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Meta-Analysis
. 2019 May 14;5(5):CD012245.
doi: 10.1002/14651858.CD012245.pub2.

Biochemical tests of placental function versus ultrasound assessment of fetal size for stillbirth and small-for-gestational-age infants

Alexander Ep Heazell  1 , Dexter Jl Hayes, Melissa Whitworth, Yemisi Takwoingi, Susan E Bayliss, Clare Davenport
Affiliations
Meta-Analysis

Biochemical tests of placental function versus ultrasound assessment of fetal size for stillbirth and small-for-gestational-age infants

Alexander Ep Heazell et al. Cochrane Database Syst Rev. .

Abstract

Background: Stillbirth affects 2.6 million pregnancies worldwide each year. Whilst the majority of cases occur in low- and middle-income countries, stillbirth remains an important clinical issue for high-income countries (HICs) - with both the UK and the USA reporting rates above the mean for HICs. In HICs, the most frequently reported association with stillbirth is placental dysfunction. Placental dysfunction may be evident clinically as fetal growth restriction (FGR) and small-for-dates infants. It can be caused by placental abruption or hypertensive disorders of pregnancy and many other disorders and factorsPlacental abnormalities are noted in 11% to 65% of stillbirths. Identification of FGA is difficult in utero. Small-for-gestational age (SGA), as assessed after birth, is the most commonly used surrogate measure for this outcome. The degree of SGA is associated with the likelihood of FGR; 30% of infants with a birthweight < 10th centile are thought to be FGR, while 70% of infants with a birthweight < 3rd centile are thought to be FGR. Critically, SGA is the most significant antenatal risk factor for a stillborn infant. Correct identification of SGA infants is associated with a reduction in the perinatal mortality rate. However, currently used tests, such as measurement of symphysis-fundal height, have a low reported sensitivity and specificity for the identification of SGA infants.

Objectives: The primary objective was to assess and compare the diagnostic accuracy of ultrasound assessment of fetal growth by estimated fetal weight (EFW) and placental biomarkers alone and in any combination used after 24 weeks of pregnancy in the identification of placental dysfunction as evidenced by either stillbirth, or birth of a SGA infant. Secondary objectives were to investigate the effect of clinical and methodological factors on test performance.

Search methods: We developed full search strategies with no language or date restrictions. The following sources were searched: MEDLINE, MEDLINE In Process and Embase via Ovid, Cochrane (Wiley) CENTRAL, Science Citation Index (Web of Science), CINAHL (EBSCO) with search strategies adapted for each database as required; ISRCTN Registry, UK Clinical Trials Gateway, WHO International Clinical Trials Portal and ClinicalTrials.gov for ongoing studies; specialist abstract and conference proceeding resources (British Library's ZETOC and Web of Science Conference Proceedings Citation Index). Search last conducted in Ocober 2016.

Selection criteria: We included studies of pregnant women of any age with a gestation of at least 24 weeks if relevant outcomes of pregnancy (live birth/stillbirth; SGA infant) were assessed. Studies were included irrespective of whether pregnant women were deemed to be low or high risk for complications or were of mixed populations (low and high risk). Pregnancies complicated by fetal abnormalities and multi-fetal pregnancies were excluded as they have a higher risk of stillbirth from non-placental causes. With regard to biochemical tests, we included assays performed using any technique and at any threshold used to determine test positivity.

Data collection and analysis: We extracted the numbers of true positive, false positive, false negative, and true negative test results from each study. We assessed risk of bias and applicability using the QUADAS-2 tool. Meta-analyses were performed using the hierarchical summary ROC model to estimate and compare test accuracy.

Main results: We included 91 studies that evaluated seven tests - blood tests for human placental lactogen (hPL), oestriol, placental growth factor (PlGF) and uric acid, ultrasound EFW and placental grading and urinary oestriol - in a total of 175,426 pregnant women, in which 15,471 pregnancies ended in the birth of a small baby and 740 pregnancies which ended in stillbirth. The quality of included studies was variable with most domains at low risk of bias although 59% of studies were deemed to be of unclear risk of bias for the reference standard domain. Fifty-three per cent of studies were of high concern for applicability due to inclusion of only high- or low-risk women.Using all available data for SGA (86 studies; 159,490 pregnancies involving 15,471 SGA infants), there was evidence of a difference in accuracy (P < 0.0001) between the seven tests for detecting pregnancies that are SGA at birth. Ultrasound EFW was the most accurate test for detecting SGA at birth with a diagnostic odds ratio (DOR) of 21.3 (95% CI 13.1 to 34.6); hPL was the most accurate biochemical test with a DOR of 4.78 (95% CI 3.21 to 7.13). In a hypothetical cohort of 1000 pregnant women, at the median specificity of 0.88 and median prevalence of 19%, EFW, hPL, oestriol, urinary oestriol, uric acid, PlGF and placental grading will miss 50 (95% CI 32 to 68), 116 (97 to 133), 124 (108 to 137), 127 (95 to 152), 139 (118 to 154), 144 (118 to 161), and 144 (122 to 161) SGA infants, respectively. For the detection of pregnancies ending in stillbirth (21 studies; 100,687 pregnancies involving 740 stillbirths), in an indirect comparison of the four biochemical tests, PlGF was the most accurate test with a DOR of 49.2 (95% CI 12.7 to 191). In a hypothetical cohort of 1000 pregnant women, at the median specificity of 0.78 and median prevalence of 1.7%, PlGF, hPL, urinary oestriol and uric acid will miss 2 (95% CI 0 to 4), 4 (2 to 8), 6 (6 to 7) and 8 (3 to 13) stillbirths, respectively. No studies assessed the accuracy of ultrasound EFW for detection of pregnancy ending in stillbirth.

Authors' conclusions: Biochemical markers of placental dysfunction used alone have insufficient accuracy to identify pregnancies ending in SGA or stillbirth. Studies combining U and placental biomarkers are needed to determine whether this approach improves diagnostic accuracy over the use of ultrasound estimation of fetal size or biochemical markers of placental dysfunction used alone. Many of the studies included in this review were carried out between 1974 and 2016. Studies of placental substances were mostly carried out before 1991 and after 2013; earlier studies may not reflect developments in test technology.

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Conflict of interest statement

Susan Bayliss: none known.

