Ultrasound assessment of fetal cardiac function

Fàtima Crispi, Brenda Valenzuela-Alcaraz, Monica Cruz-Lemini, Eduard Gratacós, Fàtima Crispi, Brenda Valenzuela-Alcaraz, Monica Cruz-Lemini, Eduard Gratacós

Abstract

Introduction: Fetal heart evaluation with US is feasible and reproducible, although challenging due to the smallness of the heart, the high heart rate and limited access to the fetus. However, some cardiac parameters have already shown a strong correlation with outcomes and may soon be incorporated into clinical practice. Materials and Methods: Cardiac function assessment has proven utility in the differential diagnosis of cardiomyopathies or prediction of perinatal mortality in congenital heart disease. In addition, some cardiac parameters with high sensitivity such as MPI or annular peak velocities have shown promising results in monitoring and predicting outcome in intrauterine growth restriction or congenital diaphragmatic hernia. Conclusion: Cardiac function can be adequately evaluated in most fetuses when appropriate expertise, equipment and time are available. Fetal cardiac function assessment is a promising tool that may soon be incorporated into clinical practice to diagnose, monitor or predict outcome in some fetal conditions. Thus, more research is warranted to further define specific protocols for each fetal condition that may affect cardiac function.

Keywords: 4D STIC; echocardiography; fetal cardiac function; myocardial imaging; tissue Doppler.

Figures

Figure 1
Figure 1
Graphic representation of the three‐directional myocardial motility involving longitudinal, radial and circumferential contraction. The motion is shown as a single point motility determined by displacement and systolic (s') and early diastolic (E') annular peak velocities; and deformation by the change in length or thickness between two points represented as strain or strain rate.
Figure 2
Figure 2
Illustration of the right and left ventricular outflow tracts for measuring stroke volume (SV) and cardiac output (CO). The valve diameter (D) is measured in a 2D image. Velocity time integral (VTI) of the blood flow and heart rate (HR) are evaluated in the spectral Doppler waveform. Combined cardiac output (CCO) is calculated by the sum of both CO, and cardiac index (CI) represents the normalization by estimated fetal weight (EFW).
Figure 3
Figure 3
Image of the E/A ratio evaluation. The sample gate is placed just below the atrio‐ventricular valves in a four‐chamber view in order to display biphasic inflow (including the E (early diastole) and A (atrial contraction).
Figure 4
Figure 4
Illustration of myocardial performance index (MPI) assessment by spectral Doppler. Placing the Doppler sample volume in a four‐chamber view on the medial wall of the ascending aorta, the mitral biphasic inflow (grey arrow, early (E) and atrial (A) waveforms) and the aortic outflow (blue arrow and waveform (Ao)) are displayed in the same spectral image. The MPI is calculated by measuring time intervals including: isovolumic contraction time (ICT) from the closure of the mitral valve to the opening of the aortic valve; ejection time (ET) from the opening to closure of the aorta; and isovolumic relxaxation time (IRT) from the closure of the aortic valve to the opening of the mitral valve.
Figure 5
Figure 5
Illustration of a transverse four‐chamber view in order to measure shortening (SF) and ejection fractions (EF) of the right (RV) and left ventricles (LV) by M‐mode. The arrows between the septal and right free walls show the measurement of end‐diastolic (EDD) and end systolic (ESD) diameters required for the SF and EF calculation. RVW= right ventricle wall; LVW= left ventricle wall.
Figure 6
Figure 6
Illustration of the tricuspid annular plane systolic excursion (TAPSE) measurement by applying M‐mode at the tricuspid valve annulus in an apical four‐chamber view.
Figure 7
Figure 7
Example of early (E') and late (A') diastolic and systolic (s') peak annular velocities obtained by spectral tissue Doppler at the right annulus.
Figure 8
Figure 8
Offline analysis of strain (above) and strain rate (below) waveforms at the right basal free wall using color tissue Doppler.
Figure 9
Figure 9
Offline analysis of regional and global strain waveforms of the left ventricle wall using 2D speckle tracking.
Figure 10
Figure 10
Post‐processing analysis of the left ventricular volume through virtual organ computerized analysis using 4D‐spatio temporal correlation.
Figure 11
Figure 11
Graphic representation of cardiac function parameters at the different stages of the fetal adaptation to disease, illustrating longitudinal and diastolic function becoming abnormal at earlier stages than radial and systolic. Ductus venosus, E/A ratios, myocardial performance index (MPI) and cardiac output are measured by conventional Doppler; ejection fraction and longitudinal displacement by M‐mode; systolic (s') and early diastolic (E') annular pea k velocities by spectral tissue Doppler; and strain and strain‐rate by offline tissue Doppler or 2D speckle tracking.

