemimaa, M, Suonpaa, M, Ryynanen, M, Heinonen, S. First trimester Down’s syndrome screening shows high detection rate for trisomy 21, but poor performance in structural abnormalities – regional outcome results. Fetal Diagn Ther 2007; 22: 4550.Google Scholar
46.Bartelings, MM, Gittenberger-de Groot, AC. Morphogenetic considerations on congenital malformations of the outflow tract. Part 2:complete transposition of the great arteries and double outlet right ventricle. Int J Cardiol 1991; 33: 526.Google Scholar
47.Liebman, J, Cullum, L, Belloc, NB. Natural history of transpositon of the great arteries. Anatomy and birth and death characteristics. Circulation 1969; 40: 237262.CrossRefGoogle ScholarPubMed
48.Pinto, NM, Keenan, HT, Minich, LL, Puchalski, MD, Heywood, M, Botto, LD. Barriers to prenatal detection of congenital heart disease: a population-based study. Ultrasound Obstet Gynecol 2012; 40: 418425.Google Scholar
49.Christensen, N, Andersen, H, Garne, E, et al. Atrioventricular septal defects among infants in Europe: a population-based study of prevalence, associated anomalies, and survival. Cardiol Young 2012: 18.Google Scholar
50.Cohen, MS, Jacobs, ML, Weinberg, PM, Rychik, J. Morphometric analysis of unbalanced common atrioventricular canal using two-dimensional echocardiography. J Am Coll Cardiol 1996; 28: 10171023.CrossRefGoogle ScholarPubMed
51.Yildirim, G, Gungorduk, K, Yazicioglu, F, et al. Prenatal diagnosis of complete atrioventricular septal defect: perinatal and neonatal outcomes. Obstet Gynecol Int 2009: 958496.Google Scholar
52.Peoples, WM, Moller, JH, Edwards, JE. Polysplenia: a review of 146 cases. Pediatr Cardiol 1983; 4: 129137.Google Scholar
53.Irving, CA, Chaudhari, MP. Cardiovascular abnormalities in Down’s syndrome: spectrum, management and survival over 22 years. Arch Dis Child 2012; 97: 326330.Google Scholar
54.Allan, LD. Development of congenital lesions in mid or late gestation. Int J Cardiol 1988; 19: 361362.Google Scholar
55.Allan, LD. Evolution of echocardiographic findings in the fetus. Circulation 1997; 96: 391392.Google Scholar
56.Todros, T, Presbitero, P, Gaglioti, P, Demarie, D. Pulmonary stenosis with intact ventricular septum: documentation of development of the lesion echocardiographically during fetal life. Int J Cardiol 1988; 19: 355362.Google Scholar
57.Rice, MJ, McDonald, RW, Reller, MD. Progressive pulmonary stenosis in the fetus: two case reports. Am J Perinatol 1993; 10: 424427.Google Scholar
58.Allan, LD, Crawford, DC, Tynan, M. Evolution of coarctation of the aorta in intra-uterine life. Brit Heart J 1984; 52: 471473.CrossRefGoogle Scholar
59.Allan, LD, Sharland, G, Tynan, MJ. The natural history of the hypoplastic left heart syndrome. Int J Cardiol 1989; 25: 341343.Google Scholar
60.Yagel, S, Weissman, A, Rotstein, Z, et al. Congenital heart defects: natural course and in utero development. Circulation 1997; 96: 550555.Google Scholar
61.Weiner, Z, Weizman, B, Beloosesky, R, Goldstein, I, Bombard, A. Fetal cardiac scanning performed immediately following an abnormal nuchal translucency examination. Prenat Diagn 2008; 28: 934938.Google Scholar
62.Hartge, DR, Weichert, J, Krapp, M, Germer, U, Gembruch, U, Axt-Fliedner, R. Results of early foetal echocardiography and cumulative detection rate of congenital heart disease. Cardiol Young 2011; 21: 505517.Google Scholar
63.Eleftheriades, M, Tsapakis, E, Sotiriadis, A, Manolakos, E, Hassiakos, D, Botsis, D. Detection of congenital heart defects throughout pregnancy; impact of first trimester ultrasound screening for cardiac abnormalities. J Matern Fetal Neonatal Med 2012; 25: 25462550.Google Scholar
64.Garne, E, Stoll, C, Clementi, M. Evaluation of prenatal diagnosis of congenital heart diseases by ultrasound: experience from 20 European registries. Ultrasound Obstet Gynecol 2001; 17: 386391.CrossRefGoogle ScholarPubMed
65.Jaeggi, ET, Sholler, GF, Jones, OD, Cooper, SG. Comparative analysis of pattern, management and outcome of pre- versus postnatally diagnosed major congenital heart disease: a population-based study. Ultrasound Obstet Gynecol 2001; 17: 380385.Google Scholar
66.Paladini, D, Palmieri, S, Lamberti, A, Teodoro, A, Martinelli, P, Nappi, C. Characterization and natural history of ventricular septal defects in the fetus. Ultrasound Obstet Gynecol 2000; 16: 118122.Google Scholar
67.Rustico, MA, Benettoni, A, D'Ottavio, G, et al. Early screening for fetal cardiac anomalies by transvaginal echocardiography in an unselected population: the role of operator experience. Ultrasound Obstet Gynecol 2000; 16: 614619.Google Scholar
