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The Value of 3D Ultrasound Measurement of Placental Volume in Prediction of IUGR, in Cases of Pre-eclampsia
Design: A longitudinal case-controlled prospective study.
Setting: Obstetrics and Gynecology Department of Al - Azhar University Hospitals between October 2001 to April 2003.
Aim of the Work: Is to study the possible correlation between the placental volume estimation using 3D ultrasound in cases of pre- eclampsia (P.E.) and the associated IUGR and to identify if the placental volume is a reliable index of fetal welfare in pregnancy complicated by pre-eclampsia.
Patients and Methods: Hundred and fifty pregnant women were included in this study, with gestational age between 36-38 weeks and they were followed till delivery. They were classified into 3 groups:
All cases were subjected to history taking, laboratory investigations and 3D ultrasonic examination for gestational age, biophysical profile, placental volume (measured by a parallel ultrasonographic section scan method).
All 3-D ultrasonographic data were recorded at 36 weeks of gestation to be statistically analyzed.
After delivery the newborns were evaluated by Apgar score and birth weight. The placental weight and thickness were determined.
Results: The severe P.E group had the smallest placental volume (612.7+31.6ml) compared to mild P.E (740.1+36.9ml) and control group (850.3+40.1ml). There was a positive correlation between placental volume measured by 3D U/S and the placental weight and thickness measured after birth.
The severe P.E group had significantly higher IUGR rate (82%) compared to (24%) and (12.%) for mild P.E and control groups.
Severe P.E group had significantly lower mean birth weight (2.53+0.38kg) V.S. (3.08+0.24kg) and (3.48+0.32kg) for mild P.E and control groups. There is significant negative correlation between placental volume measured by 3D U/S and the incidence of IUGR in cases of pre-eclampsia. There were significant positive correlation between placental volume and the biophysical profile and Apgar score in cases of severe P.E.
Conclusion : 3-D ultrasound measurement of the placental volume well correlated with placental weight and thickness and neonatal birth weight.
3-D ultrasound measurement of the placental volume is a reliable index of fetal growth and welfare in cases of pre-eclampsia. It can be used as a predictor of IUGR in these cases.
Hypertensive disease with pregnancy is one of the obstetric problems in which the fetus as well as the mother are at risk (Robson, 1999).
Varity of techniques that has been used for appraising the health of the embryo and fetus in utero.
Although Intra uterine growth retardation (IUGR) is a usual finding in pre-eclampsia, little is known about the value of placental volume measurement and it’s relation to the IUGR in cases of pre-eclampsia.
Determination of placental size is a part of the overall assessment of intrauterine environment, placental growth can be estimated by either measuring the thickness or estimating its volume (Geirsson et al., 1985).
Longitudinal sonographic studies of the placental volume have shown wide variation in each stage of gestation (Bleker et al., 1977).
There is some evidence that IUGR is preceded by reduced placental volume in the first half of pregnancy. The development of 3D ultrasound has improve the clinical value of placental volume measurement (Jurkovie et al., 1994).
The aim of this work is to study the possible correlation between the placental volume estimation using 3D ultrasound in cases of pre-eclampsia and the IUGR, and to identify if the placental volume is a reliable index of fetal welfare in pregnancy complicated by pre-eclampsia.
Patients and Methods:
This longitudinal case-controlled prospective study included 150 pregnant women. They were classified into 3 equal groups. Group I included 50 normal pregnant women as a control, group II included 50 pregnant patients with mild pre-eclampsia and group III included 50 pregnant patients with severe pre-eclampsia which was diagnosed and classified according to Cunningham et al. ( 1977).
All measurements in pre-eclamptic patients were made before administration of any antihypertensive medication. Inclusion criteria included : patients between (20-30)years old, primigravidae, with gestational age between 36 and 38 wks., of singleton viable pregnancy without fetal anomalies. All cases were free from any other medical disorders with pregnancy as diabetes mellitus. Approved consent was taken from each case after counseling.
Cases in all groups were subjected to the following:
Results:Table (1) shows descriptive criteria of the studied groups. There was a significant difference between maternal age in the studied groups (P value < 0.05), cases with severe pre-eclampsia were of older age than both mild P.E. and control groups, body mass index (BMI) showed also highly significant increase in cases of sever pre-eclampsia compared to mild P.E. or control groups (P value < 0.001).