References

    1. Carvalho JS, Chaoui R, Copel JA, DeVore GR, Hecher K, Lee W, et al. ISUOG practice guidelines (updated): sonographic screening examination of the fetal heart. Ultrasound Obstet Gynecol 2013; (41): 348–59.
    1. Lee W, Allan L, Carvalho JS, Chaoui R, Copel J, Devore G, et al. ISUOG consensus statement: what constitutes a fetal echocardiogram? Ultrasound Obstet Gynecol 2008; 32 (2): 239–42.
    1. Rychik J, Tian Z, Bebbington M, Xu F, McCann M, Mann S, et al. The twin‐twin transfusion syndrome: spectrum of cardiovascular abnormality and development of a cardiovascular score to assess severity of disease. Am J Obstet Gynecol 2007; 197 (4): 392. e1–8.
    1. Crispi F, Hernandez‐Andrade E, Pelsers MM, Plasencia W, Benavides‐Serralde JA, Eixarch E, et al. Cardiac dysfunction and cell damage across clinical stages of severity in growth‐restricted fetuses. Am J Obstet Gynecol 2008; 199 (3): 254. e1–8.
    1. Van Mieghem T, Gucciardo L, Done E, Van Schoubroeck D, Graatsma EM, Visser GH, 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): 424–29.
    1. Jessup MA, Casey DE, Feldman AM, Francis GS, Ganiats TG, Konstam MA, 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; 14 (119): 1977–2016.
    1. Huhta JC. Guidelines for the evaluation of heart failure in the fetus with or without hydrops. Pediatr Cardiol 2004; 25 (3): 274–86.
    1. Opie LH, Commerford PJ, Gersh BJ. MA. P. Controversies in ventricular remodelling. Lancet 2006; 367: 356–67.
    1. Figueras F, Puerto B, Martinez JM, Cararach V, Vanrell JA. Cardiac function monitoring of fetuses with growth restriction. Eur J Obstet Gynecol Reprod Biol 2003; 110 (2): 159–63.
    1. Karatza AA, Wolfenden JL, Taylor MJ, Wee L, Fisk NM, Gardiner HM. Influence of twin‐twin transfusion syndrome on fetal cardiovascular structure and function: prospective case‐control study of 136 monochorionic twin pregnancies. Heart 2002; 88 (3): 271–77.
    1. Stirnemann JJ, Mougeot M, Proulx F, Nasr B, Essaoui M, Fouron JC, et al. Profiling fetal cardiac function in twin‐twin transfusion syndrome. Ultrasound Obstet Gynecol; 35 (1): 19–27.
    1. Gardiner HM, Pasquini L, Wolfenden J, Kulinskaya E, Li WMH. Increased periconceptional maternal glycated haemoglobin in diabetic mothers reduces fetal long axis cardiac function. Heart 2006; 92: 1125–30.
    1. Turan S, Turan OM, Miller J, Harman C, Reece EA, et al. Decreased fetal cardiac performance in the first trimester correlates with hyperglycemia in pre‐gestational maternal diabetes. Ultrasound Obstet Gynecol 2011; 38: 325–31.
    1. Stressig R, Fimmers R, Eising K, Gembruch U, Kohl T. Preferential streaming of the ductus venosus and inferior caval vein towards the right heart is associated with left heart underdevelopment in human fetuses with left‐sided diaphragmatic hernia. Heart; 96 (19): 1564–8.
    1. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989; 298 (6673): 564–67.
    1. Hennington BS, Alexander BT. Linking IUGR and Blood Pressure: Insight into the Human Origins of Cardiovascular Disease. Circulation 2013; Epub ahead of print.
    1. Bjarnegard N, Morsing E, Cinthio M, Lanne T, Brodszki J. Cardiovascular function in adulthood following intrauterine growth restriction with abnormal fetal blood flow. Ultrasound Obstet Gynecol 2013; 41 (2): 177–84.
