Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • State of the Art
  • Published:

State-of-the-Art

Clinician performed ultrasound in fetal growth restriction: fetal, neonatal and pediatric aspects

Abstract

Fetal growth restriction (FGR) affects 7–10% pregnancies. Conventional and tissue Doppler imaging has noted cardiac compromise during fetal and early neonatal periods in this cohort. In this article, we discuss the use of salient ultrasound parameters across age groups. During fetal life, certain feto-placental sonographic parameters have been linked to adverse perinatal outcomes and are predictive of later life hypertension. During the early postnatal period altered morphometry (hypertrophied and globular hearts) with sub-clinical impairment of cardiac function has been noted in both term and preterm infants with FGR. Vascular imaging has noted thickened and stiffer arteries in association with significantly elevated blood pressure. Similar findings in the pediatric age groups indicate persistence of these alterations, and have formed the basis of intervention studies. Assessment methodology and clinical relevance of these parameters, especially in designing and monitoring of intervention strategies is discussed. Frontline care givers (obstetricians and neonatologists) are increasingly using point of care ultrasound to discern these manifestations of FGR during the sub-clinical phase.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

References

  1. Evans N . Echocardiography on neonatal intensive care units in Australia and New Zealand. J Paediatr Child Health 2000; 36 (2): 169–171.

    Article  CAS  Google Scholar 

  2. Sehgal A, Mehta S, Evans N, McNamara PJ . Cardiac sonography by the neonatologist: clinical usefulness and educational perspective. J Ultrasound Med 2014; 33 (8): 1401–1406.

    Article  Google Scholar 

  3. Nguyen J, Amirnovin R, Ramanathan R, Noori S . The state of point-of-care ultrasonography use and training in neonatal–perinatal medicine and pediatric critical care medicine fellowship programs. J Perinatol 2016; 36: 972–976.

    Article  CAS  Google Scholar 

  4. Figueras F, Gratacós E . Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther 2014; 36 (2): 86–98.

    Article  Google Scholar 

  5. Gardosi J, Madurasinghe V, Williams M, Malik A, Francis A . Maternal and fetal risk factors for stillbirth: population-based study. Brit Med J 2013; 346: f108.

    Article  Google Scholar 

  6. Baschat AA . Neurodevelopment after fetal growth restriction. Fetal Diagn Ther 2014; 36 (2): 136–142.

    Article  Google Scholar 

  7. Demicheva E, Crispi F . Long-term follow-up of intrauterine growth restriction: cardiovascular disorders. Fetal Diagn Ther 2014; 36 (2): 143–153.

    Article  Google Scholar 

  8. Lees C, Marlow N, Arabin B, Bilardo CM, Brezinka C, Derks JB et al. Perinatal morbidity and mortality in early-onset fetal growth restriction: cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE). Ultrasound Obstet Gynecol 2013; 42 (4): 400–408.

    Article  CAS  Google Scholar 

  9. Arbeille P, Maulik D, Fignon A, Stale H, Berson M, Bodard S et al. Assessment of the fetal PO 2 changes by cerebral and umbilical Doppler on lamb fetuses during acute hypoxia. Ultrasound Med Biol 1995; 21: 861–870.

    Article  CAS  Google Scholar 

  10. Baschat AA, Gembruch U . The cerebroplacental Doppler ratio revisited. Ultrasound Obstet Gynecol 2003; 21: 124–127.

    Article  CAS  Google Scholar 

  11. Fouron JC, Gosselin J, Raboisson MJ, Lamoureux J, Tison CA, Fouron C et al. The relationship between an aortic isthmus blood flow velocity index and the postnatal neurodevelopmental status of fetuses with placental circulatory insufficiency. Am J Obstet Gynecol 2005; 192: 497–503.

    Article  Google Scholar 

  12. Baschat AA, Cosmi E, Bilardo CM, Wolf H, Berg C, Rigano S et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol 2007; 109: 253–261.

    Article  Google Scholar 

  13. Rodríguez-López M, Cruz-Lemini M, Valenzuela-Alcaraz B, Garcia-Otero L, Sitges M, Bijnens B et al. Descriptive analysis of the different phenotypes of cardiac remodelling in fetal growth restriction. Ultrasound Obstet Gynecol 2016 (doi:10.1002/uog.17365; e-pub ahead of print).

  14. Cruz-Lemini M, Crispi F, Valenzuela-Alcaraz B, Figueras F, Gómez O, Sitges M et al. A fetal cardiovascular score to predict infant hypertension and arterial remodelling in intrauterine growth restriction. Am J Obstet Gynecol 2014; 210 (6): 552.e1–552.e22.

