Sonographic Assessment of Fetal Cardiac Function: Indirect Measurements of Fetal Cardiac Function, Newer Techniques and Clinical Applications

Zusammenfassung

Die nicht invasive Untersuchung fetaler Blutflussmuster mit Doppler-Ultraschall ist das Hauptwerkzeug zur Beurteilung des Kreislaufzustands bedrohter Feten. Sie erfolgt meist durch eine qualitative Untersuchung peripherer Arterien und, in bestimmten klinischen Situationen wie Wachstumsretardierung oder Volumenüberlastung, auch an herznahen Venen oder an Flussmustern im fetalen Herz, um das Stadium der fetalen Kreislauf-Kompensation zu bewerten. Eine echte quantitative Beurteilung der treibenden Kraft des fetalen Kreislaufs, also die direkte Beurteilung des fetalen Herzauswurfs, ist aber weiterhin ein angestrebtes wichtiges Ziel in der Fetalmedizin. Teil 1 dieser Übersicht beschreibt das Konzept der Untersuchung der fetalen Herzfunktion und des „cardiac output“. Teil 2 fasst die Nutzen der fetalen Doppler-Untersuchungen zusammen und gibt eine Übersicht über die anderen Methoden zur direkten und indirek24ten Messung der fetalen kardialen Funktion einschließlich neuerer klinischer Anwendungen.

Abstract

Noninvasive blood flow measurements based on Doppler ultrasound studies are the main clinical tool for studying the cardiovascular status of fetuses at risk for circulatory compromise. Usually, qualitative analysis of peripheral arteries and in particular clinical situations such as severe growth restriction or volume overload also of venous vessels close to the heart or of flow patterns in the heart is being used to gauge the level of compensation in a fetus. However, quantitative assessment of the driving force of the fetal circulation, the cardiac output remains an elusive goal in fetal medicine. This article reviews the methods for direct and indirect assessment of cardiac function and explains new clinical applications. Part 1 of this review describes the concept of cardiac function and cardiac output and the techniques that have been used to quantify output. Part 2 summarizes the use of arterial and venous Doppler studies in the fetus and gives a detailed description of indirect measurements of cardiac function (like indices derived from the duration of segments of the cardiac cycle) with current examples of their application.

