Cardiovascular Changes in IUGR

  • Giancarlo Mari
  • Brian Brocato
  • Roopali V. Donepudi


Despite a plethora of publications existing in the literature, there is still confusion about the definition and management of intrauterine growth-restricted fetuses. A second source of confusion lies in the fundamental misunderstanding that all growth-restricted fetuses are the same and all will progress to cardiovascular failure following a similar time frame. Once intrauterine growth restriction is identified, obstetrical management is focused on assuring safety while the fetus continues to mature within a potentially hostile intrauterine environment. In the United States, the approach to management and delivery of the premature growth-restricted fetus is often based on serial biophysical profile evaluations, whereas in Europe it is usually based on the result of the cardiotocography. However, there is no single test that seems superior to the other available tests for timing the delivery of the growth-restricted fetus. Therefore, the decision to deliver a fetus, especially at <32 weeks, remains mostly on the basis of empirical management. The staging system may allow comparison of outcome data for IUGR fetuses and may be valuable in determining more timely delivery for these high-risk fetuses. Most investigators agree that Doppler ultrasonography of the umbilical artery and the middle cerebral arteries, in combination with biometry provides the best tool to identify small fetuses at risk for adverse outcomes. The umbilical artery and the middle cerebral artery are the two vessels that have been extensively studied. Recent studies have looked into the analysis of the fetal venous system and the association between changes in this system with the fetal outcome.


Middle Cerebral Artery Uterine Artery Pulsatility Index Fetal Heart Rate Umbilical Artery 



