REVIEW
Fetal cardiac function evaluation: A review
Lorenzo Vasciaveo,
Erika Zanzarelli,
Francesco D'Antonio,
Corresponding Author
Lorenzo Vasciaveo
Maternal Fetal Medicine Unit, Department of Obstetrics and Gynaecology, University of Foggia, Foggia, Italy
Correspondence
Lorenzo Vasciaveo, Department of Obstetrics and Gynaecology, University of Foggia, Foggia, Italy.
Email: [email protected]
Search for more papers by this authorErika Zanzarelli
Maternal Fetal Medicine Unit, Department of Obstetrics and Gynaecology, University of Foggia, Foggia, Italy
Search for more papers by this authorFrancesco D'Antonio
Centre for High-Risk Pregnancy and Fetal Care, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy
Search for more papers by this authorLorenzo Vasciaveo,
Erika Zanzarelli,
Francesco D'Antonio,
Corresponding Author
Lorenzo Vasciaveo
Maternal Fetal Medicine Unit, Department of Obstetrics and Gynaecology, University of Foggia, Foggia, Italy
Correspondence
Lorenzo Vasciaveo, Department of Obstetrics and Gynaecology, University of Foggia, Foggia, Italy.
Email: [email protected]
Search for more papers by this authorErika Zanzarelli
Maternal Fetal Medicine Unit, Department of Obstetrics and Gynaecology, University of Foggia, Foggia, Italy
Search for more papers by this authorFrancesco D'Antonio
Centre for High-Risk Pregnancy and Fetal Care, Department of Obstetrics and Gynecology, University of Chieti, Chieti, Italy
Search for more papers by this authorAbstract
The aim of this review is to provide an up to date on the current use of fetal echocardiography in assessing the fetal cardiac function and its potential research and clinical applications. Despite classically is been used for prenatal diagnosis of fetal heart defects, assessment of fetal cardiac function has been recently proposed as a fundamental tool to assess pregnancies complicated by several disorders with long-term impact on post-natal cardiovascular health, such as placental insufficiency and fetal growth restriction. In this review we present anatomical and functional fetal cardiac development mechanisms and an overview of the currently available techniques for evaluating fetal heart function.
Open Research
DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created or analyzed in this study.
REFERENCES
- 1Van Mieghem T, Gucciardo L, Doné E, et al. Left ventricular cardiac function in fetuses with congenital diaphragmatic hernia and the effect of fetal endoscopic tracheal occlusion. Ultrasound Obstet Gynecol. 2009; 34(4): 424-429.
- 2Crispi F, Gratacós E. Fetal cardiac function: technical considerations and potential research and clinical applications. Fetal Diagn Ther. 2012; 32(1–2): 47-64.
- 3Jessup M, Abraham WT, Casey DE, et al. 2009 focused update: ACCF/AHA guidelines for the diagnosis and Management of Heart Failure in adults: a report of the American College of Cardiology Foundation/American Heart Association Task Force on practice guidelines: developed in collaboration with the International Society for Heart and Lung Transplantation. Circulation. 2009; 119(14): 1977-2016.
- 4Huhta JC. Guidelines for the evaluation of heart failure in the fetus with or without hydrops. Pediatr Cardiol. 2004; 25(3): 274-286.
- 5Crispi F, Hernandez-Andrade E, Pelsers MM, et al. Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses. Am J Obstet Gynecol. 2008; 199(3): 254.e1-254.e8.
- 6Opie LH, Commerford PJ, Gersh BJ, Pfeffer MA. Controversies in ventricular remodelling. Lancet. 2006; 367(9507): 356-367.
- 7Möllmann H, Nef HM, Kostin S, et al. Ischemia triggers BNP expression in the human myocardium independent from mechanical stress. Int J Cardiol. 2010; 143: 289-297.
- 8Iruretagoyena JI, Gonzalez-Tendero A, Garcia-Canadilla P, et al. Cardiac dysfunction is associated with altered sarcomere ultrastructure in intrauterine growth restriction. Am J Obstet Gynecol. 2014; 210(6): 550.e1-550.e7.
- 9Jouk PS, Usson Y, Michalowicz G, Grossi L. Three-dimensional cartography of the pattern of the myofibres in the second trimester fetal human heart. Anat Embryol (Berl). 2000; 202(2): 103-118.
- 10Fernandez-Teran MA, Hurle JM. Myocardial fiber architecture of the human heart ventricles. Anat Rec. 1982; 204(2): 137-147.
- 11Godfrey ME, Messing B, Cohen SM, Valsky DV, Yagel S. Functional assessment of the fetal heart: a review. Ultrasound Obstet Gynecol. 2012; 39(2): 131-144.
- 12Simpson J. Echocardiographic evaluation of cardiac function in the fetus. Prenat Diagn. 2004; 24(13): 1081-1091. doi:10.1002/pd.1065
- 13Hall JE. Guyton and Hall textbook of medical physiology. Guyton Physiology. 12th ed. W B Saunders; 2015.
