Advertisement

Size and shape of the four-chamber view of the fetal heart in fetuses with an estimated fetal weight less than the tenth centile

      Background

      Fetuses with an estimated fetal weight below the 10th centile have an increased risk of adverse perinatal and long-term outcomes as well as increased rates of cardiac dysfunction, which often alters cardiac size and shape of the 4-chamber view and the individual ventricles. As a result, a simple method has emerged to screen for potential cardiac dysfunction in fetuses with estimated fetal weights <10th centile by measuring the size and shape of the 4-chamber view and the size of the ventricles.

      Objective

      To determine the number of fetuses with an abnormal size and shape of the 4-chamber view and size of the ventricles in fetuses with an estimated fetal weight <10th centile.

      Materials and Methods

      This was a retrospective study of 50 fetuses between 25 and 37 weeks of gestation with an estimated fetal weight <10th centile. Data from their last examination were analyzed. From an end-diastolic image of the 4-chamber view, the largest basal–apical length and transverse width were measured from their corresponding epicardial borders. This allowed the 4-chamber view area and global sphericity index (4-chamber view length/4-chamber view width) to be computed. In addition, tracing along the endocardial borders with speckle tracking software enabled measurements of the right and left ventricular chamber areas and the right ventricle/left ventricle area ratios to be computed. Doppler waveform pulsatility indices from the umbilical (umbilical artery pulsatility index) and middle cerebral arteries (middle cerebral artery pulsatility index) were analyzed, and the cerebroplacental ratio (middle cerebral artery pulsatility index/umbilical artery pulsatility index) computed. Umbilical artery pulsatility indices >90th and cerebroplacental ratios <10th centile were considered abnormal. Using data from the control fetuses, the centile for each of the cardiac measurements was categorized by whether it was <10th or >90th centile, depending upon the measurement.

      Results

      Of the 50 fetuses with estimated fetal weight <10th centile, 50% (n = 25) had a normal umbilical artery pulsatility index and cerebroplacental ratio. These fetuses had significantly more (P < 0.02 to <0.0001) abnormalities of the size and shape of the 4-chamber view than controls. In all, 44% had a 4-chamber view area >90th centile, 32% had a 4-chamber view global sphericity index <10th centile, 56% had a 4-chamber view width >90th centile, and 80% had 1 or more abnormalities of size and/or shape. The remaining 50% of fetuses (n = 25) had abnormalities of 1 or both for the umbilical artery pulsatility index and/or cerebroplacental ratio. These fetuses had significantly higher rates of abnormalities (P <0.05 to <0.0001) than controls for the following 4-chamber view measurements: 36% had a 4-chamber view area >90th centile; 28% had a 4-chamber view global sphericity index <10th centile; and 68% had a 4-chamber view width >90th centile. Only those fetuses with an abnormal umbilical artery pulsatility index had significant changes in ventricular size; 56% had a left ventricular area <10th centile; 28% had a right ventricular area <10th centile; 36% had right ventricular/left ventricular area ratio >90th centile. One or more of the above abnormal measurements were present in 92% of the fetuses.