Clare Davenport's employer (The University of Birmingham) received funding for her participation in this review as part of an NIHR clinical fellowship awarded to Alexander Heazell (the lead author and contact person).

Dexter Hayes: none known.

Yemisi Takwoingi's employer (The University of Birmingham) received funding for her participation in this review as part of an NIHR clinical fellowship awarded to Alexander Heazell (the lead author and contact person).

Melissa Whitworth was on the NICE guideline development group for Intrapartum Care in High Risk Pregnancy and travel to committee meetings was paid by NICE

Alexander Heazell has received research grants from Alere (UK) and Action Medical Research to investigate placental factors in maternal serum in women with reduced fetal movements. He is also a Supervisor for a Clinical Research Fellowship from Action Medical Research which incorporates projects to detect placental factors in maternal serum. In addition, he holds a Clinician Scientist Award from National Institute of Health Research (NIHR) (CS‐2013‐13‐009) and this review is part of that programme of work. The views expressed here are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health.

Figures

1
1
Current clinical pathway and three proposed uses of a placental function test. Currently, women are screened for a small‐for‐gestational age fetus (as a proxy for placental dysfunction) using symphysis‐fundal height and maternal awareness of fetal movements. Women deemed to be at increased risk are screened using ultrasound measurement of fetal biometry. We propose three different clinical pathways for placental function tests. Firstly, they could be used as an additional test when Doppler measurements are normal. They could be used in combination with currently used tests, and finally they could be used as a triage test to differentiate infants who are constitutionally small from those with placental dysfunction. Although treatment decisions would be tailored to individual cases, a positive test would be expected to lead to increased surveillance or intervention (planned delivery) and a negative test would lead to continuing with the pregnancy.
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PRISMA flow diagram for selection of studies.
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3
Risk of bias and applicability concerns graph: review authors' judgements about each domain presented as percentages across included studies. E3 = oestriol; EFW = estimated fetal weight; hPL = human placental lactogen; PlGF = placental growth factor. Each bar shows the number of studies in each category for a domain. The index test domain was evaluated separately for each test. Of the 91 included studies, 9 studies evaluated more than one test and so the numbers of studies shown for the 7 index test domains do not add up to 91 across tests.
4
4
Forest plot of structural tests for identifying small‐for‐gestational age (birthweight ≤tenth centile) infants. EFW = estimated fetal weight; FN = false negative; FP = false positive; SGA = small‐for‐gestational‐age; TN = true negative; TP = true positive. For each test, the forest plot shows the estimates of sensitivity and specificity from each study, the threshold used to define test positivity, risk of SGA pregnancy and whether there was an intervention that may have altered outcome. Studies are sorted by threshold, risk and intervention status.
5
5
Forest plot of biochemical tests for identifying small‐for‐gestational‐age (birthweight ≤tenth centile) infants. E3 = oestriol; FN = false negative; FP = false positive; hPL = human placental lactogen; PlGF = placental growth factor; SGA = small‐for‐gestational‐age; TN = true negative; TP = true positive; UA = uric acid. For each test, the forest plot shows the estimates of sensitivity and specificity from each study, the threshold used to define test positivity, risk of SGA pregnancy and whether there was an intervention that may have altered outcome. Studies are sorted by threshold, risk and intervention status.
6
6
Summary ROC plot of ultrasound estimated fetal weight (EFW) at a tenth centile threshold for identifying small‐for‐gestational‐age (birthweight ≤tenth centile) infants. The study points are shown using different symbols for the formulas used. The study points were scaled according to the precision of sensitivity and specificity in the studies. The solid circle (summary point) represents the summary estimate of sensitivity and specificity for all 25 studies, and is surrounded by a dotted line representing the 95% confidence region and a dashed line representing the 95% prediction region. The 95% prediction region is the region within which one is 95% certain the results of a new study will lie.
7
7
Summary ROC plot of placental grading for identifying small‐for‐gestational‐age (birthweight ≤tenth centile) infants. The study points are shown using different symbols for different risk groups. The study points were scaled according to the precision of sensitivity and specificity in the studies. The solid circle (summary point) represents the summary estimate of sensitivity and specificity for all 12 studies, and is surrounded by a dotted line representing the 95% confidence region and a dashed line representing the 95% prediction region. The 95% prediction region is the region within which one is 95% certain the results of a new study will lie.
8
8
Summary ROC plot of human placental lactogen (hPL) for identifying small‐for‐gestational‐age (birthweight ≤tenth centile) infants. The study points are shown using different symbols for different risk groups. The study points were scaled according to the precision of sensitivity and specificity in the studies. The solid circle (summary point) represents the summary estimate of sensitivity and specificity for all nine studies, and is surrounded by a dotted line representing the 95% confidence region and a dashed line representing the 95% prediction region. The 95% prediction region is the region within which one is 95% certain the results of a new study will lie.
9
9
Summary ROC plot of structural and biochemical tests for identifying small‐for‐gestational‐age (birthweight ≤tenth centile) infants. E3 = oestriol; EFW = estimated fetal weight; hPL = human placental lactogen; PlGF = placental growth factor; SGA = small‐for‐gestational‐age; UA =uric acid. The curve for each test is drawn within the range of estimates of specificity from the studies included for the test. Compared to the other curves, the curve for EFW lies closest to the top left hand corner (ideal position where sensitivity and specificity both equal 1). The position of the curves for UA and placental grading is very similar. The SROC curve for UA is the green curve lying above the pink curve for placental grading.