    Article  Google Scholar 

  15. Crispi F, Bijnens B, Sepulveda-Swatson E, Cruz-Lemini M, Rojas-Benavente J, Gonzalez-Tendero A et al. Postsystolic shortening by myocardial deformation imaging as a sign of cardiac adaptation to pressure overload in fetal growth restriction. Circ Cardiovasc Imaging 2014; 7 (5): 781–787.

    Article  Google Scholar 

  16. Sehgal A, Doctor T, Menahem S . Cardiac function and arterial indices in infants born small for gestational age: analysis by speckle tracking. Acta Paediatr 2014; 103: e49–e54.

    Article  Google Scholar 

  17. Pérez-Cruz M, Cruz-Lemini M, Fernández MT, Parra JA, Bartrons J, Gómez-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 (4): 465–471.

    Article  Google Scholar 

  18. Turan OM, Turan S, Gungor S, Berg C, Moyano D, Gembruch U et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008; 32: 160–167.

    Article  CAS  Google Scholar 

  19. Veronese E, Tarroni G, Visentin S, Cosmi E, Linguraru MG, Grisan E . Estimation of prenatal aorta intima-media thickness from ultrasound examination. Phys Med Biol 2014; 59: 6355–6371.

    Article  CAS  Google Scholar 

  20. Zanardo V, Visentin S, Bertin M, Zaninotto M, Trevisanuto D, Cavallin F et al. Aortic wall thickness and amniotic fluid albuminuria in growth-restricted twin fetuses. Twin Res Hum Genet 2013; 16: 720–726.

    Article  Google Scholar 

  21. Alfirevic Z, Stampalija T, Gyte GM . Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev 2010; CD007529.

  22. Thornton JG, Hornbuckle J, Vail A, Spiegelhalter DJ, Levene M . GRIT study group.et al: Infant well-being at 2 years of age in the Growth Restriction Intervention Trial (GRIT): multi-centred randomised controlled trial. Lancet 2004; 364: 513–520.

    Article  CAS  Google Scholar 

  23. Skilton MK, Evans N, Griffiths KA, Harmer JA, Celermajer DS . Aortic wall thickness in newborns with intrauterine restriction. Lancet 2005; 23: 1484–1486.

    Article  Google Scholar 

  24. Altın H, Karaarslan S, Karataş Z, Alp H, Şap F, Baysal T . Evaluation of cardiac functions in term small for gestational age newborns with mild growth retardation: a serial conventional and tissue Doppler imaging echocardiographic study. Early Hum Dev 2012; 88 (9): 757–764.

    Article  Google Scholar 

  25. 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.

    Article  Google Scholar 

  26. Sehgal A, Skilton MR, Crispi F . Human fetal growth restriction: a cardiovascular journey through to adolescence. J Dev Orig Health Dis 2016; 7: 1–10.

    Article  Google Scholar 

  27. Fouzas S, Karatza AA, Davlouros PA, Chrysis D, Alexopoulos D, Mantagos S et al. Neonatal cardiac dysfunction in intrauterine growth restriction. Pediatr Res 2014; 75: 651–657.

    Article  Google Scholar 

  28. Bradley TJ, Potts JE, Lee SK, Potts MT, De Souza AM, Sandor GG . Early changes in the biophysical properties of the aorta in pre-adolescent children born small for gestational age. J Pediatr 2010; 156: 388–392.

    Article  Google Scholar 

  29. Crispi F, Figueras F, Cruz-Lemini M, Bartrons J, Bijnens B, Gratacos E et al. Cardiovascular programming in children born small for gestational age and relationship with prenatal signs of severity. Am J Obstet Gynecol 2012; 207: 121.e1–121.e9.

    Article  Google Scholar 

  30. Sehgal A, Allison BJ, Gwini SM, Miller SL, Polglase GR . Cardiac morphology and function in preterm growth restricted infants: relevance for clinical sequelae. J Pediatr 2017; pii: S0022-3476(17)30772-2.

  31. Mahomed FA . Remarks on arterio-capillary fibrosis and its clinical recognition. Lancet 1877; 110 (2816): 232–234.

    Article  Google Scholar 

  32. Riva-Rocci S . Un nuovo sfigmomanometro. Gazz Med Torino 1896; 50–51: 1001–1007.

    Google Scholar 

  33. Martyn CN, Greenwald SE . Impaired synthesis of elastin in walls of aorta and large conduit arteries during early development as an initiating event in pathogenesis of systemic hypertension. Lancet 1997; 350: 953–955.

