Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Journal of Perinatal Medicine

Official Journal of the World Association of Perinatal Medicine

Editor-in-Chief: Dudenhausen, MD, FRCOG, Joachim W.

Ed. by Bancalari, Eduardo / Chappelle, Joseph / Chervenak, Frank A. / D'Addario , Vincenzo / Genc, Mehmet R. / Greenough, Anne / Grunebaum, Amos / Konje, Justin C. / Kurjak M.D., Asim / Romero, Roberto / Zalud, MD PhD, Ivica

IMPACT FACTOR 2018: 1.361
5-year IMPACT FACTOR: 1.578

CiteScore 2018: 1.29

SCImago Journal Rank (SJR) 2018: 0.522
Source Normalized Impact per Paper (SNIP) 2018: 0.602

See all formats and pricing
More options …
Volume 47, Issue 8


Comparison of fetal cardiac functions between small-for-gestational age fetuses and late-onset growth-restricted fetuses

Başak Kaya / Ahmet Tayyar / Deniz Kanber Açar
  • Department of Maternal-Fetal Medicine, Health Sciences University, Bakırköy Dr. Sadi Konuk Education and Research Hospital, İstanbul, Turkey
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Serdar Kaya
Published Online: 2019-08-06 | DOI: https://doi.org/10.1515/jpm-2019-0206



This study aimed to investigate fetal cardiac functions by spectral tissue Doppler imaging (s-TDI) in pregnancies complicated with late-onset fetal growth restriction (LO-FGR) and small-for-gestational age (SGA).


Forty pregnancies complicated with late-onset FGR and 40 pregnancies complicated with SGA between the 34th and 37th weeks of gestation were enrolled in this study. Forty gestational age-matched pregnant women with no obstetrics complication were randomly selected as a control group. Small fetuses were classified as fetal growth restriction or SGA according to estimated fetal weight (EFW), umbilical artery pulsatility index (PI), cerebroplacental ratio (CPR) and uterine artery PI. s-TDI measurements were obtained at the right atrioventricular valve annulus.


SGA and LO-FGR fetuses had significantly lower A′ and S′ values, and higher E′/A′ ratio than the control group (P < 0.001). In comparison to controls, significantly prolonged isovolumetric contraction time (ICT′) and isovolumetric relaxation time (IRT′) and, significantly shortened ejection time (ET′) were observed in fetuses with SGA and LO-FGR. Increased myocardial performance index (MPI′) values were also found in fetuses with SGA and LO-FGR compared to controls.


The signs of cardiac dysfunction were observed both in fetuses with SGA and LO-FGR. The fetal cardiac function assessment with s-TDI could be a valuable method in the diagnosis of true growth restricted fetuses and in the management of these fetuses.

Keywords: fetal cardiac function; late-onset fetal growth restriction; small-for-gestational age; spectral tissue Doppler imaging


  • 1.

    Mendez-Figueroa H, Truong VT, Pedroza C, Khan AM, Chauhan SP. Small-for-gestational-age infants among uncomplicated pregnancies at term: a secondary analysis of 9 Maternal-Fetal Medicine Units Network studies. Am J Obstet Gynecol 2016;215:628.e1–7.Google Scholar

  • 2.

    Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, et al. Child health, developmental plasticity, and epigenetic programming. Endocr Rev 2011;32:159–224.Google Scholar

  • 3.

    Figueras F, Gratacos E. Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther 2014;36:86–98.Google Scholar

  • 4.

    Oros D, Figueras F, Cruz-Martinez R, Meler E, Munmany M, Gratacos E. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol 2011;37:191–5.Google Scholar

  • 5.

    Soothill PW, Bobrow CS, Holmes R. Small for gestational age is not a diagnosis. Ultrasound Obstet Gynecol 1999;13: 225–8.Google Scholar

  • 6.

    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;199:254.e1–8.Google Scholar

  • 7.

    Comas M, Crispi F. Assessment of fetal cardiac function using tissue Doppler techniques. Fetal Diagn Ther 2012;31:30–8.Google Scholar

  • 8.

    Watanabe S, Hashimoto I, Saito K, Watanabe K, Hirono K, Uese K, et al. Characterization of ventricular myocardial performance in fetus by tissue Doppler imaging. Circ J 2009;73:943–7.Google Scholar

  • 9.

    Harada K, Tsuda A, Orino T, Tanaka T, Takada G. Tissue Doppler imaging in the normal fetus. Int J Cardiol 1999;71: 227–34.Google Scholar

  • 10.

    Chan LY, Fok WY, Wong JT, Yu CM, Leung TN, Lau TK. Reference charts of gestation-specific tissue Doppler imaging indices of systolic and diastolic functions in the normal fetal heart. Am Heart J 2005;150:750–5.Google Scholar

  • 11.