      Conclusion

      Higher rates of abnormalities of cardiac size and shape of the 4-chamber view were found in fetuses with an estimated fetal weight <10th centile, regardless of their umbilical artery pulsatility index and cerebroplacental ratio measurements. Those with a normal umbilical artery pulsatility index and an abnormal cerebroplacental ratio had larger and wider measurements of the 4-chamber view. In addition, the shape of the 4-chamber view was more globular or round than in controls. These fetuses may have an increased risk of perinatal complications and childhood and/or adult cardiovascular disease. Screening tools derived from the 4-chamber view, acting as surrogates for ventricular dysfunction, may identify fetuses who could benefit from further comprehensive testing and future preventive interventions.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Obstetrics & Gynecology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Cnattingius S.
        • Haglund B.
        • Kramer M.S.
        Differences in late fetal death rates in association with determinants of small for gestational age fetuses: population based cohort study.
        BMJ (Clinical research ed). 1998; 316: 1483-1487
        • Khalil A.A.
        • Morales-Rosello J.
        • Elsadigg M.
        • et al.
        The association between fetal Doppler and admission to neonatal unit at term.
        Am J Obstet Gynecol. 2015; 213: 57
        • Eixarch E.
        • Meler E.
        • Iraola A.
        • et al.
        Neurodevelopmental outcome in 2-year-old infants who were small-for-gestational age term fetuses with cerebral blood flow redistribution.
        Ultrasound Obst Gynecol. 2008; 32: 894-899
        • Cruz-Lemini M.
        • Crispi F.
        • Valenzuela-Alcaraz B.
        • et al.
        Fetal cardiovascular remodelling persists at 6 months of life in infants with intrauterine growth restriction.
        Ultrasound Obstet. 2016; 48: 349-356
        • Barker D.J.
        • Winter P.D.
        • Osmond C.
        • Margetts B.
        • Simmonds S.J.
        Weight in infancy and death from ischaemic heart disease.
        Lancet. 1989; 2: 577-580
        • Crispi F.
        • Miranda J.
        • Gratacos E.
        Long-term cardiovascular consequences of fetal growth restriction: biology, clinical implications, and opportunities for prevention of adult disease.
        Am J Obstet Gynecol. 2018; 218: S869-S879
        • Madden J.V.
        • Flatley C.J.
        • Kumar S.
        Term small-for-gestational-age infants from low-risk women are at significantly greater risk of adverse neonatal outcomes.
        Am J Obstet Gynecol. 2018; 218: 525
        • McEwen E.C.
        • Guthridge S.L.
        • He V.Y.F.
        • McKenzie J.W.
        • Boulton T.J.
        • Smith R.
        What birthweight percentile is associated with optimal perinatal mortality and childhood education outcomes?.
        Am J Obstet Gynecol. 2018; 218: S712-S724
        • Malhotra A.
        • Allison B.J.
        • Castillo-Melendez M.
        • Jenkin G.
        • Polglase G.R.
        • Miller S.L.
        Neonatal morbidities of fetal growth restriction: pathophysiology and impact.
        Front Endocrinol. 2019; 10: 55
        • Gordijn S.J.
        • Beune I.M.
        • Thilaganathan B.
        • et al.
        Consensus definition of fetal growth restriction: a Delphi procedure.
        Ultrasound Obstet Gynecol. 2016; 48: 333-339
        • DeVore G.R.
        The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses.
        Am J Obstet Gynecol. 2015; 213: 5-15
        • Hiersch L.
        • Melamed N.
        Fetal growth velocity and body proportion in the assessment of growth.
        Am J Obstet Gynecol. 2018; 218: S700-S711
        • Figueras F.
        • Caradeux J.
        • Crispi F.
        • Eixarch E.
        • Peguero A.
        • Gratacos E.
        Diagnosis and surveillance of late-onset fetal growth restriction.
        Am J Obstet Gynecol. 2018; 218: S790-S802
        • Villar J.
        • Papageorghiou A.T.
        • Pang R.
        • et al.
        The likeness of fetal growth and newborn size across non-isolated populations in the INTERGROWTH-21st Project: the Fetal Growth Longitudinal Study and Newborn Cross-Sectional Study.
        Lancet Diabetes Endocrinol. 2014; 2: 781-792
        • Grantz K.L.
        • Hediger M.L.