Table (2) shows placental volume (ml) estimated by 3D U/S in the studied groups. There was highly significant difference between the studied groups, patients with severe P.E. had the smallest placental volume compared to both mild P.E. and control groups (P value <0.001), also mild P.E. group had sig. small placental volume than control group. P value < 0.05.
Table (3) shows perinatal outcome in the studied groups. Fetuses of cases of severe pre-eclampsia had a lower biophysical profile than those in other groups. The severe P.E. group had sig. higher percentage of IUGR 82% than booth mild P.E. and control groups 24% and 12% respectively. Also mild P.E. group had sig. higher rate of IUGR than control group.
The C.S rate was (64%) in sever pre-eclampsia group V.S. (30%) in mild P.E. group and (18%) in control group with highly statistically significant difference P<0.001. Babies born to severe pre-eclampsia group had lower Apgar score at 1 and 5 minutes, than control and mild P.E. groups. Babies born to severe P.E. group had sig. lower birth weight than both other groups P<0.001.
Table (4) shows placental weight and thickness in the studied groups with highly significant difference between all groups.
Severe pre-eclampsia group had the lowest placental weight and thickness P value <0.001 than other both groups. The mild P.E. group had a significantly lower placental weight and thickness than control group P value < 0.001.
Table (5) shows correlation between 3D U/S measured placental volume and perinatal outcome. In control group there was a positive correlation between placental volume and birth weight, the larger the placental volume the higher is the birth weight. In mild and severe P.E groups; there was a significant negative correlation between placental volume and percentage of IUGR. The smaller the placental volume, the higher is the incidence of IUGR and significant positive correlation was found between placental volume and birth weight, the smaller the placental volume the lower is the birth weight.
In severe P.E group a significant positive correlation was found between placental volume and both the biophysical profile, and Apgar score at 1 and 5 minutes. The lower the placental volume the less are BPP and Apgar score.
Table (6) shows correlation between placental volume as determined by 3D U/S and its weight and thickness at birth with significant positive correlation, the larger the placental volume the higher are placental weight and thickness.
|Control (No.=50)||Mild P.E.T (No. =50)||Severe P.E.T (No.=50)|
|Maternal age (years) X+S.D||22.4+3.21||22.1+3.01||25.3+4.2||12.68||<0.05*|
|Maternal weight (kg)X+S.D||72.7+3.2||75.5+3.67||88.78+4.47||53.27||<0.001**|
|Body mass index (kg/m2)X+S.D||26.58+2.4||29.78+2.77||37.0+1.95||48.48||<0.001**|
|Mean art. B.P. (mmHg)X+S.D||98.6+26||138+28||157+38||32.6||<0.001**|
|Control (No.=50)||Mild P.E.T (No. =50)||Severe P.E.T (No.=50)|
|Placental volume X+S.D||850.3+40.1||740.1+36.9||612.7+31.6||56.21||<0.001*|
|Control (No.=50)||Mild P.E.T (No. =50)||Severe P.E.T (No.=50)|
Test of Sig
|Biophysical profile X+S.D||9.68+0.74||8.4+1.51||6.92+1.957||F=43.20||<0.001*|
|IUGR No. (%)||6 (12%)||12 (24%)||41 (82%)||X2 = 51.53||<0.001*|
|V.D No. (%)||41 (82%)||35 (70%)||18 (36%)||X2 = 24.34||<0.001*|
|C.S No. (%)||9 (18%)||15 (30%)||32 (64%)|
|1st minute :X+S.D||7.5+0.76||6.42+1.43||5.1+1.97||F = 33.48||<0.001*|
|5th minute X+S.D||9.48+0.79||8.84+1.2||7.46+1.81||F = 29.94||<0.001*|
|Birth weight (kgm) X+S.D||3.48+0.32||3.08+0.24||2.53+0.38||F = 21.75||<0.001*|
|Control (No.=50)||Mild P.E.T (No. =50)||Severe P.E.T (No.=50)|
|Placental weight (gm) Range X+S.D||450-600541+41.66||300-620459.2+78.81||300-500390+51.54||79.99||<0.0001*|
|Placental thickness (cm)Range X+S.D||3.5-65.18+0.8||3-5.23.84+0.63||1.2-42.1+0.884||197.26||<0.0001*|
Hypertention is the most common medical disorder with pregnancy and pre-eclampsia constitutes two thirds of cases of hyperention with pregnancy (Seligman et al., 1994). It complicates 5-10% of all pregnancies and is a strong indication of women at risk of perinatal complications and poor pregnancy outcome (Acromite et al., 1999). In earlier studies, Dawn (1995) and Theam et al. (2001) described the positive predictive value of a small second-trimester placental volume as measured by U/S in prediction of the fetal outcome. While, Hafner et al. (1998) and Hanfer et al. (2001) found poor correlation between placental volume (measured by 3D U/S in the second trimester) and, the fetal size with poor prediction of IUGR. The present study was performed to obtain further information about the relationship between placental volume (measured by 3D U/S) and fetal growth and welfare with special interest to pre-ecalmptic cases between 36 and 38 weeks of pregnancy.