10
10
Summary ROC plot of direct comparisons of human placental lactogen and oestriol for identifying small‐for‐gestational‐age (birthweight ≤tenth centile) infants. E3 = oestriol; hPL = human placental lactogen; SGA = small‐for‐gestational‐age. Each symbol represents the pair of sensitivity and specificity for one test from a study. The pair of points for the two tests from a study are connected by a dotted line. The size of each symbol was scaled according to the precision of sensitivity and specificity in the study. Each summary curve was restricted to the range of specificities for each test from the five studies that evaluated both tests in the same patients.
11
11
Forest plot of ultrasound estimated fetal weight (EFW) and placental growth factor (PlGF) for identifying small‐for‐gestational age (birthweight <third centile) infants. FN = false negative; FP = false positive; SGA3 = small‐for‐gestational‐age birthweight <third centile; TN = true negative; TP = true positive. For each test, the forest plot shows the estimates of sensitivity and specificity from each study, the threshold used to define test positivity, risk of SGA pregnancy and whether there was an intervention that may have altered outcome. Studies are sorted by threshold, risk and intervention status.
12
12
Forest plot of structural and biochemical tests for predicting stillbirth. E3 = oestriol; FN = false negative; FP = false positive; hPL = human placental lactogen; PlGF = placental growth factor; TN = true negative; TP = true positive; UA = uric acid. For each test, the forest plot shows the estimates of sensitivity and specificity from each study, the threshold used to define test positivity, risk of stillbirth and whether there was an intervention that may have altered outcome. Studies are sorted by threshold, risk and intervention.
13
13
Summary ROC plot of biochemical tests for predicting stillbirth. E3 = Oestriol; hPL = human placental lactogen; PlGF = placental growth factor; SGA = small‐for‐gestational‐age; UA =uric acid. The SROC curves for the four tests are parallel. The curve for each test is drawn within the range of estimates of specificity from the studies included for the test. Compared to the other curves, the curve for PlGF lies closest to the top left hand corner (ideal position where sensitivity and specificity both equal 1).
14
14
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of human placental lactogen (hPL)
15
15
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of placental grading.
16
16
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of serum oestriol (E3).
17
17
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of estimated fetal weight (EFW).
18
18
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of placental growth factor (PlGF).
19
19
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of uric acid.
20
20
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study of urinary oestriol (UE3).
21
21
Forest plot of studies with evaluations of both small‐for‐gestational‐age (SGA birthweight ≤tenth centile) infants and stillbirth. E3 = oestriol; hPL = human placental lactogen; PlGF = placental growth factor; UA = uric acid. Two studies (Altmann 1978; Chen 2012) evaluated placental grading for both SGA and stillbirth but not possible to include them on the plot. Studies are sorted by test and study identifier.
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Miller 1988 {published data only}
    1. Miller JM Jr, Brown HL, Kissling GA, Gabert HA. The relationship of placental grade to fetal size and growth at term. American Journal of Perinatology 1988;5:19‐21. - PubMed
Molvarec 2013 {published data only}
    1. Molvarec A, Gullai N, Stenczer B, Fugedi G, Nagy B, Rigo J. Comparison of placental growth factor and fetal flow Doppler ultrasonography to identify fetal adverse outcomes in women with hypertensive disorders of pregnancy: an observational study. BMC Pregnancy and Childbirth 2013;13:161. - PMC - PubMed
Montan 1986 {published data only}
    1. Montan S, Jorgensen C, Svalenius E, Ingemarsson I. Placental grading with ultrasound in hypertensive and normotensive pregnancies. A prospective, consecutive study. Acta Obstetrica et Gynecologica Scandinavica 1986; Vol. 65:477‐80. - PubMed
Nice 2016 {published and unpublished data}
    1. Nice D, Hayden K, Higgins L, Garrod A, Johnstone E, Heazell A. Human placental lactogen and placental growth factor differentiate adverse pregnancy outcome from healthy outcomes in high‐risk pregnancies. BJOG: an international journal of obstetrics and gynaecology 2016;123:44‐5.
Nielsen 1985 {published data only}
    1. Nielsen PV, Schultz‐Larsen P, Schioeler V. Screening in pregnancy with unconjugated estriol compared with total estriol. Acta Obstetricia et Gynecologica Scandinavica 1985;64:297‐301. - PubMed
Nisbet 1982 {published data only}
    1. Nisbet AD, Horne CH, Jandial V, Bremner RD, Cruickshank N, Sutcliffe RG. Measurement of plasma placental proteins and estriol in the detection of intrauterine growth retardation. European Journal of Obstetrics, Gynecology, & Reproductive Biology 1982;13:333‐42. - PubMed
Oats 1979 {published data only}
    1. Oats JJ, Beischer NA. The recurrence rate and significance of low oestriol excretion in successive pregnancies. British Journal of Obstetrics and Gynaecology 1979;86:15‐8. - PubMed
Obiekwe 1983 {published data only}
    1. Obiekwe BC, Chard T. A comparative study of the clinical use of four placental proteins in the third trimester. Journal of Perinatal Medicine 1983;11:121‐6. - PubMed
Odendaal 1981 {published data only}
    1. Odendaal HJ, Malan C, Oosthuizen J. Hormonal placental functions and intrauterine growth retardation in patients with positive contraction stress tests. South African Medical Journal 1981;59:822‐4. - PubMed
Odendaal 1997 {published data only}
    1. Odenaal HJ, Pienaar ME. Are high uric acid levels in patients with early preeclampsia an indication for delivery?. South African Medical Journal 1997;87:213‐8. - PubMed
Ott 1984 {published data only}
    1. Ott WJ, Doyle S. Ultrasonic diagnosis of altered fetal growth by use of a normal ultrasonic fetal weight curve. Obstetrics & Gynecology 1984;63:201‐4. - PubMed
Palo 1987 {published data only}