        • Liu D.
        • Buck Louis G.M.
        Fetal growth standards: the NICHD fetal growth study approach in context with INTERGROWTH-21st and the World Health Organization Multicentre Growth Reference Study.
        Am J Obstet Gynecol. 2018; 218: S641-S655
        • Clausson B.
        • Gardosi J.
        • Francis A.
        • Cnattingius S.
        Perinatal outcome in SGA births defined by customised versus population-based birthweight standards.
        Br J Obstet Gynecol. 2001; 108: 830-834
        • O'Dwyer V.
        • Burke G.
        • Unterscheider J.
        • et al.
        Defining the residual risk of adverse perinatal outcome in growth-restricted fetuses with normal umbilical artery blood flow.
        Am J Obstet Gynecol. 2014; 211: 420
        • McCowan L.M.
        • Figueras F.
        • Anderson N.H.
        Evidence-based national guidelines for the management of suspected fetal growth restriction: comparison, consensus, and controversy.
        Ame J Obstet Gynecol. 2018; 218: S855-S868
        • Figueras F.
        • Caradeux J.
        • Crispi F.
        • Eixarch E.
        • Peguero A.
        • Gratacos E.
        Diagnosis and surveillance of late-onset fetal growth restriction.
        Am J Obstet Gynecol. 2018; 218: S790-S802
        • Crispi F.
        • Figueras F.
        • Cruz-Lemini M.
        • Bartrons J.
        • Bijnens B.
        • Gratacos E.
        Cardiovascular programming in children born small for gestational age and relationship with prenatal signs of severity.
        Am J Obstet Gynecol. 2012; 207: 121
        • Ananth C.V.
        • Vintzileos A.M.
        Distinguishing pathological from constitutional small for gestational age births in population-based studies.
        Early Hum Dev. 2009; 85: 653-658
        • Cohen E.
        • Whatley C.
        • Wong F.Y.
        • et al.
        Effects of foetal growth restriction and preterm birth on cardiac morphology and function during infancy.
        Acta Paediatr. 2018; 107: 450-455
        • Crispi F.
        • Bijnens B.
        • Figueras F.
        • et al.
        Fetal growth restriction results in remodeled and less efficient hearts in children.
        Circulation. 2010; 121: 2427-2436
        • Agata Y.
        • Hiraishi S.
        • Oguchi K.
        • et al.
        Changes in left ventricular output from fetal to early neonatal life.
        J Pediatr. 1991; 119: 441-445
        • Patey O.
        • Carvalho J.S.
        • Thilaganathan B.
        Perinatal changes in cardiac geometry and function in growth restricted fetuses at term.
        Ultrasound Obstet Gynecol. 2019; 53: 655-662
        • Veille J.C.
        • Hanson R.
        • Sivakoff M.
        • Hoen H.
        • Ben-Ami M.
        Fetal cardiac size in normal, intrauterine growth retarded, and diabetic pregnancies.
        Am J Perinatol. 1993; 10: 275-279
        • DeVore G.R.
        Examination of the fetal heart in the fetus with intrauterine growth retardation using M-mode echocardiography.
        Semin Perinatol. 1988; 12: 66-79
        • Rodriguez-Lopez M.
        • Cruz-Lemini M.
        • Valenzuela-Alcaraz B.
        • et al.
        Descriptive analysis of the different phenotypes of cardiac remodeling in fetal growth restriction.
        Ultrasound Obstet Gynecol. 2017; 50: 207-214
        • Devore G.R.
        Advanced assessment of fetal cardiac function.
        in: Kline-Fath B BD Bahado-Sing R. Fundamental and advanced fetal imaging—ultrasound and MRI. 1st ed. Wolters Kluwer, Philadelphia, PA2015: 114-164
        • DeVore G.R.
        • 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: 2309-2318
        • DeVore G.R.
        • Satou G.
        • Sklansky M.
        Area of the fetal heart's four-chamber view: a practical screening tool to improve detection of cardiac abnormalities in a low-risk population.
        Prenatal diagnosis. 2017; 37: 151-155
        • Hadlock F.P.
        • Deter R.L.
        • Harrist R.B.
        • Park S.K.
        Estimating fetal age: computer-assisted analysis of multiple fetal growth parameters.
        Radiology. 1984; 152: 497-501
        • Hadlock F.P.
        • Harrist R.B.
        • Sharman R.S.
        • Deter R.L.
        • Park S.K.
        Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study.
        Am J Obstet Gynecol. 1985; 151: 333-337
        • DeVore G.R.
        • Klas B.