    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;113:39–47.Google Scholar

  • 12.

    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’ of gestation. Ultrasound Obstet Gynecol 2011;37:57–64.Google Scholar

  • 13.

    Sohn DW, Chai IH, Lee DJ, Kim HC, Kim HS, Oh BH, et al. Assessment of mitral annulus velocity by Doppler tissue imaging in the evaluation of left ventricular diastolic function. J Am Coll Cardiol 1997;30:474–80.Google Scholar

  • 14.

    Tsyvian P, Malkin K, Artemieva O, Wladimiroff JW. Assessment of left ventricular filling in normally grown fetuses, growth-restricted fetuses and fetuses of diabetic mothers. Ultrasound Obstet Gynecol 1998;12:33–8.Google Scholar

  • 15.

    Sağol S, Sağol O, Ozdemir N. Stereological quantification of placental villus vascularization and its relation to umbilical artery Doppler flow in intrauterine growth restriction. Prenat Diagn 2002;22:398–403.Google Scholar

  • 16.

    M Kady S, Gardosi J. Perinatal mortality and fetal growth restriction. Best Pract Res Clin Obstet Gynecol 2004;18: 397–410.Google Scholar

  • 17.

    Figueras F, Eixarch E, Meler E, Iraola A, Figueras J, Peurto B, et al. Small-for-gestational-age fetuses with normal umbilical artery Doppler have suboptimal perinatal and neurodevelopmental outcome. Eur J Obstet Gynecol Reprod Biol 2008;136:34–8.Google Scholar

  • 18.

    Figueras F, Peurto B, Martinez JM, Cararach V, Vanrell JA. Cardiac function monitoring of fetuses with growth restriction. Eur J Obstet Gynecol Reprod Biol 2003;110:159–63.Google Scholar

  • 19.

    Hecher K, Snijders R, Campbell S, Nicolaides K. Fetal venous, intracardiac, and arterial blood flow measurements in intrauterine growth retardation: relationship with fetal blood gases. Am J Obstet Gynecol 1995;173:10–5.Google Scholar

  • 20.

    Naujorks AA, Zielinsky P, Beltrame PA, Castagna RC, Petracco R, Busato A, et al. Myocardial tissue Doppler assessment of diastolic function in the growth-restricted fetus. Ultrasound Obstet Gynecol 2009;34:68–73.Google Scholar

  • 21.

    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;203:45.e1–7.Google Scholar

  • 22.

    Yu CM, Sanderson JE, Marwick TH, Oh JK. Tissue Doppler imaging a new prognosticator for cardiovascular diseases. J Am Coll Cardiol 2007;49:1903–14.Google Scholar

  • 23.

    Ganame J, Claus P, Uyttebroeck A, Renard M, D’hooge J, Bijnens B, et al. Myocardial dysfunction late after low-dose anthracycline treatment in asymptomatic pediatric patients. J Am Soc Echocardiogr 2007;20:1351–8.Google Scholar

  • 24.

    Comas M, Crispi F, Cruz-Martinez R, Figueras F, Gratacos E. Tissue Doppler echocardiographic markers of cardiac dysfunction in small-for-gestational age fetuses. Am J Obstet Gynecol 2011;205:57.e1–6.Google Scholar

  • 25.

    Perez-Cruz M, Cruz-Lemini M, Fernandez MT, Parra JA, Bartrons J, Gomez-Roig MD, et al. Fetal cardiac function in late-onset intrauterine growth restriction vs. small-for-gestational age, as defined by estimated fetal weight, cerebroplacental ratio and uterine artery Doppler. Ultrasound Obstet Gynecol 2015;46:465–71.Google Scholar

About the article

Corresponding author: Başak Kaya, MD, Department of Maternal-Fetal Medicine, Istanbul Medipol University Hospital, TEM Avrupa Otoyolu Göztepe Çıkışı no: 1, Bağcılar, Istanbul 34214, Turkey

Received: 2019-06-07

Accepted: 2019-07-21

Published Online: 2019-08-06

Published in Print: 2019-10-25

Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

Research funding: None declared.

Employment or leadership: None declared.

Honorarium: None declared.

Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

Citation Information: Journal of Perinatal Medicine, Volume 47, Issue 8, Pages 879–884, ISSN (Online) 1619-3997, ISSN (Print) 0300-5577, DOI: https://doi.org/10.1515/jpm-2019-0206.

Export Citation

© 2019 Walter de Gruyter GmbH, Berlin/Boston.Get Permission

Comments (0)

Please log in or register to comment.
Log in