    Article  CAS  Google Scholar 

  34. Cheung YF, Taylor MJ, Fisk NM, Redington AN, Gardiner HM . Fetal origins of reduced arterial distensibility in the donor twin in twin-twin transfusion syndrome. Lancet 2000; 355: 1157–1158.

    Article  CAS  Google Scholar 

  35. McGill HC Jr, McMahan CA, Herderick EE, Zieske AW, Malcom GT, Tracy RE et al. Pathobiological determinants of atherosclerosis in youth research group - effect of coronary heart disease risk factors on atherosclerosis of selected regions of the aorta and right coronary artery. Arterioscler Thromb Vasc Biol 2000; 20: 836–845.

    Article  Google Scholar 

  36. Litwin M, Niemirska A . Intima-media thickness measurements in children with cardiovascular risk factors. Pediatr Nephrol 2008; 24: 707–719.

    Article  Google Scholar 

  37. Sehgal A, Allison BJ, Gwini SM, Menahem S, Miller SL, Polglase GR . Early vascular ageing and arterial-ventricular maladaptive coupling in preterm infants with fetal growth restriction. J Perinatol 2017 (in press).

  38. Agostoni C, Braegger C, Decsi T, Kolacek S, Koletzko B, Michaelsen KF et al. Breast-feeding: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr 2009; 49: 112–125.

    Article  Google Scholar 

  39. Ayer JG, Harmer JA, Xuan W, Toelle B, Webb K, Almqvist C et al. Dietary supplementation with n-3 polyunsaturated fatty acids in early childhood: effects on blood pressure and arterial structure and function at age 8 y. Am J Clin Nutr 2009; 90: 438–446.

    Article  CAS  Google Scholar 

  40. Rees S, Harding R, Inder T . The Developmental Environment and the Origins of Neurological Disorders. Cambridge University Press: Cambridge, UK, 2006.

    Book  Google Scholar 

  41. Figueras F, Benavides A, Del Rio M, Crispi F, Eixarch E, Martinez JM et al. Monitoring of fetuses with intrauterine growth restriction: longitudinal changes in ductus venosus and aortic isthmus flow. Ultrasound Obstet Gynecol 2009; 33: 39–43.

    Article  CAS  Google Scholar 

  42. Cruz-Martinez R, Tenorio V, Padilla N, Crispi F, Figueras F, Gratacos E . Risk of ultrasound-detected neonatal brain abnormalities in intrauterine growth-restricted fetuses born between 28 and 34 weeks' gestation: relationship with gestational age at birth and fetal Doppler parameters. Ultrasound Obstet Gynecol 2015; 46: 452–459.

    Article  CAS  Google Scholar 

  43. Fonta C, Imbert M . Vascularization in the primate visual cortex during development. Cereb Cortex 2002; 12: 199–211.

    Article  Google Scholar 

  44. Senitz D, Benninghoff J . Histomorphology of angiogenesis in human perinatal orbitofrontal cortex: a Golgi and electron microscopic study of anastomosis formation. Anat Embryol (Berl) 2003; 206: 479–485.

    Article  Google Scholar 

  45. Geva R, Eshel R, Leitner Y, Fattal-Valevski A, Harel S . Memory functions of children born with asymmetric intrauterine growth restriction. Brain Res 2006; 1117: 186–194.

    Article  CAS  Google Scholar 

  46. Makikallio K, Rasanen J, Makikallio T, Vuolteenaho O, Huhta JC . Human fetal cardiovascular profile score and neonatal outcome in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008; 31: 48–54.

    Article  CAS  Google Scholar 

  47. Appleton RE, Lee RE, Hey EN . Neurodevelopmental outcome of transient neonatal intracerebral echodensities. Arch Dis Child 1990; 65: 27–29.

    Article  CAS  Google Scholar 

  48. Padilla-Gomes NF, Enríquez G, Acosta-Rojas R, Perapoch J, Hernandez-Andrade E, Gratacos E . Prevalence of neonatal ultrasound brain lesions in premature infants with and without intrauterine growth restriction. Acta Pædiatr 2007; 96: 1582–1587.

    Article  Google Scholar 

  49. Tolsa CB, Zimine S, Warfield SK, Freschi M, Sancho Rossignol A, Lazeyras F et al. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res 2004; 56: 132–138.

    Article  Google Scholar 

  50. Keunen K, Kersbergen KJ, Groenendaal F, Isgum I, de Vries LS, Benders MJ . Brain tissue volumes in preterm infants: prematurity, perinatal risk factors and neurodevelopmental outcome: a systematic review. J Matern Fetal Neonatal Med 2012; 25: 89–100.