    1. Palo P, Erkkola R, Irjala K, Taina E. Serum free estriol inefficient in the detection of intrauterine growth retardation. Annales Chirurgiae et Gynaecologiae 1987;Suppl 202:20‐2. - PubMed
Palo 1989 {published data only}
    1. Palo P, Erkkola R, Piiroinen O, Ruotsalainen P. Accuracy of ultrasonic fetal weight estimation and detection of small for gestational age fetuses. American Journal of Perinatology 1989; Vol. 6:400‐4. - PubMed
Patterson 1983 {published data only}
    1. Patterson RM, Hayashi RH, Cavazos D. Ultrasonographically observed early placental maturation and perinatal outcome. American Journal of Obstetrics and Gynecology 1983;147:773‐7. - PubMed
Redman 1976 {published data only}
    1. Redman CW, Beckin LJ, Bonnar J, Wilkinson RH. Plasma urate measurements in predicting fetal death in hypertensive pregnancy. Lancet 1976;307:1370‐3. - PubMed
Roma 2015 {published data only}
    1. Roma E, Arnau A, Berdala R, Bergos C, Montesinos J, Figueras F. Ultrasound screening for fetal growth restriction at 36 vs 32weeks' gestation: a randomized trial (ROUTE). Ultrasound in Obstetrics & Gynecology 2015;46:391‐7. - PubMed
Sagen 1984 {published data only}
    1. Sagen N, Nilsen ST, Kim HC, Koller O, Bergsjo P. The predictive value of total estriol; HPL and Hb on perinatal outcome in severe pre‐eclampsia. Acta Obstetricia et Gynecologica Scandinavica 1984; Vol. 63:603‐8. - PubMed
Sekar 2016 {published data only}
    1. Sekar R, Khatun M, Barrett HL, Duncombe G. A prospective pilot study in assessing the accuracy of ultrasound estimated fetal weight prior to delivery. Australian & New Zealand Journal of Obstetrics & Gynaecology 2016;56:49‐53. - PubMed
Shawkat 2015 {published and unpublished data}
    1. Shawkat E, Johnstone E, Nice D, Sayce A, Hayden K, Myers J. [105‐POS] : Clinical evaluation of placental growth factor (PlGF) for the management of suspected placental pathology in high‐risk pregnancies. Pregnancy Hypertension 2015;5:57.
Siebert 1974 {published data only}
    1. Siebert W, Meitinger C, Vogt W, Sandel P. [HPL serum levels in intrauterine retardation of fetal growth during late pregnancy (author's transl)]. Geburtshilfe und Frauenheilkunde 1974;34:520‐4. - PubMed
Skovron 1991 {published data only}
    1. Skovron ML, Berkowitz GS, Lapinski RH, Kim JM, Chitkara U. Evaluation of early third‐trimester ultrasound screening for intrauterine growth retardation. Journal of Ultrasound in Medicine 1991;10:153‐9. - PubMed
Sovio 2015 {published data only}
    1. Sovio U, Smith G, Dacey A, Pasupathy D, White I. Screening for fetal growth restriction (FGR) using universal third trimester ultrasonography: A prospective cohort study of 3,977 nulliparous women. American Journal of Obstetrics and Gynecology 2015;1:S92. - PMC - PubMed
Spernol 1989 {published data only}
    1. Spernol R, Hecher K, Szalay S. [The value of fetal blood flow measurements in intrauterine growth retardation in comparison with E3 and human placental lactogen determinations]. Geburtshilfe und Frauenheilkunde 1989;49:463‐5. - PubMed
Steiner 1991 {published data only}
    1. Steiner H, Schaffer H, Lassmann R, Staudach A, Batka M. [Comparison of biochemical and Doppler sonographic monitoring of high‐risk pregnancies]. Geburtshilfe und Frauenheilkunde 1991;51:540‐3. - PubMed
Takeuchi 1985 {published data only}
    1. Takeuchi K. [Antenatal assessment of intrauterine growth retardation by ultrasonic fetal biometry and non‐stress fetal heart rate testing]. Nippon Sanka Fujinka Gakkai Zasshi ‐ Acta Obstetrica et Gynaecologica Japonica 1985;37:2376‐84. - PubMed
Trudinger 1979 {published data only}
    1. Trudinger BJ, Gordon YB, Grudzinskas JG, Hull MG, Lewis PJ, Arrans ME. Fetal breathing movements and other tests of fetal wellbeing: a comparative evaluation. British Medical Journal 1979;2:577‐9. - PMC - PubMed
Turitz 2014 {published data only}
    1. Turitz AL. Isolated abdominal circumference<5% or estimated fetal weight 10 to 19% as predictors of small for gestational age infants. American Journal of Perinatology 2014; Vol. 31:469‐76. - PubMed
Valino 2016 {published data only}
    1. Valino N, Giunta G, Gallo DM, Akolekar R, Nicolaides KH. Biophysical and biochemical markers at 35‐37 weeks' gestation in the prediction of adverse perinatal outcome. Ultrasound in Obstetrics & Gynecology 2016;47:203‐9. - PubMed
Voto 1988 {published data only}
    1. Voto LS, Ilia R, Darbon‐Grosso A, Uranga Imaz F, Marguiles M. Uric acid levels: a useful index of the severity of preeclampsia and perinatal prognosis. Journal of Perinatal Medicine 1988;16:123‐6. - PubMed
Walker 2010 {published data only}
    1. Walker GM, Hindmarsh, PC, Geary M, Kingdom JC. Sonographic maturation of the placenta at 30 to 34 weeks is not associated with second trimester markers of placental insufficiency in low‐risk pregnancies. Journal of Obstetrics and Gynaecology Canada 2010;32(12):1134‐9. - PubMed
Weerasinghe 1977 {published data only}
    1. Weerasinghe DS, Legge M, Aickin DR. The clinical significance of low urine oestriol values. New Zealand Medical Journal 1977;86:383‐4. - PubMed
Weiner 2016 {published data only}
    1. Weiner E, Fainstein N, Mizrachi Y, Elyashiv O, Mevorach‐Zussman N, Bar J, et al. Comparison between three methods for the detection of macrosomia and growth restriction in patients presenting in active labor‐a prospective study. American Journal of Obstetrics and Gynecology 2016;1:S225‐6.
Westergaard 1984 {published data only}
    1. Westergaard JG, Teisner B, Hau J, Grudzinskas JG. Placental protein measurements in complicated pregnancies. I. Intrauterine growth retardation. British Journal of Obstetrics and Gynaecology 1984;91:1216‐23. - PubMed
Williams 2002 {published data only}
    1. Williams KP, Galerneau F. The role of serum uric acid as a prognostic indicator of the severity of maternal and fetal complications in hypertensive pregnancies. Journal of Obstetrics & Gynaecology Canada: JOGC 2002;24:628‐32. - PubMed
Yassaee 2003 {published data only}
    1. Yassaee F. Hyperuricaemia and perinatal outcomes in patients with severe preeclampsia. Iranian Journal of Medical Sciences 2003;28(4):198‐9.
Ylikorkala 1973 {published data only}
    1. Ylikorkala O. Maternal serum HPL levels in normal and complicated pregnancy as an index of placental function. Acta Obstetricia et Gynecologica Scandinavica ‐ Supplement 1973;26:1‐52. - PubMed
Zhang 1990 {published data only}
    1. Zhang WY. [Single radial immunodiffusion of human placental lactogen and its clinical uses]. Chung‐Hua Fu Chan Ko Tsa Chih [Chinese Journal of Obstetrics & Gynecology] 1990;25:278‐81, 316. - PubMed

