Angiogenic Factors and Doppler Evaluation in Normally Growing Fetuses at Routine Third-Trimester Scan: Prediction of Subsequent Low Birth Weight

Fetal Diagnosis and Therapy

Volumn 40, Issue 1, 2016, Pages 13-20

  Triunfo, Stefania ^a,b   Parra Saavedra, Miguel ^a,b,d   Rodriguez Sureda, Victor ^b,c   Crovetto, Francesca ^a,b,e   Dominguez, Carmen ^b,c   Gratacós, Eduard ^a,b   Figueras, Francesc ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^d CEDIUL   (Colombia)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

Doppler parameters; Fetal growth restriction; Placental growth factor; Smallness for gestational age at birth; Soluble fms like tyrosine kinase 1

Indexed keywords

ANGIOGENIC FACTOR; PLACENTAL GROWTH FACTOR; SOLUBLE FMS LIKE TYROSINE KINASE 1; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; BIOLOGICAL MARKER;

ADULT; ARTICLE; BLOOD VESSEL PARAMETERS; CASE CONTROL STUDY; CEREBROPLACENTAL RATIO; CONTROLLED STUDY; DIAGNOSTIC VALUE; DOPPLER ULTRASONOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FALSE POSITIVE RESULT; FEMALE; FETUS; FETUS ECHOGRAPHY; HUMAN; MAJOR CLINICAL STUDY; MEAN UTERINE ARTERY PULSATILITY INDEX; PARAMETERS CONCERNING THE FETUS, NEWBORN AND PREGNANCY; PRENATAL DIAGNOSIS; PRIORITY JOURNAL; REAL TIME ULTRASOUND SCANNER; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; SMALL FOR DATE INFANT; THIRD TRIMESTER PREGNANCY; UMBILICAL CORD BLOOD FLOW; UMBILICAL VEIN; UTERINE ARTERY; VEIN BLOOD FLOW; COHORT ANALYSIS; DIAGNOSTIC IMAGING; INTRAUTERINE GROWTH RETARDATION; LOW BIRTH WEIGHT; METABOLISM; NEWBORN; PREGNANCY; STATISTICAL MODEL;

ANGIOGENESIS INDUCING AGENTS; BIOMARKERS; CASE-CONTROL STUDIES; COHORT STUDIES; FEMALE; FETAL GROWTH RETARDATION; HUMANS; INFANT, LOW BIRTH WEIGHT; INFANT, NEWBORN; LOGISTIC MODELS; PREGNANCY; PREGNANCY TRIMESTER, THIRD; ROC CURVE; ULTRASONOGRAPHY, PRENATAL;

EID: 84942693680     PISSN: 10153837     EISSN: 14219964     Source Type: Journal    
DOI: 10.1159/000440650     Document Type: Article

References (49)