        • Satou G.
        • Sklansky M.
        Evaluation of fetal left ventricular size and function using speckle-tracking and the Simpson rule.
        J Ultrasound Med. 2019; 38: 1209-1221
        • DeVore G.R.
        • Polanco B.
        • Satou G.
        • Sklansky M.
        Two-dimensional speckle tracking of the fetal heart: a practical step-by-step approach for the fetal sonologist.
        J Ultrasound Med. 2016; 35: 1765-1781
        • Ebbing C.
        • Rasmussen S.
        • Kiserud T.
        Middle cerebral artery blood flow velocities and pulsatility index and the cerebroplacental pulsatility ratio: longitudinal reference ranges and terms for serial measurements.
        Ultrasound Obstet Gynecol. 2007; 30: 287-296
        • DeVore G.R.
        • Klas B.
        • Satou G.
        • Sklansky M.
        Evaluation of the right and left ventricles: an integrated approach measuring the area, length, and width of the chambers in normal fetuses.
        Prenatal Diagnosis. 2017; 37: 1203-1212
        • DeVore G.R.
        • Gumina D.
        • Hobbins J.C.
        Assessment of ventricular contractility in fetuses with an estimated fetal weight less than the tenth centile.
        Am J Obstet Gynecol. 2019; 221: 498.e1-498.e22
        • Girsen A.
        • Ala-Kopsala M.
        • Makikallio K.
        • Vuolteenaho O.
        • Rasanen J.
        Cardiovascular hemodynamics and umbilical artery N-terminal peptide of proB-type natriuretic peptide in human fetuses with growth restriction.
        Ultrasound Obstet Gynecol. 2007; 29: 296-303
        • 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
        • Parra-Saavedra M.
        • Simeone S.
        • Triunfo S.
        • et al.
        Correlation between histological signs of placental underperfusion and perinatal morbidity in late-onset small-for-gestational-age fetuses.
        Ultrasound Obstet Gynecol. 2015; 45: 149-155
        • Mari G.
        Arterial blood flow velocity waveforms of the pelvis and lower extremities in normal and growth-retarded fetuses.
        Am J Obstet Gynecol. 1991; 165: 143-151
        • Yamamoto Y.
        • Hirose A.
        • Howley L.
        • Savard W.
        • Jain V.
        • Hornberger L.K.
        Parameters of fetal pulmonary vascular health: baseline trends and response to maternal hyperoxia in the second and third trimesters.
        Ultrasound Obstet Gynecol. 2017; 50: 618-623
        • Cruz-Martinez R.
        • Figueras F.
        • Oros D.
        • et al.
        Cerebral blood perfusion and neurobehavioral performance in full-term small-for-gestational-age fetuses.
        Am J Obstet Gynecol. 2009; 201: 474
        • Mayhew T.M.
        • Wijesekara J.
        • Baker P.N.
        • Ong S.S.
        Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia.
        Placenta. 2004; 25: 829-833
        • Burton G.J.
        • Jauniaux E.
        Pathophysiology of placental-derived fetal growth restriction.
        Am J Obstet Gynecol. 2018; 218: S745
        • Sultana Z.
        • Maiti K.
        • Dedman L.
        • Smith R.
        Is there a role for placental senescence in the genesis of obstetric complications and fetal growth restriction?.
        Am J Obstet Gynecol. 2018; 218: S762-S773
        • ACOG
        ACOG practice bulletin no. 134: fetal growth restriction.
        Obstet Gynecol. 2013; 121: 1122-1133
        • 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
        • 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
        • Barker D.J.
        • Osmond C.
        • Golding J.
        • Kuh D.
        • Wadsworth M.E.
        Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease.
        BMJ (Clin Res Ed). 1989; 298: 564-567
        • Arnott C.
        • Skilton M.R.
        • Ruohonen S.
        • et al.
        Subtle increases in heart size persist into adulthood in growth restricted babies: the Cardiovascular Risk in Young Finns Study.
        Open Heart. 2015; 2: e000265
        • Sanz-Cortes M.
        • Egana-Ugrinovic G.
        • Simoes R.V.
        • Vazquez L.
        • Bargallo N.
        • Gratacos E.
        Association of brain metabolism with sulcation and corpus callosum development assessed by MRI in late-onset small fetuses.
        Am J Obstet Gynecol. 2015; 212: 804
        • Lindstrom L.
        • Wikstrom A.K.
        • Bergman E.
        • Lundgren M.