References to studies excluded from this review

Adekanle 2013 {published data only}
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Agboola 1978 {published data only}
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Aggarwal 2006 {published data only}
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Agorastos 2014 {published data only}
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Ahmad 1979 {published data only}
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Aickin 1983 {published data only}
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Alahakoon 2014 {published data only}
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Alberry 2009 {published data only}
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Alvarez‐Fernandez 2014 {published data only}
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Anderson 1978 {published data only}
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Arabin 1995 {published data only}
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Arias 1977 {published data only}
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Ariyuki 1995 {published data only}
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Atzeni 2012 {published data only}
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Aviram 2015 {published data only}
    1. Aviram A, Yogev Y, Bardin R, Meizner I, Wiznitzer A, Hadar E. Small for gestational age newborns ‐ Does pre‐recognition make a difference in pregnancy outcome?. Journal of Maternal‐fetal & Neonatal Medicine 2015;28:1520‐4. - PubMed
Axelsson 1978 {published data only}
    1. Axelsson O, Nilsson BA, Johansson ED. Assessment of placental function in uncomplicated and complicated late pregnancy by estimation of unconjugated oestrogens in plasma after an intravenous injection of dehydroepiandrosterone sulphate. Acta Endocrinologica 1978;89:359‐71. - PubMed
Baeza Valenzuela1995 {published data only}
    1. Baeza Valenzuela A, Garcia Mendez A. Premature aging of the placenta. Ultrasonic diagnosis. [Spanish]. Ginecologia y Obstetricia de Mexico 1995;63:287‐92. - PubMed
Bahado‐Singh 1998 {published data only}
    1. Bahado‐Singh RO, Dashe J, Deren O, Daftary G, Copel JA, Ehrenkranz RA. Prenatal prediction of neonatal outcome in the extremely low‐birth‐weight infant. American Journal of Obstetrics and Gynecology 1998;178:462‐8. - PubMed
Bainbridge 2008 {published data only}
    1. Bainbridge SA, Roberts JM. Uric acid as a pathogenic factor in preeclampsia. Placenta 2008;29 Suppl A:S67‐S72. - PMC - PubMed
Bakketeig 1984 {published data only}
    1. Bakketeig LS, Eik‐Nes SH, Jacobsen G. Randomised controlled trial of ultrasonographic screening in pregnancy. Lancet 1984;2:207‐11. - PubMed
Baltajian 2016 {published data only}
    1. Baltajian K, Bajracharya S, Salahuddin S, Berg AH, Geahchan C, Wenger JB, et al. Sequential plasma angiogenic factors levels in women with suspected preeclampsia. American Journal of Obstetrics & Gynecology 2016;215:89.e1‐89.e10. - PubMed
Barden 1999 {published data only}
    1. Barden AE, Beilin LJ, Ritchie J, Walters BN, Graham D, Michael CA. Is proteinuric pre‐eclampsia a different disease in primigravida and multigravida?. Clinical Science 1999;97:475‐83. - PubMed
Bardien 2016 {published data only}
    1. Bardien N, Whitehead CL, Tong S, Ugoni A, McDonald S, Walker SP. Placental insufficiency in fetuses that slow in growth but are born appropriate for gestational age: a prospective longitudinal study. PLOS One 2016;11:e0142788. - PMC - PubMed
Baron 1996 {published data only}
    1. Baron F, Graham D. Age‐independent assessment of abnormal fetal growth in the third trimester. Journal of Ultrasound in Medicine 1996;15:381‐4. - PubMed
Barrilleaux 2007 {published data only}
    1. Barrilleaux PS, Magann EF, Chauhan SP, York BM, Philibert L, Lewis DF. Amniotic fluid index as a predictor of adverse perinatal outcome in the HELLP syndrome. Journal of Reproductive Medicine 2007;52:293‐8. - PubMed
Bartha 2003 {published data only}
    1. Bartha JL, Romero‐Carmona R, Escobar‐Llompart M, Paloma‐Castro O, Comino‐Delgado R. Human chorionic gonadotropin and vascular endothelial growth factor in normal and complicated pregnancies. Obstetrics and Gynecology 2003;102:995‐9. - PubMed
Bashir 1982 {published data only}
    1. Bashir T, Brash JH, Buchan PC, Bevis DC, Clayden AD. Screening for the small‐for‐dates: a clinical and biochemical appraisal. European Journal of Obstetrics, Gynecology, & Reproductive Biology 1982;13:61‐6. - PubMed
Bastek 2009 {published data only}
    1. Bastek JA, Parr E, Wang E, Elovitz MA, Srinivas SK. Limitations of ultrasound in diagnosing intrauterine growth restriction in severe preeclampsia. Journal of Maternal‐fetal & Neonatal Medicine 2009;22:1039‐44. - PubMed
Battaglia 1995 {published data only}
    1. Battaglia C, Artini PG, Ballestri M, Bonucchi D, Galli PA, Bencini S, et al. Hemodynamic, hematological and hemorrheological evaluation of post‐term pregnancy. Acta Obstetricia et Gynecologica Scandinavica 1995;74:336‐40. - PubMed
Beischer 1975 {published data only}
    1. Beischer NA. Low oestriol excretion: incidence, significance and treatment in an obstetric population. Medical Journal of Australia 1975;2:379‐81. - PubMed
Bell 1967 {published data only}
    1. Bell ET, Loraine JA, McEwan HP, Charles D. Serial hormone assays in patients with uteroplacental insufficiency. American Journal of Obstetrics and Gynecology 1967;97:562‐70. - PubMed
Benton 2010 {published data only}
    1. Benton S, Hu Y, Fang X, Knudsen AB, Kronborg CS, Vittinghus E, et al. Placental growth factor as a diagnostic for early onset pre‐eclampsia and normotensive intrauterine growth restriction of placental origin. Placenta 2010; Vol. 1:S24.
Benton 2011 {published data only}
    1. Benton S, Hu Y, Xie F, Kupfer K, Lee SW, Magee L, et al. Can placental growth factor identify placental intra‐uterine growth restriction in fetuses who are antenatally identified as being small for gestational age?. Placenta 2011;32(9):A100.
Benton 2011a {published data only}
    1. Benton S, Hu Y, Xie F, Kupfer K, Lee SW, Magee L, et al. Placental growth factor quantified on rapid assay as a diagnostic test for early‐onset pre‐eclampsia. Placenta 2011;32(9):A84.
Benton 2012 {published data only}
    1. Benton S, Knudsen U, Hu Y, Vittinghus E, Allen J, Konborg C, et al. Angiogenic factor imbalance is not specific to the maternal syndrome of pre‐eclampsia. Reproductive Sciences 2012;1:317A‐8A.