It was found that the mean age for cases with severe pre-eclampsia were significantly higher than both mild P.E. and control groups, this result goes in agreement with Davey (1995) who stated that pregnant women over 30 years whether primigravidae or multigravidae have increased incidence of pre-eclampsia and perinatal mortality. Gunningham and associates (1977) found that in cases of sever pre-eclampsia, fluid retention, maternal weight gain and body mass index may be extreme in those women and the possibility of fulminate pre-eclampsia or even eclampsia is high.
In the present study, means of maternal weight and BMI in severe and mild P.E. groups are increased with high statistical significance. In the present study patients with sever pre-eclampsia had the lowest placental weight, thickness and the smallest placental volume, also there is a significant positive correlation between placental volume and it’s weight or thickness. The larger the placental volume the higher are the placental weight and thickness. These results parallel with (Chase and Cayea, 1991), They stated that after 23 weeks the placenta should not be thinner than 0.5 cm or thicker than 1.5cm, a thin placenta may be due to IUGR, placental infarction and pregnancy with essential hypertention and pre-eclampsia. Sivaro et al. (2002) found positive correlation between placental volume and neonatal birth weight and babies length.
The present study proved the significant negative correlation between placental volume and percentage of IUGR (the smaller the placental volume the higher the incidence of IUGR, in addition to a significant positive correlation between placental volume and birth weight (the smaller the placental volume the lower the birth weight. This go in agreement with the recent study done by Hafner et al. (2003) who found significant positive correlation of 3D U/S placental volume measurements and poor fetal outcome in cases of pre-eclampsia.
From the present study, it was found that the 3D ultrasound measurement of placental volume is correlated with placental weight and thickness, fetal growth, B.P.P., birth weight and Apgar score. So, 3D ultrasound measurement of placental volume is recommended for predication of intra uterine growth retardation (IUGR) in pregnancy complicated by pre-eclampsia.
1. Acromite, M.T.; Mantzoros, C.S. Leach, R.E. et al. (1999) : Androgens in pre-eclampsia. Am. J. Obstet Gynecol., 180:60-63.
2. Bleker, O.P.; Kloosterman, G.J.; Breur, W.; Mieras, D.J. (1977) : The volumetric growth of the human placenta : a longitudinal ultrasonic study. Am. J. Obstet. Gynecol., 127:657-61.
3. Chase, L.M. and Cayea, P.D. (1991) : The placenta and umbilical cord. IN Berman, M.C. (ed). Diagnostic Medical Sonography. A Guide to Clinical Practice. 1st ed. Philadelphia, J.B. Lippincott Company, p. 301-330.
4. Cunningham, F.G.; Mac-Donald, P.O.; Gant, N.F. et al. (1977) : Hypertensive disorders of pregnancy. In : William’s obstetrics 20th edition. London : Prentice Hall. Int. Inc., pp. 693-744.
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7. Geirsson, R.T.; Ogston, S.A.; Patel, N.B.; Christie, A.D. (1985) : Growth of total intrauterine, intra-amniotic and placental volume in normal singleton pregnancy measured by ultrasound. Br. J. Obstet. Gynaecol. 92:46-53.
8. Hafner, E.; Metzenbuaer, M.; Hofinger, D.; Munkel, M.; Gassner, R. and Philipp, K. (2003) : Placental growth from the first to the second trimester of pregnancy in SGA-fetuses and pre-eclamptic pregnancies compared to normal fetuses. Placenta 24(4): 336-42.