Key words

heart - 3D ultrasound - 4D ultrasound - echocardiography - ultrasound

References

• 1 Baschat A A. Fetal growth restriction – from observation to intervention.  J Perinat Med. 2010;  38 239-246
• 2 Zhang J, Merialdi M, Platt L D et al. Defining normal and abnormal fetal growth: promises and challenges.  Am J Obstet Gynecol. 2010;  202 522-528
• 3 Hoffman C, Galan H L. Assessing the ‘at-risk’ fetus: Doppler ultrasound.  Curr Opin Obstet Gynecol. 2009;  21 161-166
• 4 Haws R A, Yakoob M Y, Soomro T et al. Reducing stillbirths: screening and monitoring during pregnancy and labour.  BMC Pregnancy Childbirth. 2009;  9 S5
• 5 Manning F A. Antepartum fetal testing: a critical appraisal.  Curr Opin Obstet Gynecol. 2009;  21 348-352
• 6 Miller J, Turan S, Baschat A A. Fetal growth restriction.  Semin Perinatol. 2008;  32 274-280
• 7 Turan S, Miller J, Baschat A A. Integrated testing and management in fetal growth restriction.  Semin Perinatol. 2008;  32 194-200
• 8 Sebire N J, Sepulveda W. Correlation of placental pathology with prenatal ultrasound findings.  J Clin Pathol. 2008;  61 1276-1284
• 9 Mari G, Hanif F. Fetal Doppler: umbilical artery, middle cerebral artery, and venous system.  Semin Perinatol. 2008;  32 253-257
• 10 Mari G, Hanif F, Kruger M. Sequence of cardiovascular changes in IUGR in pregnancies with and without preeclampsia.  Prenat Diagn. 2008;  28 377-383
• 11 Picconi J L, Hanif F, Drennan K et al. The transitional phase of ductus venosus reversed flow in severely premature IUGR fetuses.  Am J Perinatol. 2008;  25 199-203
• 12 Soothill P W, Bobrow C S, Holmes R. Small for gestational age is not a diagnosis.  Ultrasound Obstet Gynecol. 1999;  13 225-228
• 13 Alfirevic Z, Neilson J P. Doppler ultrasonography in high-risk pregnancies: systematic review with meta-analysis.  Am J Obstet Gynecol. 1995;  172 1379-1387
• 14 Kingdom J C, Burrell S J, Kaufmann P. Pathology and clinical implications of abnormal umbilical artery Doppler waveforms.  Ultrasound Obstet Gynecol. 1997;  9 271-286
• 15 Sebire N J. Umbilical artery Doppler revisited: pathophysiology of changes in intrauterine growth restriction revealed.  Ultrasound Obstet Gynecol. 2003;  21 419-422
• 16 Baschat A A, Gembruch U, Harman C R. The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens.  Ultrasound Obstet Gynecol. 2001;  18 571-577
• 17 Bilardo C M, Muller M A, Zikulnig L et al. Ductus venosus studies in fetuses at high risk for chromosomal or heart abnormalities: relationship with nuchal translucency measurement and fetal outcome.  Ultrasound Obstet Gynecol. 2001;  17 288-294
• 18 Cosmi E, Ambrosini G, D’Antona D et al. Doppler, cardiotocography, and biophysical profile changes in growth-restricted fetuses.  Obstet Gynecol. 2005;  106 1240-1245
• 19 Ferrazzi E, Bozzo M, Rigano S et al. Temporal sequence of abnormal Doppler changes in the peripheral and central circulatory systems of the severely growth-restricted fetus.  Ultrasound Obstet Gynecol. 2002;  19 140-146
• 20 Rizzo G, Arduini D. Fetal cardiac function in intrauterine growth retardation.  Am J Obstet Gynecol. 1991;  165 876-882
• 21 Harman C R, Baschat A A. Comprehensive assessment of fetal wellbeing: which Doppler tests should be performed?.  Curr Opin Obstet Gynecol. 2003;  15 147-157
• 22 Harman C R, Baschat A A. Arterial and venous Dopplers in IUGR.  Clin Obstet Gynecol. 2003;  46 931-946
• 23 Kiserud T, Eik-Nes S H, Blaas H G et al. Ultrasonographic velocimetry of the fetal ductus venosus.  Lancet. 1991;  338 1412-1414
• 24 Kiserud T. In a different vein: the ductus venosus could yield much valuable information.  Ultrasound Obstet Gynecol. 1997;  9 369-372
• 25 Kiserud T. The ductus venosus.  Semin Perinatol. 2001;  25 11-20
• 26 Kiserud T, Acharya G. The fetal circulation.  Prenat Diagn. 2004;  24 1049-1059
• 27 Kiserud T, Ebbing C, Kessler J et al. Fetal cardiac output, distribution to the placenta and impact of placental compromise.  Ultrasound Obstet Gynecol. 2006;  28 126-136