Benton 2012a {published data only}
    1. Benton SJ, Hu X, Xie F, Kupfer K, Lee SW, Magee LA, et al. Can placental growth factor in maternal circulation identify fetuses with placental intrauterine growth restriction?. American Journal of Obstetrics and Gynecology 2012;206(2):163. - PubMed
Benton 2014 {published data only}
    1. Benton S, Hu Y, Magee L, Dadelszen P. Angiogenic factors and the prediction of complications in a high‐risk pregnancy cohort. Reproductive Sciences 2014;1:186A‐187A.
Benton 2014a {published data only}
    1. Benton S, Yockell‐Lelievre J, Grynspan D, Magee L, Hu Y, Gruslin A, et al. Low maternal placental growth factor is associated with abnormal placental morphology in fetuses with suspected intrauterine growth restriction. Placenta 2014;35(9):A44.
Benz 1980 {published data only}
    1. Benz J, Ingold W, Landolt A, Keller PJ. [Hormonal diagnosis in fetal intrauterine retardation]. Gynakologische Rundschau 1980;20 Suppl 1:74‐6. - PubMed
Berendtsen 1985 {published data only}
    1. Berendtsen H, Klunder KB, Norskov O. Biparietal measurements, human placental‐lactogenic hormone and oestriol in assessment of foetal condition. Ugeskrift for Laeger 1985; Vol. 147, issue 38:2984‐6. - PubMed
Bergsjo 1973 {published data only}
    1. Bergsjo P, Bakke T, Salamonsen LA, Stoa KF, Thorsen T. Urinary oestriol in pregnancy, daily fluctuation, and correlation with fetal growth. Journal of Obstetrics & Gynaecology of the British Commonwealth 1973;80:305‐10. - PubMed
Berle 1973 {published data only}
    1. Berle P. [Value of hormone analysis for the assessment of placenta function in late pregnancy]. Deutsche Medizinische Wochenschrift 1973;98:2146‐50. - PubMed
Berle 1973a {published data only}
    1. Berle P. Maternal serum levels of human placental lactogen in placental insufficiency. Geburtshilfe und Frauenheilkunde 1973; Vol. 33, issue 6:455‐9. - PubMed
Berle 1973b {published data only}
    1. Berle P, Leyen H, Rossler H. [Proceedings: Diagnosis of placenta insufficiency by determination of placental lactogen in maternal blood]. Archiv fur Gynakologie 1973;214:213‐5. - PubMed
Berle 1975 {published data only}
    1. Berle P, Haselmayer B, Plambeck H. [Comparative studies on CTG and hormonal parameters in the diagnosis of placenta insufficiency]. Archiv fur Gynakologie 1975;219:426‐8. - PubMed
Bernardes 2013 {published data only}
    1. Bernardes LS, Francisco RP, Dourado RM, Doro GF, Zugaib M. Ultrasound evaluation of the placenta in fetuses of IUGR. Placenta 2013;34:A92.
Bernatavicius 2013 {published data only}
    1. Bernatavicius G, Roberts S, Garrod A, Whitworth MK, Johnstone ED, Gillham JC, et al. A feasibility study for a randomised controlled trial of management of reduced fetal movements after 36 weeks gestation. Archives of Disease in Childhood: Fetal and Neonatal Edition 2013;98:35. - PMC - PubMed
Bersinger 2004 {published data only}
    1. Bersinger NA, Odegard RA. Second‐ and third‐trimester serum levels of placental proteins in preeclampsia and small‐for‐gestational age pregnancies. Acta Obstetricia et Gynecologica Scandinavica 2004;83:37‐45. - PubMed
Bersinger 2005 {published data only}
    1. Bersinger NA, Odegard RA. Serum levels of macrophage colony stimulating, vascular endothelial, and placenta growth factor in relation to later clinical onset of pre‐eclampsia and a small‐for‐gestational age birth. American Journal of Reproductive Immunology 2005;54:77‐83. - PubMed
Bhansali 1975 {published data only}
    1. Bhansali KG. Placental function tests by blood analysis. Journal of the National Medical Association 1975;67:137‐9. - PMC - PubMed
Bian 1992 {published data only}
    1. Bian XM. [Choice of ultrasound fetal weight estimation formulae]. Chung‐Hua i Hsueh Tsa Chih [Chinese Medical Journal] 1992;72:677‐9, 703. - PubMed
Biberoglu 2016 {published data only}
    1. Biberoglu E, Kirbas A, Daglar K, Biberoglu K, Timur H, Demirtas C, et al. Serum angiogenic profile in abnormal placentation. Journal of Maternal‐Fetal & Neonatal Medicine 2016;29:3193‐7. - PubMed
Bieglmayer 1981 {published data only}
    1. Bieglmayer C, Spona J. [Monitoring of at‐risk pregnancies through E3 and HPL]. Acta Universitatis Palackianae Olomucensis Facultatis Medicae 1981;101:38‐42. - PubMed
Bila 1980 {published data only}
    1. Bila S, Sulovic V, Genbacev O. [Human placental lactogen in the blood in fetal growth retardation]. Srpski Arhiv Za Celokupno Lekarstvo 1980;108:317‐24. - PubMed
Bitzer 1985 {published data only}
    1. Bitzer J, Hendry M, Richter R. [Detection of intrauterine growth retardation within the scope of routine prenatal care]. Geburtshilfe und Frauenheilkunde 1985; Vol. 45, issue 2:79‐82. - PubMed
Blaskova 1977 {published data only}
    1. Blaskova O, Sasko A, Pont'uch A, Chabada J. The value of estriol determination, and cytologic, ultrasound, and amnioscopic investigation in high‐risk pregnancy with a view to placental insufficiency (author's transl). [Slovak]. Ceskoslovenska Gynekologie 1977;42:411‐4. - PubMed
Bligh 2015 {published data only}
    1. Bligh L, Al Solai A, Greer RM, Kumar S. Intrapartum fetal compromise is associated with lower maternal placental growth factor (PlGF) levels at term. BJOG: an international journal of obstetrics and gynaecology 2015;122:162‐3.
Blitz 2016 {published data only}
    1. Blitz MJ, Rochelson B, Vohra N. Maternal serum analyses as predictors of fetal growth restriction with different degrees of placental vascular dysfunction. Clinics in Laboratory Medicine 2016;36:353‐67. - PubMed
Blumenfeld 2007 {published data only}
    1. Blumenfeld Y, Lee H, Pullen K, Wong A, Pettit K, Taslimi M. Ultrasound accuracy of estimated fetal weight in pregnancies complicated by intra‐uterine growth restriction. American Journal of Obstetrics and Gynecology 2007;197:S59.
Bobrow 2002 {published data only}
    1. Bobrow CS, Holmes RP, Muttukrishna S, Mohan A, Groome N, Murphy DJ, et al. Maternal serum activin A, inhibin A, and follistatin in pregnancies with appropriately grown and small‐for‐gestational‐age fetuses classified by umbilical artery Doppler ultrasound. American Journal of Obstetrics and Gynecology 2002;186:283‐7. - PubMed
Bock 1976 {published data only}
    1. Bock JE, Gaede P, Trolle D. Human placental lactogen hormone in serum from pregnant women with rhesus (anti‐D) isoimmunization. Acta Obstetricia et Gynecologica Scandinavica ‐ Supplement 1976; Vol. 53:14‐9. - PubMed