9. Hafner, E.; Philipp, K.; Schuchter, K. and Bauer, P. (1998) : Second trimester measurement of placental volume by three dimensional ultrasound to predict small for gestation age infants. Ultrasound Obstet Gynecol 12(2): 97-102.
10. Hafner, E.; Schucher, K.; Van Leeuwen, M. and Philipp, K. (2001) : 3D sonographic volumetry of the placenta and fetus between weeks 15 and 17 of gestation. Ultrasound Obstet Gynecol 18(2) : 116-20.
11. Jurkovic, D.; Jauniaux, E. and Cobnpbell, S. (1994) : Three dimensional ultrasound in obstetrics and gynecology. In Kurjak, A. and Chervenak, F.A (eds.). The fetus as patient, pp. 135-40. (Carnlortl, U.K : The Parthenon Publishing Group).
12. Robson, S.C. (1999) : Hypertension and renal disease in pregnancy. In : Edmonds, D.K. (ed). Dewhurst’s Textbook of Obstetrics and Gynecology of Postgraduates. 6th edition, London : Blackwell Science, pp. 166-185.
13. Seligman, S.P.; Abramson, S.B.; Young, B.K.; Buyon, J.P. (1994) : The role of nitric oxide (NO) in the pathogenesis of pre-eclampsia. Am.J. Obstet. Gynecol., 170:240.
14. Sivaro, S.; Vidyadaran, M.K.; Jammal, A.B.; Zinab, S. and Ramesh, K.N. (2002) : Weight, volume and surface area of placenta of normal pregnant women and their relation to maternal and neonatal parameters in Malay, Chinese, and Indian ethnic group. Placenta 23 (8-9) : 691-6.
15. Theam, M.; Osmond, C.; Wilks, R.; Benett, F.I. and Forrester, T.E. (2001) : Second trimester placental volume and infant size at birth. Obstet Gynecol 98(2) : 279-83.
Prenat Diagn. 2003 Jan;23(1):16-20.: Triploidy in a twin pregnancy: small placenta volume as an early sonographical marker. Gassner R, Metzenbauer M, Hafner E, Vallazza U, Philipp K. Ludwig-Boltzmann-Institute for Clinical Obstetrics and Gynaecology, Department of Obstetrics and Gynaecology, Donauspital Vienna, Austria. [firstname.lastname@example.org]
Introduction: We report a case of a twin pregnancy with triploidy of maternal phenotype of one foetus and no chromosomal anomaly of the other twin and the role of sonographical placental volumetry.
Case: At 12 weeks of gestation, a dichorionic twin pregnancy discordant in growth is diagnosed. 3D ultrasound reveals a distinctly small placental volume of foetus II. Amniocentesis at 16 weeks discloses triploidy of this foetus. Sonography reveals asymmetrical foetal growth retardation, a severe heart defect and bilateral cleft lip and palate, typical findings in triploidy. Selective feticide at week 20+3 is followed by pre-term birth of foetus I at 27 weeks.
Conclusion: Small placental volume in addition to growth restriction of one foetus early in the course of a twin pregnancy could be an important early marker influencing the decision for chorionic villous sampling at 12 weeks instead of amniocentesis at 16 weeks and it could lead to an earlier selective pregnancy termination of a triploid twin. This would lower the risk of pre-term birth and enable a better outcome for the remaining healthy foetus.
Copyright 2002 John Wiley & Sons, Ltd.
PMID: 12533806 [PubMed - indexed for MEDLINE]
Z. Geburtshilfe Neonatol. 2002 Jul-Aug;206(4):138-41.: Associations between birth weight and placental volume in the first trimester [Article in German]. Metzenbauer M, Hafner E, Hoefinger D, Schuchter K, Philipp K. Ludwig-Boltzmann-Institut fur klinische Geburtshilfe und Gynakologie, Abteilung fur Geburtshilfe und Gynakologie, Donauspital am SMZ-Ost Wien, Germany. [email@example.com]
Introduction: Associations between the size of the placenta and birth weight have been described before. This connection has also been found in (sonographically estimated) second trimester placental size. The aim of this study was to find out if there are any differences in first trimester placental volume between various birth weight groups.