    1. Brodszki J, Lanne T, Marsal K, Ley D. Impaired vascular growth in late adolescence after intrauterine growth restriction. Circulation 2005; 111 (20): 2623–28.
    1. Guyton AC. HJ. Textboook of Medical Phisiology. 12 ed. Philadelphia: Elsevier Saunders; 2011.
    1. Bijnens 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.
    1. Anderson RH, Smerup M, Sanchez‐Quintana D, Loukas M, Lunkenheimer PP. The three‐dimensional arrangement of the myocytes in the ventricular walls. Clin Anat 2009; 22 (1): 64–76.
    1. Tobita K, Garrison JB, Liu LJ, Tinney JP, Keller BB. Three‐dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. Anat Rec A Discov Mol Cell Evol Biol 2005; 283 (1): 193–201.
    1. AIUM practice guideline for the performance of fetal echocardiography. J Ultrasound Med 2011; 30 (1): 127–36.
    1. Hernandez‐Andrade E, Benavides‐Serralde JA, Cruz‐Martinez R, Welsh A, Mancilla‐Ramirez J. Evaluation of conventional Doppler fetal cardiac function parameters: E/A ratios, outflow tracts, and myocardial performance index. Fetal Diagn Ther; 32 (1–2): 22–29.
    1. Comas M, Crispi F, Gomez O, Puerto B, Figueras F, Gratacos E. Gestational age and estimated fetal weight‐adjusted reference ranges for myocardial tissue Doppler indices at 24–41 weeks' gestation. Ultrasound Obstet Gynecol 2011; 37 (1): 57–64.
    1. Comas M, Crispi F. Assessment of fetal cardiac function using tissue Doppler techniques. Fetal Diagn Ther 2012; 32 (1–2): 30–38.
    1. Germanakis I, Gardiner H. Assessment of fetal myocardial deformation using speckle tracking techniques. Fetal Diagn Ther 2012; 32 (1–2): 39–46.
    1. Carceller‐Blanchard AM, Fouron JC. Determinants of the Doppler flow velocity profile through the mitral valve of the human fetus. Br Heart J 1993; 70 (5): 457–60.
    1. Tulzer G, Khowsathit P, Gudmundsson S, Wood DC, Tian ZY, Schmitt K, et al. Diastolic function of the fetal heart during second and third trimester: a prospective longitudinal Doppler‐echocardiographic study. Eur J Pediatr 1994; 153 (3): 151–54.
    1. van der Mooren K, Barendregt LG, Wladimiroff JW. Fetal atrioventricular and outflow tract flow velocity waveforms during normal second half of pregnancy. Am J Obstet Gynecol 1991; 165 (3): 668–74.
    1. Rizzo G, Pietropolli A, Capponi A, Cacciatore C, Bufalino L, Arduini D, et al. Echocardiographic studies of the fetal heart. J Perinat Med 1994; 22 (Suppl 1): 46–50.
    1. Hernandez‐Andrade E, Figueroa‐Diesel H, Kottman C, Illanes S, Arraztoa J, Acosta‐Rojas R, et al. Gestational‐age‐adjusted reference values for the modified myocardial performance index for evaluation of fetal left cardiac function. Ultrasound Obstet Gynecol 2007; 29 (3): 321–25.
    1. Cruz‐Martinez R, Figueras F, Bennasar M, Garcia‐Posadas R, Crispi F, Hernandez‐Andrade E, et al. Normal reference ranges from 11 to 41 weeks' gestation of fetal left modified myocardial performance index by conventional Doppler with the use of stringent criteria for delimitation of the time periods. Fetal Diagn Ther 2012; 32 (1–2): 79–86.