        Born small for gestational age and poor school performance—how small is too small?.
        Horm Res Paediatr. 2017; 88: 215-223
        • Darendeliler F.
        IUGR: genetic influences, metabolic problems, environmental associations/triggers, current and future management.
        Best Practice Res Clin Endocrinol Metabolism. 2019 Jan 22; ([Epub ahead of print]): 101260https://doi.org/10.1016/j.beem.2019.01.001
        • Henry A.
        • Alphonse J.
        • Tynan D.
        • Welsh A.W.
        Fetal myocardial performance index in assessment and management of small-for-gestational-age fetus: a cohort and nested case-control study.
        Ultrasound Obstet Gynecol. 2018; 51: 225-235
        • Messing B.
        • Gilboa Y.
        • Lipschuetz M.
        • Valsky D.V.
        • Cohen S.M.
        • Yagel S.
        Fetal tricuspid annular plane systolic excursion (f-TAPSE): evaluation of fetal right heart systolic function with conventional M-mode ultrasound and spatiotemporal image correlation (STIC) M-mode.
        Ultrasound Obstet Gynecology. 2013; 42: 182-188
        • DeVore G.R.
        • Klas B.
        • Satou G.
        • Sklansky M.
        Speckle tracking of the basal lateral and septal wall annular plane systolic excursion of the right and left ventricles of the fetal heart.
        Journal Ultrasound. 2019; 38: 1309-1318
        • DeVore G.R.
        • Klas B.
        • Satou G.
        • Sklansky M.
        Longitudinal annular systolic displacement compared to global strain in normal fetal hearts and those with cardiac abnormalities.
        J Ultrasound Med. 2018; 37: 1159-1171
        • DeVore G.R.
        • 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: 1129-1141
        • Corstius H.B.
        • Zimanyi M.A.
        • Maka N.
        • et al.
        Effect of intrauterine growth restriction on the number of cardiomyocytes in rat hearts.
        Pediatr Res. 2005; 57: 796-800
        • Schipke J.
        • Gonzalez-Tendero A.
        • Cornejo L.
        • et al.
        Experimentally induced intrauterine growth restriction in rabbits leads to differential remodelling of left versus right ventricular myocardial microstructure.
        Histochem Cell Biol. 2017; 148: 557-567
        • Sehgal A.
        • Doctor T.
        • Menahem S.
        Cardiac function and arterial biophysical properties in small for gestational age infants: postnatal manifestations of fetal programming.
        J Pediatr. 2013; 163: 1296-1300
        • Zanardo V.
        • Fanelli T.
        • Weiner G.
        • et al.
        Intrauterine growth restriction is associated with persistent aortic wall thickening and glomerular proteinuria during infancy.
        Kidney Int. 2011; 80: 119-123
        • Rodriguez-Lopez M.
        • Osorio L.
        • Acosta-Rojas R.
        • et al.
        Influence of breastfeeding and postnatal nutrition on cardiovascular remodeling induced by fetal growth restriction.
        Pediatr Res. 2016; 79: 100-106
        • Skilton M.R.
        • Raitakari O.T.
        • Celermajer D.S.
        High intake of dietary long-chain omega-3 fatty acids is associated with lower blood pressure in children born with low birth weight: NHANES 2003-2008.
        Hypertension. 2013; 61: 972-976
        • Cruz-Lemini M.
        • Crispi F.
        • Valenzuela-Alcaraz B.
        • et al.
        A fetal cardiovascular score to predict infant hypertension and arterial remodeling in intrauterine growth restriction.
        Am J Obstet Gynecol. 2014; 210: 552
        • Jiang H.L.
        • Cao L.Q.
        • Chen H.Y.
        Blood folic acid, vitamin B12, and homocysteine levels in pregnant women with fetal growth restriction.
        Genet Mol Res. 2016; 15
        • Skilton M.R.
        • Pahkala K.
        • Viikari J.S.
        • et al.
        The association of dietary alpha-linolenic acid with blood pressure and subclinical atherosclerosis in people born small for gestational age: the Special Turku Coronary Risk Factor Intervention Project study.
        J Pediatr. 2015; 166: 1252-1257
        • DeVore G.R.
        • Cuneo B.F.
        • Satou G.
        • Sklansky M.
        How to determine the percent of study subjects below the 5th or above the 95th centiles of the control group when only the mean and standard deviations are provided.
        Ultrasound Obstet Gynecol. 2019; 54: 139-141