• 28 Hecher K, Campbell S, Doyle P et al. Assessment of fetal compromise by Doppler ultrasound investigation of the fetal circulation. Arterial, intracardiac, and venous blood flow velocity studies.  Circulation. 1995;  91 129-138
• 29 Hecher K, Snijders R, Campbell S et al. Fetal venous, intracardiac, and arterial blood flow measurements in intrauterine growth retardation: relationship with fetal blood gases.  Am J Obstet Gynecol. 1995;  173 10-15
• 30 Hecher K, Bilardo C M, Stigter R H et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study.  Ultrasound Obstet Gynecol. 2001;  18 564-570
• 31 Lees C, Baumgartner H. The TRUFFLE study – a collaborative publicly funded project from concept to reality: how to negotiate an ethical, administrative and funding obstacle course in the European Union.  Ultrasound Obstet Gynecol. 2005;  25 105-107
• 32 Huhta J C. Guidelines for the evaluation of heart failure in the fetus with or without hydrops.  Pediatr Cardiol. 2004;  25 274-286
• 33 Respondek M L, Kammermeier M, Ludomirsky A et al. The prevalence and clinical significance of fetal tricuspid valve regurgitation with normal heart anatomy.  Am J Obstet Gynecol. 1994;  171 1265-1270
• 34 Tulzer G, Khowsathit P, Gudmundsson S et al. Diastolic function of the fetal heart during second and third trimester: a prospective longitudinal Doppler-echocardiographic study.  Eur J Pediatr. 1994;  153 151-154
• 35 Rychik J, Tian Z, Bebbington M 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;  197 392, e391-e398
• 36 Harada K, Tsuda A, Orino T et al. Tissue Doppler imaging in the normal fetus.  Int J Cardiol. 1999;  71 227-234
• 37 Paladini D, Lamberti A, Teodoro A et al. Tissue Doppler imaging of the fetal heart.  Ultrasound Obstet Gynecol. 2000;  16 530-535
• 38 Tutschek B, Zimmermann T, Buck T et al. Fetal tissue Doppler echocardiography: detection rates of cardiac structures and quantitative assessment of the fetal heart.  Ultrasound Obstet Gynecol. 2003;  21 26-32
• 39 Dalen H, Thorstensen A, Aase S A et al. Segmental and global longitudinal strain and strain rate based on echocardiography of 1266 healthy individuals: the HUNT study in Norway.  Eur J Echocardiogr. 2010;  11 176-183
• 40 Larsen L U, Petersen O B, Norrild K et al. Strain rate derived from color Doppler myocardial imaging for assessment of fetal cardiac function.  Ultrasound Obstet Gynecol. 2006;  27 210-213
• 41 Larsen L U, Sloth E, Petersen O B et al. Systolic myocardial velocity alterations in the growth-restricted fetus with cerebroplacental redistribution.  Ultrasound Obstet Gynecol. 2009;  34 62-67
• 42 Di Salvo G, Russo M G, Paladini D et al. Two-dimensional strain to assess regional left and right ventricular longitudinal function in 100 normal foetuses.  Eur J Echocardiogr. 2008;  9 754-756
• 43 Ta-Shma A, Perles Z, Gavri S et al. Analysis of segmental and global function of the fetal heart using novel automatic functional imaging.  J Am Soc Echocardiogr. 2008;  21 146-150
• 44 Younoszai A K, Saudek D E, Emery S P et al. Evaluation of myocardial mechanics in the fetus by velocity vector imaging.  J Am Soc Echocardiogr. 2008;  21 470-474
• 45 Barker P C, Houle H, Li J S et al. Global longitudinal cardiac strain and strain rate for assessment of fetal cardiac function: novel experience with velocity vector imaging.  Echocardiography. 2009;  26 28-36
• 46 Peng Q H, Zhou Q C, Zeng S et al. Evaluation of regional left ventricular longitudinal function in 151 normal fetuses using velocity vector imaging.  Prenat Diagn. 2009;  29 1149-1155
• 47 Mori Y, Rice M J, McDonald R W et al. Evaluation of systolic and diastolic ventricular performance of the right ventricle in fetuses with ductal constriction using the Doppler Tei index.  Am J Cardiol. 2001;  88 1173-1178
• 48 Tei C, Ling L H, Hodge D O et al. New index of combined systolic and diastolic myocardial performance: a simple and reproducible measure of cardiac function – a study in normals and dilated cardiomyopathy.  J Cardiol. 1995;  26 357-366
• 49 Tsutsumi T, Ishii M, Eto G et al. Serial evaluation for myocardial performance in fetuses and neonates using a new Doppler index.  Pediatr Int. 1999;  41 722-727