1. McIntire DD, Bloom SL, Casey BM, Leveno KJ: Birth weight in relation to morbidity and mortality among newborn infants. N Engl J Med 1999; 340: 1234-1238.
2. Breeze AC, Lees CC: Prediction and perinatal outcomes of fetal growth restriction. Semin Fetal Neonatal Med 2007; 12: 383-397.
3. Figueras F, Oros D, Cruz-Martinez R, Padilla N, Hernandez-Andrade E, Botet F, Costas-Moragas C, Gratacos E: Neurobehavior in term, small-for-gestational age infants with normal placental function. Pediatrics 2009; 124:e934-e941.
4. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS: Fetal nutrition and cardiovascular disease in adult life. Lancet 1993; 341: 938-941.
5. Demicheva E, Crispi F: Long-term follow-up of intrauterine growth restriction: cardiovascular disorders. Fetal Diagn Ther 2014; 36: 143-153.
6. Gardosi J, Madurasinghe V, Williams M, Malik A, Francis A: Maternal and fetal risk factors for stillbirth: population based study. BMJ 2013; 346:f108.
7. Lindqvist PG, Molin J: Does antenatal identification of small-for-gestational age fetuses significantly improve their outcome? Ultrasound Obstet Gynecol 2005; 25: 258-264.
8. Hepburn M, Rosenberg K: An audit of the detection and management of small-for-gestational age babies. Br J Obstet Gynaecol 1986; 93: 212-216.
9. Souka AP, Papastefanou I, Pilalis A, Michalitsi V, Kassanos D: Performance of third-trimester ultrasound for prediction of small-forgestational-age neonates and evaluation of contingency screening policies. Ultrasound Obstet Gynecol 2012; 39: 535-542.
10. Bricker L, Neilson JP, Dowswell T: Routine ultrasound in late pregnancy (after 24 weeks' gestation). Cochrane Database Syst Rev 2008; 4:CD001451.
11. Parra-Saavedra M, Crovetto F, Triunfo S, Savchev S, Peguero A, Nadal A, Parra G, Gratacos E, Figueras F: Placental findings in late-onset SGA births without Doppler signs of placental insufficiency. Placenta 2013; 34: 1136-1141.
12. Mifsud W, Sebire NJ: Placental pathology in early-onset and late-onset fetal growth restriction. Fetal Diagn Ther 2014; 36: 117-128.
13. 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-forgestational age fetuses. Ultrasound Obstet Gynecol 2011; 37: 191-195.
14. Severi FM, Bocchi C, Visentin A, Falco P, Cobellis L, Florio P, Zagonari S, Pilu G: Uterine and fetal cerebral Doppler predict the outcome of third-trimester small-for-gestational age fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 2002; 19: 225-228.
15. Vergani P, Roncaglia N, Andreotti C, Arreghini A, Teruzzi M, Pezzullo JC, Ghidini A: Prognostic value of uterine artery Doppler velocimetry in growth-restricted fetuses delivered near term. Am J Obstet Gynecol 2002; 187: 932-936.
16. Ghosh GS, Gudmundsson S: Uterine and umbilical artery Doppler are comparable in predicting perinatal outcome of growth-restricted fetuses. BJOG 2009; 116: 424-430.
17. Hershkovitz R, Kingdom JC, Geary M, Rodeck CH: Fetal cerebral blood flow redistribution in late gestation: identification of compromise in small fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 2000; 15: 209-212.
18. Cruz-Martinez R, Figueras F, Oros D, Padilla N, Meler E, Hernandez-Andrade E, Gratacos E: Cerebral blood perfusion and neurobehavioral performance in full-term small-for-gestational-age fetuses. Am J Obstet Gynecol 2009; 201: 474.e1-474.e7.
19. Parra-Saavedra M, Crovetto F, Triunfo S, Savchev S, Parra G, Sanz M, Gratacos E, Figueras F: Added value of umbilical vein flow as a predictor of perinatal outcome in term small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 2013; 42: 189-195.
20. Shibata E, Rajakumar A, Powers RW, Larkin RW, Gilmour C, Bodnar LM, Crombleholme WR, Ness RB, Roberts JM, Hubel CA: Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab 2005; 90: 4895-4903.
21. Andraweera PH, Dekker GA, Roberts CT: The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum Reprod Update 2012; 18: 436-457.
22. Soto E, Romero R, Kusanovic JP, Ogge G, Hussein Y, Yeo L, Hassan SS, Kim CJ, Chaiworapongsa T: Late-onset preeclampsia is associated with an imbalance of angiogenic and anti-angiogenic factors in patients with and without placental lesions consistent with maternal underperfusion. J Matern Fetal Neonatal Med 2012; 25: 498-507.
23. Crovetto F, Figueras F, Triunfo S, Crispi F, Rodriguez-Sureda V, Peguero A, Dominguez C, Gratacos E: Added value of angiogenic factors for the prediction of early and late preeclampsia in the first trimester of pregnancy. Fetal Diagn Ther 2014; 35: 258-266.
24. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, Gotsch F, Erez O, Mazaki-Tovi S, Gomez R, Edwin S, Chaiworapongsa T, Levine RJ, Karumanchi SA: A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med 2008; 21: 9-23.
25. Lobmaier SM, Figueras F, Mercade I, Perello M, Peguero A, Crovetto F, Ortiz JU, Crispi F, Gratacós E: Angiogenic factors vs Doppler surveillance in the prediction of adverse outcome among late-pregnancy small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 2014; 43: 533-540.