Methods: Placental volume was obtained from non-smoking women at the end of the first trimester during a period of eight months. After birth, the newborns were divided into four groups: below the 10th, 10th to 50th 50th to 90th and above the 90th centile. As is known from previous research, placenta size changes in proportion to crown-rump-length. Therefore, the medians of the "placenta quotients" (placental volume/CRL) of each group were compared in order to correct for differences in gestational age.
Results: Data from 1476 pregnancies could be evaluated. The overall median of the placenta quotient was 0.98. It was 0.85 in the group below the 10th, 0.92 between 10th and 50th, 1.02 between 50th and 90th and 1.10 above the 90th centile (p
Discussion: The finding of associations between early pregnancy placental size and birth weight at term gives hope for the development of new diagnostic methods for the recognition of placenta-associated problems. Further research is required to estimate the clinical possibilities for the detection of pregnancies at risk of severe growth retardation and other conditions.
PMID: 12198590 [PubMed - indexed for MEDLINE]
Ultrasound Obstet Gynecol. 2002 Mar;19(3):240-2.: First-trimester placental volume as a marker for chromosomal anomalies: preliminary results from an unselected population. Metzenbauer M, Hafner E, Schuchter K, Philipp K. Ludwig-Boltzmann Institute for Clinical Obstetrics and Gynaecology, Department of Obstetrics and Gynaecology, Donauspital Vienna, Vienna, Austria. [firstname.lastname@example.org]
Objective: To compare first-trimester placental volume in chromosomally abnormal and normal pregnancies.
Methods: Placental volumes were routinely recorded at the time of nuchal translucency thickness measurement at 10-13 weeks of gestation. This was done using customized three-dimensional ultrasound equipment and measurements were then converted to the placental quotient (placental volume/fetal crown-rump length). The possible difference in placental quotient between chromosomally normal and abnormal pregnancies was examined.
Results: A total of 2863 pregnancies was evaluated, including 17 with major chromosomal defects (nine cases of trisomy 21, four of trisomy 18, two of trisomy 13, and one each of Turner syndrome and 48,XXY + 21). The median placental quotient in the chromosomally abnormal group (0.67) was significantly lower than that in the normal fetuses (0.98). In nine of the 17 affected pregnancies the quotient was below the 10th centile of the normal range.
Conclusions: Assessment of placental volume may prove to be useful in first-trimester risk assessment for chromosomal anomalies.
PMID: 11896942 [PubMed - indexed for MEDLINE]
Ultrasound Obstet Gynecol. 2001 Dec;18(6):590-2.: Uterine artery Doppler and placental volume in the first trimester in the prediction of pregnancy complications.
Schuchter K, Metzenbauer M, Hafner E, Philipp K. Department of Obstetrics and Gynecology, Ludwig Boltzmann Institute of Clinical Obstetrics and Gynecology, Donauspital am SMZ-Ost, Danubehospital, Langobardenstrasse 122, 1120 Vienna, Austria. [email@example.com]
Objective: To evaluate placental volume and uterine artery Doppler in the first trimester in the prediction of pregnancies that subsequently develop pre-eclampsia, pregnancy-induced hypertension, preterm placental abruption or fetal growth restriction.
Methods: In 380 singleton pregnancies attending our center for nuchal translucency screening at 11-14 weeks of gestation, Doppler assessment of both uterine arteries was carried out for measurement of the pulsatility index and the mean pulsatility index of the two vessels was calculated. In addition, three-dimensional ultrasound was used to obtain images for subsequent measurement of placental volume. The 90th centile of the uterine artery mean pulsatility index and the 10th centile of the placental volume for crown-rump length (placental quotient) were calculated. These cut-offs were used for the prediction of pregnancy complications.
Results: Complications occurred in 36 (9.5%) of the 380 pregnancies, including 31 cases of fetal growth restriction, two of pregnancy-induced hypertension and abruption, two of pregnancy-induced hypertension, and one of abruption. The uterine artery mean pulsatility index was > or =90th centile in 38 (10%) pregnancies and this group contained nine (25%) of those that developed complications. The placental quotient was or =90th centile and the placental quotient was
Conclusion: The combination of placental volume measurement and uterine artery Doppler in the first trimester may identify women at risk for subsequent development of pregnancy complications.