• 50 Hernandez-Andrade E, Lopez-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;  26 227-232
• 51 Harada K, Tamura M, Toyono M et al. Comparison of the right ventricular Tei index by tissue Doppler imaging to that obtained by pulsed Doppler in children without heart disease.  Am J Cardiol. 2002;  90 566-569
• 52 Duan Y, Harada K, Wu W et al. Correlation between right ventricular Tei index by tissue Doppler imaging and pulsed Doppler imaging in fetuses.  Pediatr Cardiol. 2008;  29 739-743
• 53 Figueras F, Puerto B, Martinez J M et al. Cardiac function monitoring of fetuses with growth restriction.  Eur J Obstet Gynecol Reprod Biol. 2003;  110 159-163
• 54 Bahtiyar M O, Copel J A. Cardiac changes in the intrauterine growth-restricted fetus.  Semin Perinatol. 2008;  32 190-193
• 55 Crispi F, Hernandez-Andrade E, Pelsers M M et al. Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses.  Am J Obstet Gynecol. 2008;  199 254, e251-e258
• 56 Hernandez-Andrade E, Crispi F, Benavides-Serralde J A et al. Contribution of the myocardial performance index and aortic isthmus blood flow index to predicting mortality in preterm growth-restricted fetuses.  Ultrasound Obstet Gynecol. 2009;  34 430-436
• 57 Habli M, Lim F Y, Crombleholme T. Twin-to-twin transfusion syndrome: a comprehensive update.  Clin Perinatol. 2009;  36 391-416, x
• 58 Senat M V, Deprest J, Boulvain M et al. Endoscopic laser surgery versus serial amnioreduction for severe twin-to-twin transfusion syndrome.  N Engl J Med. 2004;  351 136-144
• 59 Van Hare G F, Hawkins J A, Schmidt K G et al. The effects of increasing mean arterial pressure on left ventricular output in newborn lambs.  Circ Res. 1990;  67 78-83
• 60 Barrea C, Alkazaleh F, Ryan G et al. Prenatal cardiovascular manifestations in the twin-to-twin transfusion syndrome recipients and the impact of therapeutic amnioreduction.  Am J Obstet Gynecol. 2005;  192 892-902
• 61 Herberg U, Gross W, Bartmann P et al. Long term cardiac follow up of severe twin to twin transfusion syndrome after intrauterine laser coagulation.  Heart. 2006;  92 95-100
• 62 Quintero R A, Morales W J, Allen M H et al. Staging of twin-twin transfusion syndrome.  J Perinatol. 1999;  19 550-555
• 63 Van Mieghem T, Klaritsch P, Done E et al. Assessment of fetal cardiac function before and after therapy for twin-to-twin transfusion syndrome.  Am J Obstet Gynecol. 2009;  200 400, e401-e407
• 64 Jani J C, Nicolaides K H, Gratacos E et al. Severe diaphragmatic hernia treated by fetal endoscopic tracheal occlusion.  Ultrasound Obstet Gynecol. 2009;  34 304-310
• 65 Van Mieghem T, Gucciardo L, Done 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;  34 424-429
• 66 Schmidt K G, Silverman N H, Harison M R et al. High-output cardiac failure in fetuses with large sacrococcygeal teratoma: diagnosis by echocardiography and Doppler ultrasound.  J Pediatr. 1989;  114 1023-1028
• 67 Sepulveda W, Platt C C, Fisk N M. Prenatal diagnosis of cerebral arteriovenous malformation using color Doppler ultrasonography: case report and review of the literature.  Ultrasound Obstet Gynecol. 1995;  6 282-286
• 68 Langer J C, Harrison M R, Schmidt K G et al. Fetal hydrops and death from sacrococcygeal teratoma: rationale for fetal surgery.  Am J Obstet Gynecol. 1989;  160 1145-1150
• 69 Corrigan N, Brazil D P, McAuliffe F. Fetal cardiac effects of maternal hyperglycemia during pregnancy.  Birth Defects Res A Clin Mol Teratol. 2009;  85 523-530
• 70 Stuart A, Amer-Wahlin I, Gudmundsson S et al. Ductus venosus blood flow velocity waveform in diabetic pregnancies.  Ultrasound Obstet Gynecol. 2010;  36 344-349
• 71 Zielinsky P, Marcantonio S, Nicoloso L H et al. Ductus venosus flow and myocardial hypertrophy in fetuses of diabetic mothers.  Arq Bras Cardiol. 2004;  83 51-56, 45 – 50
• 72 Zielinsky P, Nicoloso L H, Firpo C et al. Alternative parameters for echocardiographic assessment of fetal diastolic function.  Braz J Med Biol Res. 2004;  37 31-36