- 14Namana V, Gupta SS, Sabharwal N. G Hollander, clinical significance of atrial kick. QJM. 2018; 111(8): 569-570.
- 15Cohn JN, Ferrari R, Sharpe N. Cardiac remodeling–concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an international forum on cardiac remodeling. J Am Coll Cardiol. 2000; 35(3): 569-582.
- 16Garcia-Canadilla P, Dejea H, Bonnin A, et al. Complex congenital heart disease associated with disordered myocardial architecture in a Midtrimester human fetus. Circ Cardiovasc Imaging. 2018; 11(10):e007753.
- 17Soveral I, Crispi F, Walter C, et al. Early cardiac remodeling in aortic coarctation: insights from fetal and neonatal functional and structural assessment. Ultrasound Obstet Gynecol. 2020; 56(6): 837-849.
- 18Valenzuela-Alcaraz B, Crispi F, Bijnens B, et al. Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally. Circulation. 2013; 128(13): 1442-1450.
- 19Rizzo G, Pietrolucci ME, Mappa I, et al. Fetal cardiac remodeling is affected by the type of embryo transfer in pregnancies conceived by in vitro fertilization: a prospective cohort study. Fetal Diagn Ther. 2020; 13: 1-7.
- 20Boutet ML, Casals G, Valenzuela-Alcaraz B, et al. Cardiac remodeling in fetuses conceived by ARTs: fresh versus frozen embryo transfer. Hum Reprod. 2021; 36(10): 2697-2708.
- 21Rodríguez-López M, Cruz-Lemini M, Valenzuela-Alcaraz B, et al. Descriptive analysis of different phenotypes of cardiac remodeling in fetal growth restriction. Ultrasound Obstet Gynecol. 2017; 50(2): 207-214.
- 22Rizzo G, Mattioli C, Mappa I, et al. Hemodynamic factors associated with fetal cardiac remodeling in late fetal growth restriction: a prospective study. J Perinat Med. 2019; 47(7): 683-688.
- 23Patey O, Carvalho JS, Thilaganathan B. Perinatal changes in fetal cardiac geometry and function in diabetic pregnancy at term. Ultrasound Obstet Gynecol. 2019; 54(5): 634-642.
- 24Rizzo G, Pietrolucci ME, Mappa I, Bitsadze V, Khizroeva J, Makatsariya A. Fetal cardiac remodelling in pregnancies complicated by gestational diabetes mellitus: a prospective cohort study. Prenatal Cardiol. 2020; 1: 13-18. doi:10.5114/pcard.2020.94558
10.5114/pcard.2020.94558 Google Scholar
- 25Rizzo G, Mappa I, Pietrolucci ME, Lu JL, Makatsarya A, D'Antonio F. Effect of SARS-CoV-2 infection on fetal umbilical vein flow and cardiac function: a prospective study. J Perinat Med. 2022; 50(4): 398-403.
- 26García-Otero L, López M, Gómez O, et al. Zidovudine treatment in HIV-infected pregnant women is associated with fetal cardiac remodelling. Aids. 2016; 30(9): 1393-1401.
- 27Bijnens B, Cikes M, Butakoff C, Sitges M, Crispi F. Myocardial motion and deformation: what does it tell us and how does it relate to function? Fetal Diagn Ther. 2012; 32(1–2): 5-16.
- 28García-Otero L, Gómez O, Rodriguez-López M, et al. Nomograms of Fetal cardiac dimensions at 18-41 weeks of gestation. Fetal Diagn Ther. 2020; 47(5): 387-398.
- 29DeVore GR, Siassi B, Platt LD. Fetal echocardiography. IV. M-mode assessment of ventricular size and contractility during the second and third trimesters of pregnancy in the normal fetus. Am J Obstet Gynecol. 1984; 150:981e8.
- 30Tan J, Silverman NH, Hoffman JI, Villegas M, Schmidt KG. Cardiac dimensions determined by cross-sectional echocardiography in the normal human fetus from 18 weeks to term. Am J Cardiol. 1992; 70(18): 1459-1467.
- 31Sharland GK, Allan LD. Normal fetal cardiac measurements derived by cross-sectional echocardiography. Ultrasound Obstet Gynecol. 1992; 2: 175e81-175e181.
- 32Shapiro I, Degani S, Leibovitz Z, Ohel G, Tal Y, Abinader EG. Fetal cardiac measurements derived by transvaginal and transabdominal cross-sectional echocardiography from 14 weeks of gestation to term. Ultrasound Obstet Gynecol. 1998; 12: 404e18-404e418.
- 33DeVore GR. Assessing fetal cardiac ventricular function. Semin Fetal Neonatal Med. 2005; 10(6): 515-541.
- 34Di Salvo G, Russo MG, Castaldi B, et al. Settore Ricerca della Società Italiana di Ecografia; Cardiovascolare (SIEC). Valutazione della funzione cardiaca in epoca fetale [Evaluation of ventricular function in the fetus]. G Ital Cardiol (Rome). 2009; 10(8): 499-508.