26. Triunfo S, Lobmaier S, Parra-Saavedra M, Crovetto F, Peguero A, Nadal A, Gratacos E, Figueras F: Angiogenic factors at diagnosis of late-onset small-for-gestational age and histological placental underperfusion. Placenta 2014; 35: 398-403.
27. Figueras F, Meler E, Iraola A, Eixarch E, Coll O, Figueras J, Francis A, Gratacos E, Gardosi J: Customized birthweight standards for a Spanish population. Eur J Obstet Gynecol Reprod Biol 2008; 136: 20-24.
28. Robinson HP, Fleming JE: A critical evaluation of sonar 'crown-rump length' measurements. Br J Obstet Gynaecol 1975; 82: 702-710.
29. Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK: Estimation of fetal weight with the use of head, body, and femur measurements-a prospective study. Am J Obstet Gynecol 1985; 151: 333-337.
30. Gomez O, Figueras F, Fernandez S, Bennasar M, Martinez JM, Puerto B, Gratacos E: Reference ranges for uterine artery mean pulsatility index at 11-41 weeks of gestation. Ultrasound Obstet Gynecol 2008; 32: 128-132.
31. Arduini D, Rizzo G: Normal values of Pulsatility Index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med 1990; 18: 165-172.
32. Brown MA, Lindheimer MD, de Swiet M, van Assche A, Moutquin JM: The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertens Pregnancy 2001; 20:IX-XIV.
33. Gregg AR, Weiner CP: 'Normal' umbilical arterial and venous acid-base and blood gas values. Clin Obstet Gynecol 1993; 36: 24-32.
34. Baschat AA, Gembruch U: The cerebroplacental Doppler ratio revisited. Ultrasound Obstet Gynecol 2003; 21: 124-127.
35. Barbera A, Galan HL, Ferrazzi E, Rigano S, Jozwik M, Battaglia FC, Pardi G: Relationship of umbilical vein blood flow to growth parameters in the human fetus. Am J Obstet Gynecol 1999; 181: 174-179.
36. American College of Obstetricians and Gynecologists: ACOG Practice Bulletin No. 106: Intrapartum fetal heart rate monitoring: nomenclature, interpretation, and general management principles. Obstet Gynecol 2009; 114: 192-202.
37. Altaf S, Oppenheimer C, Shaw R, Waugh J, Dixon-Woods M: Practices and views on fetal heart monitoring: a structured observation and interview study. BJOG 2006; 113: 409-418.
38. Aardema MW, Oosterhof H, Timmer A, van Rooy I, Aarnoudse JG: Uterine artery Doppler flow and uteroplacental vascular pathology in normal pregnancies and pregnancies complicated by pre-eclampsia and small for gestational age fetuses. Placenta 2001; 22: 405-411.
39. Llurba E, Turan O, Kasdaglis T, Harman CR, Baschat AA: Emergence of late-onset placental dysfunction: relationship to the change in uterine artery blood flow resistance between the first and third trimesters. Am J Perinatol 2013; 30: 505-512.
40. Eixarch E, Meler E, Iraola A, Illa M, Crispi F, Hernandez-Andrade E, Gratacos E, Figueras F: Neurodevelopmental outcome in 2-yearold infants who were small-for-gestational age term fetuses with cerebral blood flow redistribution. Ultrasound Obstet Gynecol 2008; 32: 894-899.
41. Arbeille P, Maulik D, Fignon A, Stale H, Berson M, Bodard S, Locatelli A: 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.
42. Bahado-Singh RO, Kovanci E, Jeffres A, Oz U, Deren O, Copel J, Mari G: The Doppler cerebroplacental ratio and perinatal outcome in intrauterine growth restriction. Am J Obstet Gynecol 1999; 180: 750-756.
43. Gramellini D, Folli MC, Raboni S, Vadora E, Merialdi A: Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 1992; 79: 416-420.
44. Morales-Rosello J, Khalil A, Morlando M, Papageorghiou A, Bhide A, Thilaganathan B: Changes in fetal Doppler indices as a marker of failure to reach growth potential at term. Ultrasound Obstet Gynecol 2014; 43: 303-310.
45. Prior T, Mullins E, Bennett P, Kumar S: Prediction of intrapartum fetal compromise using the cerebroumbilical ratio: a prospective observational study. Am J Obstet Gynecol 2013; 208: 124.e1-124.e6.
46. Chaiworapongsa T, Romero R, Korzeniewski SJ, Kusanovic JP, Soto E, Lam J, Dong Z, Than NG, Yeo L, Hernandez-Andrade E, Conde-Agudelo A, Hassan SS: Maternal plasma concentrations of angiogenic/antiangiogenic factors in the third trimester of pregnancy to identify the patient at risk for stillbirth at or near term and severe late preeclampsia. Am J Obstet Gynecol 2013; 208: 287.e1-287.e15.
47. Ahmed A, Dunk C, Ahmad S, Khaliq A: Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PlGF) and soluble Flt-1 by oxygen-a review. Placenta 2000; 21(suppl A):S16-S24.
48. Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, Goncalves L, Edwin S, Kim YM, Erez O, Kusanovic JP, Pineles BL, Papp Z, Hassan S: Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonatal Med 2008; 21: 41-52.
49. Bakalis S, Peeva G, Gonzalez R, Poon LC, Nicolaides KH: Prediction of small-for-gestational-age neonates: screening by biophysical and biochemical markers at 30-34 weeks. Ultrasound Obstet Gynecol 2015, Epub ahead of print.