68.Stoll, C, Alembik, Y, Dott, B, et al. Evaluation of prenatal diagnosis of congenital heart disease. Prenat Diagn 1998; 18: 801807.Google Scholar
69.Queisser-Luft, A, Stopfkuchen, H, Stolz, G, Schlaefer, K, Merz, E. Prenatal diagnosis of major malformations: quality control of routine ultrasound examinations based on a five-year study of 20,248 newborn fetuses and infants. Prenat Diagn 1998; 18: 567576.Google Scholar
70.Todros, T, Faggiano, F, Chiappa, E, Gaglioti, P, Mitola, B, Sciarrone, A. Accuracy of routine ultrasonography in screening heart disease prenatally. Gruppo Piemontese for Prenatal Screening of Congenital Heart Disease. Prenat Diagn 1997; 17: 901906.Google Scholar
71.Kirk, JS, Comstock, CH, Lee, W, Smith, RS, Riggs, TW, Weinhouse, E. Sonographic screening to detect fetal cardiac anomalies: a 5-year experience with 111 abnormal cases. Obstet Gynecol 1997; 89: 227232.Google Scholar
72.Queisser-Luft, A, Stolz, G, Wiesel, A, Schlaefer, K, Spranger, J. Malformations in newborn: results based on 30,940 infants and fetuses from the Mainz congenital birth defect monitoring system (1990–1998). Arch Gynecol Obstet 2002; 266: 163167.Google Scholar
73.Gembruch, U, Knopfle, G, Bald, R, Hansmann, M. Early diagnosis of fetal congenital heart disease by transvaginal echocardiography. Ultrasound Obstet Gynecol 1993; 3: 310317.Google Scholar
74.Vimpelli, T, Huhtala, H, Acharya, G. Fetal echocardiography during routine first-trimester screening: a feasibility study in an unselected population. Prenat Diagn 2006; 26: 475482.Google Scholar
75.Smrcek, JM, Berg, C, Geipel, A, Fimmers, R, Diedrich, K, Gembruch, U. Early fetal echocardiography: heart biometry and visualization of cardiac structures between 10 and 15 weeks' gestation. J Ultrasound Med 2006; 25: 173182.Google Scholar
76.Areias, JC, Matias, A, Montenegro, N, Brandao, O. Early antenatal diagnosis of cardiac defects using transvaginal Doppler ultrasound: new perspectives? Fetal Diagn Ther 1998; 13: 111114.Google Scholar
77.Achiron, R, Rotstein, Z, Lipitz, S, Mashiach, S, Hegesh, J. First-trimester diagnosis of fetal congenital heart disease by transvaginal ultrasonography. Obstet Gynecol 1994; 84: 6972.Google Scholar
78.Baschat, AA, Gembruch, U, Knopfle, G, Hansmann, M. First-trimester fetal heart block: a marker for cardiac anomaly. Ultrasound Obstet Gynecol 1999; 14: 311314.CrossRefGoogle Scholar
79.Haak, MC, Bartelings, MM, Gittenberger-de Groot, AC, Van Vugt, JM. Cardiac malformations in first-trimester fetuses with increased nuchal translucency: ultrasound diagnosis and postmortem morphology. Ultrasound Obstet Gynecol 2002; 20: 1421.Google Scholar
80.Huggon, IC, Ghi, T, Cook, AC, Zosmer, N, Allan, LD, Nicolaides, KH. Fetal cardiac abnormalities identified prior to 14 weeks’ gestation. Ultrasound Obstet Gynecol 2002; 20: 2229.Google Scholar
81.Comas, GC, Galindo, A, Martinez, JM, et al. Early prenatal diagnosis of major cardiac anomalies in a high-risk population. Prenat Diagn 2002; 22: 586593.Google Scholar
82.Galindo, A, Comas, C, Martinez, JM, et al. Cardiac defects in chromosomally normal fetuses with increased nuchal translucency at 10–14 weeks of gestation. J Matern Fetal Neonatal Med 2003; 13: 163170.Google ScholarPubMed
83.Becker, R, Wegner, RD. Detailed screening for fetal anomalies and cardiac defects at the 11–13-week scan. Ultrasound Obstet Gynecol 2006; 27: 613618.Google Scholar
84.Bronshtein, M, Zimmer, EZ, Milo, S, Ho, SY, Lorber, A, Gerlis, LM. Fetal cardiac abnormalities detected by transvaginal sonography at 12–16 weeks’ gestation. Obstet Gynecol 1991; 78: 374378.Google Scholar
85.Axt-Fliedner, R, Kreiselmaier, P, Schwarze, A, Krapp, M, Gembruch, U. Development of hypoplastic left heart syndrome after diagnosis of aortic stenosis in the first trimester by early echocardiography. Ultrasound Obstet Gynecol 2006; 28: 106109.Google Scholar
86.Prefumo, F, Bhide, A, Thilaganathan, B, Carvalho, JS. Fetal congenital cardiac diverticulum with pericardial effusion: two cases with different presentations in the first trimester of pregnancy. Ultrasound Obstet Gynecol 2005; 25: 405408.Google Scholar
87.Jongbloed, MR, Mahtab, EAF, Blom, NA, Schalij, MJ, Gittenberger-de Groot, AC. Development of the cardiac conduction system and the possible relation to predilection sites of arrhythmogenesis. ScientificWorldJournal 2008; 8: 239269.Google Scholar