- 35Hernandez-Andrade E, López-Tenorio J, Figueroa-Diesel H, et al. A modified myocardial performance (Tei) index based on the use of valve clicks improves reproducibility of fetal left cardiac function assessment. Ultrasound Obstet Gynecol. 2005; 26(3): 227-232.
- 36Lee W, Allan L, Carvalho JS, et al. ISUOG consensus statement: what constitutes a fetal echocardiogram? Ultrasound Obstet Gynecol. 2008; 32(2): 239-242.
- 37Baschat AA, Cosmi E, Bilardo CM, et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol. 2007; 109(2 Pt 1): 253-261.
- 38Timmerman E, Clur SA, Pajkrt E, Bilardo CM. First-trimester measurement of the ductus venosus pulsatility index and the prediction of congenital heart defects. Ultrasound Obstet Gynecol. 2010; 36(6): 668-675.
- 39Biering-Sørensen T, Mogelvang R, de Knegt MC, Olsen FJ, Galatius S, Jensen JS. Cardiac time intervals by tissue Doppler imaging M-mode: normal values and association with established echocardiographic and invasive measures of systolic and diastolic function. PLoS One. 2016; 11(4):e0153636.
- 40Tei C, Nishimura RA, Seward JB, Tajik AJ. Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements. J Am Soc Echocardiogr. 1997; 10: 169-178.
- 41Friedman D, Buyon J, Kim M, Glickstein JS. Fetal cardiac function assessed by Doppler myocardial performance index (Tei index). Ultrasound Obstet Gynecol. 2003; 21(1): 33-36.
- 42Crispi F, Sepulveda-Swatson E, Cruz-Lemini M, et al. Feasibility and reproducibility of a standard protocol for 2D speckle tracking and tissue Doppler-based strain and strain rate analysis of the fetal heart. Fetal Diagn Ther. 2012; 32(1–2): 96-108.
- 43Chaoui R, Heling KS. New developments in fetal heart scanning: three- and four-dimensional fetal echocardiography. Semin Fetal Neonatal Med. 2005; 10(6): 567-577.
- 44Bennasar M, Martínez JM, Gómez O, et al. Intra- and interobserver repeatability of fetal cardiac examination using four-dimensional spatiotemporal image correlation in each trimester of pregnancy. Ultrasound Obstet Gynecol. 2010; 35(3): 318-323.
- 45DeVore GR, Falkensammer P, Sklansky MS, Platt LD. Spatio-temporal image correlation (STIC): new technology for evaluation of the fetal heart. Ultrasound Obstet Gynecol. 2003; 22(4): 380-387.
- 46Gonçalves LF, Espinoza J, Romero R, et al. A systematic approach to prenatal diagnosis of transposition of the great arteries using 4-dimensional ultrasonography with spatiotemporal image correlation. J Ultrasound Med. 2004; 23(9): 1225-1231.
- 47Chiappa EM, Cook AC, Botta G, Silverman NH. Echocardiographic Anatomy in the Fetus. Springer; 2009.
- 48DeVore GR, Satou G, Sklansky M. 4D fetal echocardiography-an update. Echocardiography. 2017; 34(12): 1788-1798.
- 49Nogué L, Gómez O, Izquierdo N, et al. Feasibility of 4D-spatio temporal image correlation (STIC) in the comprehensive assessment of the fetal heart using FetalHQ®. J Clin Med. 2022; 11(5): 1414.
- 50Luo Y, Xiao F, Long C, et al. Evaluation of the sphericity index of the fetal heart during middle and late pregnancy using fetalHQ. J Matern Fetal Neonatal Med. 2021; 23: 1-6.
- 51DeVore GR, Satou G, Sklansky M. Abnormal fetal findings associated with a global Sphericity index of the 4-chamber view below the 5th centile. J Ultrasound Med. 2017; 36(11): 2309-2318.
- 52DeVore GR, Klas B, Satou G, Sklansky M. Twenty-four segment transverse ventricular fractional shortening: a new technique to evaluate Fetal cardiac function. J Ultrasound Med. 2018; 37(5): 1129-1141.
- 53García-Otero L, Soveral I, Sepúlveda-Martínez Á, et al. Reference ranges for fetal cardiac, ventricular and atrial relative size, sphericity, ventricular dominance, wall asymmetry and relative wall thickness from 18 to 41 gestational weeks. Ultrasound Obstet Gynecol. 2021; 58(3): 388-397.
- 54Crispi F, Sepúlveda-Martínez Á, Crovetto F, Gómez O, Bijnens B, Gratacós E. Main patterns of Fetal cardiac remodeling. Fetal Diagn Ther. 2020; 47(5): 337-344.
- 55Demicheva E, Crispi F. Long-term follow-up of intrauterine growth restriction: cardiovascular disorders. Fetal Diagn Ther. 2014; 36(2): 143-153.
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