    1. Eidem BW, Edwards JM, Cetta F. Quantitative assessment of fetal ventricular function: establishing normal values of the myocardial performance index in the fetus. Echocardiography 2001; 18 (1): 9–13.
    1. Meriki N, Welsh AW. Development of Australian reference ranges for the left fetal modified myocardial performance index and the influence of caliper location on time interval measurement. Fetal Diagn Ther 2012; 32: 87–95.
    1. Allan LD, Joseph MC, Boyd EG, Campbell S, Tynan M. M‐mode echocardiography in the developing human fetus. Br Heart J 1982; 47 (6): 573–83.
    1. Godfrey ME, Messing B, Valsky DV, Cohen SM, Yagel S. Fetal cardiac function: M‐mode and 4D spatiotemporal image correlation. Fetal Diagn Ther 2012; 32 (1–2): 17–21.
    1. DeVore 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 (8): 981–88.
    1. Quinones MA, Pickering E, Alexander JK. Percentage of shortening of the echocardiographic left ventricular dimension. Its use in determining ejection fraction and stroke volume. Chest 1978; 74 (1): 59–65.
    1. Carvalho JS, O'Sullivan C, Shinebourne EA, Henein MY. Right and left ventricular long‐axis function in the fetus using angular M‐mode. Ultrasound Obstet Gynecol 2001; 18 (6): 619–22.
    1. Gardiner HM, Pasquini L, Wolfenden J, Barlow A, Li W, Kulinskaya E, et al. Myocardial tissue Doppler and long axis function in the fetal heart. Int J Cardiol 2006; 113 (1): 39–47.
    1. Cruz‐Lemini M, Crispi F, Valenzuela‐Alcaraz B, Figueras F, Sitges M, Gomez O, et al. Value of annular M‐mode displacement versus tissue Doppler velocities to assess cardiac function in intrauterine growth restriction. Ultrasound Obstet Gynecol 2013; 42 (2): 175–181.
    1. Ho CY, Solomon SD. A clinician's guide to tissue Doppler imaging. Circulation 2006; 113 (10): e396–98.
    1. Acharya G, Pavlovic M, Ewing L, Nollmann D, Leshko J, Huhta JC. Comparison between pulsed‐wave Doppler‐ and tissue Doppler‐derived Tei indices in fetuses with and without congenital heart disease. Ultrasound Obstet Gynecol 2008; 31 (4): 406–11.
    1. Harada K, Tsuda A, Orino T, Tanaka T, Takada G. Tissue Doppler imaging in the normal fetus. Int J Cardiol 1999; 71 (3): 227–34.
    1. Comas M, Crispi F, Cruz‐Martinez R, Martinez JM, Figueras F, Gratacos E. Usefulness of myocardial tissue Doppler vs conventional echocardiography in the evaluation of cardiac dysfunction in early‐onset intrauterine growth restriction. Am J Obstet Gynecol 2010; 203 (1): 45. e1–7.
    1. Yu CM, Sanderson JE, Marwick TH, Oh JK. Tissue Doppler imaging a new prognosticator for cardiovascular diseases. J Am Coll Cardiol 2007; 49 (19): 1903–14.
    1. Crispi F, Sepulveda‐Swatson E, Cruz‐Lemini M, Rojas‐Benavente J, Garcia‐Posada R, Dominguez JM, 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.
    1. Bijnens BH, Cikes M, Claus P, Sutherland GR. Velocity and deformation imaging for the assessment of myocardial dysfunction. Eur J Echocardiogr 2009; 10 (2): 216–26.
    1. Van Mieghem T, Giusca S, DeKoninck P, Gucciardo L, Done E, Hindryckx A, et al. Prospective assessment of fetal cardiac function with speckle tracking in healthy fetuses and recipient fetuses of twin‐to‐twin transfusion syndrome. J Am Soc Echocardiogr; 23 (3): 301–8.