    Article  Google Scholar 

  51. Verburg BO, Geelhoed JJM, Steegers EAP, Hofman A, Moll HA, Witteman JC et al. Fetal kidney volume and its association with growth and blood flow in fetal life: the generation R study. Int Soc Nephrol 2007; 72: 754–761.

    CAS  Google Scholar 

  52. Silver LE, Decamps PJ, Korst LM, Platt LD, Castro L . Intrauterine growth restriction is accompanied by decreased renal volume in the human fetus. Am J Obstet Gynecol 2003; 188: 1320–1325.

    Article  Google Scholar 

  53. Surányi A, Nyári T, Keresztúri A, Pál A . What does fetal renal echogenicity mean in intrauterine growth retardation? Orv Hetil 2006; 147: 1997–2002.

    PubMed  Google Scholar 

  54. Zanardo V, Fanelli T, Weiner G, Fanos V, Zaninotto M, Visentin S et al. Intrauterine growth restriction is associated with persistent aortic wall thickening and glomerular proteinuria during infancy. Kidney Int 2011; 80: 119–123.

    Article  Google Scholar 

  55. Ota E, Hori H, Mori R, Tobe-Gai R, Farrar D . Antenatal dietary education and supplementation to increase energy and protein intake. Cochrane Database Syst Rev 2015; CD000032.

  56. Mori TA, Beilin LJ . Omega-3 fatty acids and inflammation. Curr Atheroscler Rep 2004; 6: 461–467.

    Article  Google Scholar 

  57. Labayen I, Moreno LA, Ruiz JR, Ortega FB, Sjostrom M, Huybrechts I et al. Associations of birthweight with serum long chain polyunsaturated fatty acids in adolescents; the helena study. Atherosclerosis 2011; 217: 286–291.

    Article  CAS  Google Scholar 

  58. Skilton MR, Ayer JG, Harmer JA, Webb K, Leeder SR, Marks GB et al. Impaired fetal growth and arterial wall thickening: A randomized trial of omega-3 supplementation. Pediatrics 2012; 129: e698–e703.

    Article  Google Scholar 

  59. Skilton MR, Pahkala K, Viikari JS, Ronnemaa T, Simell O, Jula A 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.e1252.

    Article  CAS  Google Scholar 

  60. Skilton MR, Marks GB, Ayer JG, Garden FL, Garnett SP, Harmer JA et al. Weight gain in infancy and vascular risk factors in later childhood. Pediatrics 2013; 131: e1821–e1828.

    Article  Google Scholar 

  61. Stocks T, Renders CM, Bulk-Bunschoten AMW, Hirasing RA, van Buuren S, Seidell JC . Body size and growth in 0- to 4-year-old children and the relation to body size in primary school age. Obes Rev 2011; 12: 637–652.

    Article  CAS  Google Scholar 

  62. Rodriguez-Lopez M, Osorio L, Acosta R, Figueras J, Cruz-Lemini M, Figueras F et al. Influence of breastfeeding and postnatal nutrition on cardiovascular remodelling induced by fetal growth restriction. Pediatr Res 2016; 79: 100–106.

    Article  CAS  Google Scholar 

  63. Kizirian NV, Kong Y, Muirhead R, Brodie S, Garnett SP, Petocz P et al. Effects of a low-glycemic index diet during pregnancy on offspring growth, body composition, and vascular health: a pilot randomized controlled trial. Am J Clin Nutr 2016; 103: 1073–1082.

    Article  CAS  Google Scholar 

  64. Reiner Z, Catapano AL, De Backer G, Graham I, Taskinen MR, Wiklund O et al. Guidelines ESCCfP, Committees. Esc/eas guidelines for the management of dyslipidaemias: the task force for the management of dyslipidaemias of the European Society of Cardiology and the European Atherosclerosis Society. Eur Heart J 2011; 32: 1769–1818.

    Article  Google Scholar 

Download references

Acknowledgements

Dr Crispi's work was partially supported by grants from Obra Social la Caixa and Instituto Carlos III (PI14/00226 and INT16/00168) cofinanced by the Fondo Europeo de Desarrollo Regional de la Unión Europea "Una manera de hacer europa" (FEDER), Spain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A Sehgal.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sehgal, A., Crispi, F., Skilton, M. et al. Clinician performed ultrasound in fetal growth restriction: fetal, neonatal and pediatric aspects. J Perinatol 37, 1251–1258 (2017). https://doi.org/10.1038/jp.2017.119

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/jp.2017.119

This article is cited by

Search

Quick links