Boij 2012 {published data only}
    1. Boij R, Svensson J, Nilsson‐Ekdahl K, Sandholm K, Lindahl TL, Palonek E, et al. Biomarkers of coagulation, inflammation, and angiogenesis are independently associated with preeclampsia. American Journal of Reproductive Immunology 2012;68:258‐70. - PubMed
Borges 2005 {published data only}
    1. Borges MH, Zamudio S, Pullockaran J, Belliappa S, Albieri A, Catalano PM, et al. Fetal circulating growth factors in diabetic and normal pregnancy: relationship to placental and fetal growth. Journal of the Society for Gynecologic Investigation 2005; Vol. 12:299A.
Botasheva 2016 {published data only}
    1. Botasheva TL, Linde VA, Ermolova NV, Palieva NV, Sargsyan OD, Barinova VV. Peculiarities of angiogenic factors and cytokines in the physiological and complicated pregnancy, depending on the sex of the fetus. Journal of Maternal‐Fetal and Neonatal Medicine 2016;29:134.
Boucoiran 2012 {published data only}
    1. Boucoiran I, Thissier‐Levy S, Wu Y, Wei SQ, Zhong‐Cheng L, Delvin E, et al. Risk for preeclampsia and intrauterine growth restriction: Effective value of PlGF, Sflt‐1 and Inhibin A in singleton and multiple pregnancies. American Journal of Obstetrics and Gynecology 2012;1:S336‐7.
Branconi 1981 {published data only}
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Brush 1970 {published data only}
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Clelia 2013 {published data only}
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Rocca 1995 {published data only}
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Romero 2008 {published data only}
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Ronin‐Walknowska 1984 {published data only}
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Rosendahl 1988 {published data only}
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Rosendahl 1991 {published data only}
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Ruozi Berretta 1967 {published data only}
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Sabbagha 1979 {published data only}
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Salahuddin 2016 {published data only}
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Salas 1993 {published data only}
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Salas 1998 {published data only}
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Salkie 1977 {published data only}
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Samanta 1989 {published data only}
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Sarandakou 1989 {published data only}
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Sato 1974 {published data only}
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Secher 1986 {published data only}
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Secher 1987 {published data only}
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Selbing 1984 {published data only}
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Shaarawy 2001 {published data only}
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Shah 1996 {published data only}
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Sharf 1984 {published data only}
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Singer 1970 {published data only}
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Smith 2014 {published data only}
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Smith‐Bindman 2002 {published data only}
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Smith‐Bindman 2003 {published data only}
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Soler 1975 {published data only}
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Sood 1988 {published data only}
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Sorensen 2000 {published data only}
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Souka 2012 {published data only}
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Sovio 2014 {published data only}
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Spellacy 1967 {published data only}
    1. Spellacy WN, Cohen WD, Carlson KL. Human placental lactogen levels as a measure of placental function. American Journal of Obstetrics and Gynecology 1967;97:560‐1. - PubMed
Spellacy 1975 {published data only}
    1. Spellacy WN, Buhi WC, Birk SA. The effectiveness of human placental lactogen measurements as an adjunct in decreasing perinatal deaths. Results of a retrospective and a randomized controlled prospective study. American Journal of Obstetrics and Gynecology 1975; Vol. 121, issue 6:835‐44. - PubMed
Spellacy 1976 {published data only}
    1. Spellacy WN, Buhi WC, Birk SA. Human placental lactogen and intrauterine growth retardation. Obstetrics and Gynecology 1976;47:446‐8. - PubMed
Spona 1971 {published data only}
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Spona 1972 {published data only}
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Stefanelli 2014 {published data only}
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Stefanidis 1998 {published data only}
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Strizhakov 2013 {published data only}
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Strom 1983 {published data only}
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Sucak 2010 {published data only}
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Sudik 1982 {published data only}
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Sundrani 2013 {published data only}
    1. Sundrani D, Khot V, Pisal H, Mehendale S, Wagh G, Joshi A, et al. Gestation dependant changes in angiogenic factors and their associations with fetal growth measures in normotensive pregnancy. PLOS One 2013;8:e54153. - PMC - PubMed
Tajik 2012 {published data only}
    1. Tajik P, Boers K, Wyk L, Mol B, Sicco S. Evaluation of markers guiding management decision for intrauterine growth restriction: A sub‐analysis of a randomized trial, DIGITAT. American Journal of Obstetrics and Gynecology 2012, issue 1:S199‐S200.
Takeuchi 1988 {published data only}
    1. Takeuchi M, Morikawa H, Ueda Y, Mochizuki M. [Studies on the roles of insulin‐like growth factor‐1 (IGF‐1)/somatomedin C (SMC) during pregnancy]. Nippon Naibunpi Gakkai Zasshi ‐ Folia Endocrinologica Japonica 1988;64:489‐505. - PubMed