    1. Yagel S, Cohen SM, Shapiro I, Valsky DV. 3D and 4D ultrasound in fetal cardiac scanning: a new look at the fetal heart. Ultrasound Obstet Gynecol 2007; 29 (1): 81–95.
    1. Esh‐Broder E, Ushakov FB, Mbar T, Yagel S. Application of free‐hand three‐dimensional echocardiography in the evaluation of fetal cardiac ejection fraction: a preliminary study. Ultrasound Obstet Gynecol 2004; 24: 546–5551.
    1. Hamill N, Yeo L, Romero R, Hassan SS, Myers SA, Mittal P, et al. Fetal cardiac ventricular volume, cardiac output, and ejection fraction determined with 4‐dimensional ultrasound using spatiotemporal image correlation and virtual organ computer‐aided analysis. Am J Obstet Gynecol 2011; 205: 76. e1–e10.
    1. Messing B, Cohen SM, Valsky DV, Rosenak D, Hochner‐Celnikier D, Savchev S, et al. Fetal cardiac ventricle volumetry in the second half of gestation assessed by 4D ultrasound using STIC combined with inversion mode. Ultrasound Obstet Gynecol 2007; 30 (2): 142–51.
    1. Hamill N, Romero R, Hassan SS, Lee W, Myers SA, Mittal P, et al. Repeatability and reproducibility of fetal cardiac ventricular volume calculations using spatiotemporal image correlation and virtual organ computer‐aided analysis. J Ultrasound Med 2009; 28 (10): 1301–11.
    1. Hamill N, Romero R, Hassan SS, Lee W, Myers SA, Mittal P, et al. Repeatability and reproducibility of fetal cardiac ventricular volume calculations using spatiotemporal image correlation and virtual organ computer‐aided analysis. J Ultrasound Med 2009; 28 (10): 1301–11.
    1. Friedman KG, Margossian R, Graham DA, Harrild DM, Emani SM, Wilkins‐Haug LE, et al. Postnatal left ventricular diastolic function after fetal aortic valvuloplasty. Am J Cardiol; 108 (4): 556–60.
    1. Cruz‐Lemini M, Crispi F, Van Mieghem T, Pedraza D, Cruz‐Martinez R, Acosta‐Rojas R, et al. Risk of perinatal death in early‐onset intrauterine growth restriction according to gestational age and cardiovascular Doppler indices: a multicenter study. Fetal Diagn Ther 2012; 32 (1–2): 116–22.
    1. McElhinney DB, Vogel M, Benson CB, Marshall AC, Wilkins‐Haug LE, Silva V, et al. Assessment of left ventricular endocardial fibroelastosis in fetuses with aortic stenosis and evolving hypoplastic left heart syndrome. Am J Cardiol 2010; 106 (12): 1792–7.
    1. Pedra SR, Smallhorn JF, Ryan G, Chitayat D, Taylor GP, Khan R, et al. Fetal cardiomyopathies: pathogenic mechanisms, hemodynamic findings, and clinical outcome. Circulation 2002; 106 (5): 585–91.
    1. Wieczorek A, Hernandez‐Robles J, Ewing L, Leshko J, Luther S, Huhta J. Prediction of outcome of fetal congenital heart disease using a cardiovascular profile score. Ultrasound Obstet Gynecol 2008; 31 (3): 284–88.
    1. Pereira S, Ganapathy R, Syngelaki A, Maiz N, Nicolaides KH. Contribution of fetal tricuspid regurgitation in first‐trimester screening for major cardiac defects. Obstet Gynecol; 117 (6): 1384–91.
    1. Cruz‐Martinez R, Figueras F, Hernandez‐Andrade E, Oros D, Gratacos E. Changes in myocardial performance index and aortic isthmus and ductus venosus Doppler in term, small‐for‐gestational age fetuses with normal umbilical artery pulsatility index. Ultrasound Obstet Gynecol; 38 (4): 400–5.

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