Absent flow


Amniotic fluid index


Appropriate for gestational age


Absent/reversed end diastolic flow


Biophysical profile






Ductus venosus


Ductus venosus reversed flow


End diastolic velocity


Estimated fetal weight


Fetal death


Forward flow


Isovolumetric relaxation


Isovolumetric relaxation velocity


Intrauterine fetal demise


Intrauterine growth restriction


Inferior vena cava


Middle cerebral artery pulsatility index


Middle cerebral artery peak systolic velocity


Neonatal death


Neonatal intensive care unit


Neonatal survival


Non-stress test


Peak diastolic velocity


Pulsatility index


Reversed flow


Systolic/diastolic ratio


Short-term variability


Umbilical artery


  1. Arduini D, Rizzo G, Romanini C. Changes of pulsatility index from fetal vessels preceding the onset of late decelerations in growth-retarded fetuses. Obstet Gynecol. 1992;79:605–10.PubMedGoogle Scholar
  2. Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1:1077–81.PubMedCrossRefGoogle Scholar
  3. Baschat AA, Gembruch U, Harman CR. The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens. Ultrasound Obstet Gynecol. 2001;18:571–7.PubMedCrossRefGoogle Scholar
  4. Cosmi E, Ambrosini G, D’Antona D, Saccardi C, Mari G. Doppler, cardiotocography, and biophysical profile changes in growth restricted fetuses. Obstet Gynecol. 2005;106:1240–5.PubMedCrossRefGoogle Scholar
  5. Dawes GS, Redman CW, Smith JH. Improvements in the registration and analysis of fetal heart rate records at the bedside. Br J Obstet Gynaecol. 1985;92:317–25.PubMedCrossRefGoogle Scholar
  6. Detti L, Mari G, Akiyama M, Cosmi E, Moise KJ Jr, Stefor T, Conaway M, Deter R. Longitudinal assessment of the middle cerebral artery peak systolic velocity in healthy fetuses and in fetuses at risk for anemia. Am J Obstet Gynecol. 2002;187:937–9.PubMedCrossRefGoogle Scholar
  7. Devoe L, Golde S, Kilman Y, Morton D, Shea K, Waller J. A comparison of visual analyses of intrapartum fetal heart rate tracings according to the new national institute of child health and human development guidelines with computer analyses by an automated fetal heart rate monitoring system. Am J Obstet Gynecol. 2000;183:361–6.PubMedCrossRefGoogle Scholar
  8. Ferrazzi E, Bozzo M, Rigano S, Bellotti M, Morabito A, Pardi G, Battaglia FC, Galan HL. Temporal sequence of abnormal Doppler changes in the peripheral and central circulatory systems of the severely growth-restricted fetus. Ultrasound Obstet Gynecol. 2002;19:140–6.PubMedCrossRefGoogle Scholar
  9. Hanif F, Drennan K, Mari G. Variables affecting the middle cerebral artery peak systolic velocity in anemic and IUGR fetuses. Am J Perinatol. 2007;24:501–5.PubMedCrossRefGoogle Scholar
  10. Hecher K, Bilardo CM, Stigter RH, Ville Y, Hackelöer BJ, Kok HJ, Senat MV, Visser GH. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol. 2001;18:564–70.PubMedCrossRefGoogle Scholar
  11. Kaur S, Picconi JL, Chadha R, Kruger M, Mari G. Biophysical profile in the treatment of intrauterine growth-restricted fetuses who weigh <1000 g. Am J Obstet Gynecol. 2008;199(264):e1–4.PubMedGoogle Scholar
  12. Kontopoulos EV, Quintero RA, Chmait RH, Bornick PW, Russell Z, Allen MH. Percent absent end diastolic velocity in the umbilical artery waveform as a predictor of intrauterine fetal demise of the donor twin after selective laser photocoagulation of communication vessels in twin-twin transfusion syndrome. Ultrasound Obstet Gynecol. 2007;30:35–9.PubMedCrossRefGoogle Scholar
  13. Manning FA. Fetal biophysical profile: a critical appraisal. Clin Obstet Gynecol. 2002;45:975–85.PubMedCrossRefGoogle Scholar
  14. Mari G, Deter RL. Middle cerebral artery flow velocity waveforms in normal and small-for-gestational-age fetuses. Am J Obstet Gynecol. 1992;166:1262–70.PubMedGoogle Scholar
  15. Mari G, Wasserstrum N. Flow velocity waveforms of the fetal circulation preceding fetal death in a case of lupus anticoagulant. Am J Obstet Gynecol. 1991;164:776–8.PubMedGoogle Scholar
  16. Mari G, Deter RL, Carpenter RL, Rahman F, Zimmerman R, Moise KJ Jr, Dorman KF, Ludomirsky A, Gonzalez R, Gomez R, Oz U, Detti L, Copel JA, Bahado-Singh R, Berry S, Martinez-Poyer J, Blackwell SC. Non-invasive diagnosis by Doppler ultrasonography of fetal anemia due to maternal red cell alloimmunization. Collaborative Group for Doppler Assessment of the Blood Velocity in Anemic Fetuses. N Engl J Med. 2000;342:9–14.PubMedCrossRefGoogle Scholar
  17. Mari G, Roberts A, Detti L, Kovanci E, Stefos T, Bahado-Singh RO, Deter RL, Fisk NM. Perinatal morbidity and mortality rates in severe twin-twin transfusion syndrome: results of the International Amnioreduction Registry. Am J Obstet Gynecol. 2001;185:708–15.PubMedCrossRefGoogle Scholar
  18. Mari G, Abuhamad A, Cosmi E, Segata M, Altaye M, Akiyama M. Middle cerebral artery peak systolic velocity—technique and Variability. J Ultrasound Med. 2005;24:425–30.PubMedGoogle Scholar
  19. Mari G, Hanif F, Drennan K, Kruger M. Staging of intrauterine growth-restricted fetuses. J Ultrasound Med. 2007a;26:1469–77.PubMedGoogle Scholar
  20. Mari G, Hanif F, Kruger M, Cosmi E, Santolaya-Forgas J, Treadwell MC. Middle cerebral artery peak systolic velocity: a new Doppler parameter in the assessment of growth-restricted fetuses. Ultrasound Obstet Gynecol. 2007b;29:310–6.PubMedCrossRefGoogle Scholar
  21. Mari G, Hanif F, Treadwell MC, Kruger M. Gestational age at delivery and Doppler waveforms in very preterm IUGR fetuses as predictors of perinatal mortality. J Ultrasound Med. 2007c;26:555–9.PubMedGoogle Scholar
  22. Mari G, Hanif F, Kruger M. Sequence of cardiovascular changes in IUGR in pregnancies with and without preeclampsia. Prenat Diagn. 2008;28:377–83.PubMedCrossRefGoogle Scholar
  23. Pardi G, Cetin I, Marconi AM, Lanfranchi A, Bozzetti P, Ferrazzi E, Buscaglia M, Battaglia FC. Diagnostic value of blood sampling in fetuses with growth retardation. N Engl J Med. 1993;238:692–6.CrossRefGoogle Scholar
  24. Picconi J, Hanif F, Mari G. Ductus venosus reversed flow in IUGR fetuses: is it an indication for delivery? Am J Perinatol. 2008a;25:199–204.PubMedCrossRefGoogle Scholar
  25. Picconi JL, Kruger MS, Mari G. Ductus Venosus S-Wave/Isovolumetric A-Wave (SIA) Index and A-Wave reversed flow in severely premature growth-restricted fetuses. J Ultrasound Med. 2008b;27:1283–9.PubMedGoogle Scholar
  26. Senat MV, Loizeau S, Couderc S, Bernard JP, Villie Y. The value of middle cerebral artery peak systolic velocity in the diagnosis of fetal anemia after intrauterine death of one monochorionic twin. Am J Obstet Gynecol. 2003;189:1320–4.PubMedCrossRefGoogle Scholar
  27. Soothill PW, Ajayi RA, Campbell S, Roth EM, Candy DC, Snijders RM, Nicolaides KH. Relationship between fetal acidemia at cordocentesis and subsequent neurodevelopment. Ultrasound Obstet Gynecol. 1992;1(2):80–3.CrossRefGoogle Scholar
  28. Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins L. Fetal umbilical artery flow velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol. 1985;92:23–30.PubMedGoogle Scholar
  29. Zimmerman R, Carpenter RJ Jr, Durig P, Mari G. Longitudinal measurement of peak systolic velocity in the fetal middle cerebral artery for monitoring pregnancies complicated by red cell alloimmunisation: a prospective multicentre trial with intention-to-treat. Br J Obstet Gynaecol. 2002;109:746–52.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Giancarlo Mari
    • 1
  • Brian Brocato
    • 2
  • Roopali V. Donepudi
    • 3
  1. 1.Department of Obstetrics & GynecologyUniversity of Tennessee Health Science CenterMemphisUSA
  2. 2.Department of Obstetrics & GynecologyUniversity of Tennessee Health Science CenterMemphisUSA
  3. 3.Department of Obstetrics & Gynecology and Women’s HealthAlbert Einstein College of Medicine of Yeshiva UniversityBronxUSA

Personalised recommendations