PMID: 11844195 [PubMed - indexed for MEDLINE]
Placenta. 2001 Sep-Oct;22(8-9):729-34.: Correlation of first trimester placental volume and second trimester uterine artery Doppler flow. Hafner E, Metzenbauer M, Dillinger-Paller B, Hoefinger D, Schuchter K, Sommer-Wagner H, Philipp K. Ludwig Boltzman Institute for Clinical Obstetrics and Gynecology, Ob/Gyn Department, Donauspital am SMZ-Ost, Vienna, Austria. [firstname.lastname@example.org]
Uterine artery Doppler examination can identify impaired trophoblast invasion in the second trimester of pregnancy. High resistance and an early diastolic 'notch' show insufficient physiological conversion of the spiral arteries. Uterine artery Doppler is routinely performed between 22-24 weeks which is relatively late for treatment. In this study we wanted to find out whether women with increased uterine blood flow resistance at 22 weeks already have reduced placental volumes in the first trimester measured with 3D sonography.A total of 1060 women with singleton pregnancies had three dimensional (3D) volume measurements of their placentae between 11-13 weeks and uterine Doppler scans between 21-22 weeks. Stepwise logistic and linear regression analyses were used to show a correlation between placental volume (PV) and a CRL dependent placental quotient (PQ) with uterine perfusion parameters. Uterine perfusion at 21-22 weeks depends significantly on PV or PQ at 11-13 weeks (P
PMID: 11597193 [PubMed - indexed for MEDLINE]
Ultrasound Obstet Gynecol. 2001 Aug;18(2):116-20.: Three-dimensional sonographic volumetry of the placenta and the fetus between weeks 15 and 17 of gestation. Hafner E, Schuchter K, van Leeuwen M, Metzenbauer M, Dillinger-Paller B, Philipp K. Ludwig Boltzmann Institute for Clinical Obstetrics and Gynaecology, Department of Gynecology/Observation, Donauspital am SMZ-Ost, Langobardenstrasse 122, A-1220 Vienna, Austria. [email@example.com]
Objectives: Three-dimensional sonographic volume measurement enables for the first time direct comparison of the increase in size of different but closely interacting structures like the placenta and fetus. Our aim was to calculate the fetal and placental volumes between weeks 15 and 17 of gestation, to monitor the difference in the increase of the fetal and placental sizes and to determine their mutual relationship.
Methods: Fetal and placental sonographic volume measurements were made in 356 singleton pregnancies. To measure the relationship between fetal and placental volumes, a quotient was calculated. Regression analyses were performed to analyze the dependence of the fetal and placental volumes and placental quotient on the week of gestation and other influencing variables.
Results: The mean of the fetal volume increased markedly from 67.8 to 76.6 mL (by 13%) within the 3 weeks of observation, whereas placental volume increased only slightly (111.1 to 114 mL (by 2.6%)). The random variation of placental volumes around the mean in all three gestational weeks was considerably higher than that of fetal volumes, indicating that in this early period of gestation there is little correlation between fetal and placental sizes. Fetal volume correlated better to gestational week than did placental volume.
Conclusion: The quotient of fetal and placental volume might assist in the diagnosis of high-risk pregnancies and the assessment of a normal or large fetus with a small placenta.
PMID: 11529989 [PubMed - indexed for MEDLINE]
Placenta. 2001 Jul;22(6):602-5.: Three-dimensional ultrasound measurement of the placental volume in early pregnancy: method and correlation with biochemical placenta parameters. Metzenbauer M, Hafner E, Hoefinger D, Schuchter K, Stangl G, Ogris E, Philipp K. Ludwig-Boltzmann-Institute of Clinical Obstetrics and Gynaecology, Donauspital am SMZ-Ost, Langobardenstrasse 122, A-1220 Vienna, Austria. [firstname.lastname@example.org]
Placental size has been an interesting topic of research for many years. The main aim of this study was to investigate the feasibility of measuring the placental volume at the end of the first trimester using three-dimensional (3D) ultrasound and to correlate these volumes to known placental functional indices and to factors affecting the placenta. Women with singleton pregnancies at the end of the first trimester were included into this study. The volume data of the placentae were correlated to the crown-rump length (CRL), placenta-associated plasma protein A (PAPP-A), free beta-human chroangiogonadotropin (f-beta-hCG) and other factors that may affect the placental size or function. A total of 1462 pregnancies could be evaluated. Comparison between CRL and placental volume proved a significant correlation (r=0.43, P
PMID: 11440550 [PubMed - indexed for MEDLINE]