Tammemae 2016 {published data only}
    1. Tammemae L, Angerjas T, Szirko F. 5 Years of ERT‐quality assurance in East‐Tallinn Central Hospital, SGA. Journal of Maternal‐Fetal and Neonatal Medicine 2016;29:306‐7.
Tayama 1983 {published data only}
    1. Tayama C, Ichimaru S, Ito M, Nakayana M, Maeyama M, Miyakawa I. Unconjugated estradiol, estriol and total estriol in maternal peripheral vein, cord vein, and cord artery serum at delivery in pregnancies with intrauterine growth retardation. Endocrinologia Japonica 1983;30:155‐62. - PubMed
Taylor 2003 {published data only}
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Teoh 1971 {published data only}
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Tonari 1987 {published data only}
    1. Tonari M. Studies on the relation between fetal heart rate change, placental finding and fetal outcome. [Japanese]. Acta Obstetrica et Gynaecologica Japonica 1987;39:751‐9.
Torok 1987 {published data only}
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Triunfo 2014 {published data only}
    1. Triunfo S, Lobmaier S, Parra‐Saavedra M, Crovetto F, Peguero A, Nadal A, et al. Angiogenic factors at diagnosis of late‐onset small‐for‐gestational age and histological placental underperfusion. Placenta 2014;35:398‐403. - PubMed
Triunfo 2016 {published data only}
    1. Triunfo S, Parra‐Saavedra M, Rodriguez‐Sureda V, Crovetto F, Dominguez C, Gratacos E, et al. Angiogenic factors and Doppler evaluation in normally growing fetuses at routine third‐trimester scan: prediction of subsequent low birth weight. Fetal Diagnosis and Therapy 2016;40:13‐20. - PubMed
Triunfo 2016a {published data only}
    1. Triunfo S, Crovetto F, Scazzocchio E, Parra‐Saavedra M, Gratacos E, Figueras F. Contingent versus routine third‐trimester screening for late fetal growth restriction. Ultrasound in Obstetrics and Gynecology 2016;47:81‐8. - PubMed
Tsiakkas 2015 {published data only}
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Tsiakkas 2016 {published data only}
    1. Tsiakkas A, Saiid Y, Wright A, Wright D, Nicolaides KH. Competing risks model in screening for preeclampsia by maternal factors and biomarkers at 30‐34 weeks' gestation. American Journal of Obstetrics and Gynecology 2016;215:87.e1‐87.e17. - PubMed
Turpin 2015 {published data only}
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Van Rijn 2015 {published data only}
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Varma 1979 {published data only}
    1. Varma TR, Taylor H, Bridges C. Ultrasound assessment of fetal growth. British Journal of Obstetrics and Gynaecology 1979;86:623‐32. - PubMed
Varma 1982 {published data only}
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Vatten 2012 {published data only}
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Vinayagam 2015 {published data only}
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Wallner 2007 {published data only}
    1. Wallner W, Sengenberger R, Strick R, Strissel PL, Meurer B, Beckmann MW, et al. Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clinical Science 2007;112:51‐7. - PubMed
Watson 1973 {published data only}
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Weissbach 1985 {published data only}
    1. Weissbach A, Freymann E, Hubl W, Seefried W, Neef B, Thiele HJ. Enzymeimmunoassay of unconjugated estriol in serum and saliva during pregnancy. Experimental & Clinical Endocrinology 1985;86:178‐84. - PubMed
Whigham 1980 {published data only}
    1. Whigham KA, Howie PW, Shah MM, Prentice CR. Factor VIII related antigen/coagulant activity ratio as a predictor of fetal growth retardation: a comparison with hormone and uric acid measurements. British Journal of Obstetrics and Gynaecology 1980;87:797‐803. - PubMed
White 2016 {published data only}
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Woelkers 2016 {published data only}
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Woo 2016 {published data only}
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Woods 2015 {published data only}
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Wurz 1983 {published data only}
    1. Wurz H, Luben G, Bohn H, Kunzig HJ, Geiger W. Concentration of placental protein 10 (PP10) in maternal serum and amniotic fluid throughout normal gestation and in pregnancy complicated by fetal growth retardation. Archives of Gynecology 1983;233:165‐74. - PubMed
Xing 2016 {published data only}
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Xu 2015 {published data only}
    1. Xu Y, Lek N, Cheung YB, Biswas A, Su LL, Kwek KY, et al. Unconditional and conditional standards for fetal abdominal circumference and estimated fetal weight in an ethnic Chinese population: a birth cohort study. BMC Pregnancy & Childbirth 2015;15:141. - PMC - PubMed
Yamaguchi 1979 {published data only}
    1. Yamaguchi H, Nishiyama Y, Nose Y, Sugiyama Y. [Usefulness of serum HPL determination as an indicator of placental function and fetal growth]. Horumon to Rinsho ‐ Clinical Endocrinology 1979;27:191‐6. - PubMed
Yanaihara 1984 {published data only}
    1. Yanaihara T, Hirato K, Seo F, Mitsukawa G, Kojima S, Maruyama S, et al. [Prenatal diagnosis of IUGR by assessing the multiple hormone concentration in maternal peripheral blood]. Nippon Sanka Fujinka Gakkai Zasshi ‐ Acta Obstetrica et Gynaecologica Japonica 1984;36:182‐8. - PubMed
Zail 1975 {published data only}
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Zera 2011 {published data only}
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Zhang 2011 {published data only}
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Zlatnik 1979 {published data only}
    1. Zlatnik FJ, Varner MW, Hauser KS. Human placental lactogen: a predictor of perinatal outcome?. Obstetrics and Gynecology 1979;54:205‐10. - PubMed
Zuckerman 1974 {published data only}
    1. Zuckerman H, Gendler L, Schwarz M, Harpaz S. Human placental lactogen as an index of placental function. Israel Journal of Medical Sciences 1974;10:490‐4. - PubMed

References to studies awaiting assessment

Bracali 1968 {published data only}
    1. Bracali R, Corrado F. Clinical value of urinary estriol as an index of placental function and of fetal vitality in some pathological conditions of pregnancy. [Italian]. Quaderni di Clinica Ostetrica e Ginecologica 1968;23:1534‐52. - PubMed
Fuks 1990 {published data only}
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