CoChat
Sign Up
Cited by 287Pregnancy and preeclampsia studiesNeurological Complications and SyndromesReproductive System and Pregnancy

The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.

The change in concentrations of angiogenic and anti-angiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age

Open access
Erez, Offer, Romero, Roberto, Espinoza, Jimmy, Fu, Wenjiang, Todem, David, Kusanovic, Juan Pedro, Gotsch, Francesca, Edwin, Samuel, Nien, Jyh Kae, Chaiworapongsa, Tinnakorn, Mittal, Pooja, Mazaki-Tovi, Shali, Than, Nandor Gabor, Gomez, Ricardo, Hassan, Sonia S.·2008·The Journal of Maternal-Fetal & Neonatal Medicine
DOI 10.1080/14767050802034545PMC PMC2846114
Open this paper in CoChat — free accountOpen PDF

Abstract

INTRODUCTION: An imbalance between angiogenic and anti-angiogenic factors has been proposed as central to the pathophysiology of preeclampsia (PE). Indeed, patients with PE and those delivering small-for-gestational age (SGA) neonates have higher plasma concentrations of soluble vascular endothelial growth factor receptor-1 (sVEGFR-1) and the soluble form of endoglin (s-Eng), as well as lower plasma concentrations of vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) than do patients with normal pregnancies. Of note, this imbalance has been observed before the clinical presentation of PE or the delivery of an SGA neonate. The objective of this study was to determine if changes in the profile of angiogenic and anti-angiogenic factors in maternal plasma between the first and second trimesters are associated with a high risk for the subsequent development of PE and/or delivery of an SGA neonate. METHODS: This longitudinal case-control study included 402 singleton pregnancies in the following groups: (1) normal pregnancies with appropriate for gestational age (AGA) neonates (n = 201); (2) patients who delivered an SGA neonate (n = 145); and (3) patients who developed PE (n = 56). Maternal plasma samples were obtained at the time of each prenatal visit, scheduled at 4-week intervals from the first or early second trimester until delivery. In this study, we included two samples per patient: (1) first sample obtained between 6 and 15 weeks of gestation ('first trimester' sample), and (2) second sample obtained between 20 and 25 weeks of gestation ('second trimester' sample). Plasma concentrations of s-Eng, sVEGFR-1, and PlGF were determined by specific and sensitive immunoassays. Changes in the maternal plasma concentrations of these angiogenesis-related factors were compared among normal patients and those destined to develop PE or deliver an SGA neonate while adjusting for maternal age, nulliparity, and body mass index. General linear models and polytomous logistic regression models were used to relate the analyte concentrations, ratios, and product to the subsequent development of PE and SGA. RESULTS: (1) An increase in the maternal plasma concentration of s-Eng between the first and second trimesters conferred risk for the development of preterm PE and SGA (OR 14.9, 95% CI 4.9-45.0 and OR 2.9, 95% CI 1.5-5.6, respectively). (2) An increase in the maternal plasma concentration of sVEGFR-1 between the first and second trimester conferred risk for the development of preterm PE (OR 3.9, 95% CI 1.2-12.6). (3) A subnormal increase in maternal plasma PlGF concentration between the first and the second trimester was a risk factor for the subsequent development of preterm and term PE (OR 4.3, 95% CI 1.2-15.5 and OR 2.7, 95% CI 1.2-5.9, respectively). (4) In addition, the combination of the three analytes into a pro-angiogenic versus anti-angiogenic ratio (PlGF/(s-Eng x VEGFR-1)) conferred risk for the subsequent development of preterm PE (OR 3.7, 95% CI 1.1-12.1). (5) Importantly, patients with a high change in the s-Eng x sVEGFR-1 product had an OR of 10.4 (95% CI 3.2-33.8) for the development of preterm PE and 1.6 (95% CI 1.0-2.6) for the development of SGA. CONCLUSIONS: Changes in the maternal plasma concentrations of s-Eng, sVEGFR-1, PlGF or their ratios between the first and second trimesters of pregnancy confer an increased risk to deliver an SGA neonate and/or develop PE.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1080/14767050802034545

Cites

59 of 59 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 59 references

Research works printed but not linked: 2

  1. Richani K, 2005, J Soc Gynecol Investig, 12
  2. Gonzalez R P, 2004, Rev Med Chil, 132, 1155

Cited by

Sorted by citations

Items 201–287 of 287

Related

See all

Metadata

Authors
Erez, O., Romero, R., Espinoza, J., Fu, W., Todem, D., Kusanovic, J. P., Gotsch, F., Edwin, S., Nien, J. K., Chaiworapongsa, T., Mittal, P., Mazaki-Tovi, S., Than, N. G., Gomez, R., & Hassan, S. S.
Affiliations
  • United States Department of Health and Human Services (US)
  • National Institutes of Health (US)
  • Michigan State University (US)
  • Pontificia Universidad Católica de Chile (CL)
Corresponding author
  • Erez, Offer
  • Romero, Roberto
ORCID
Venue
The Journal of Maternal-Fetal & Neonatal Medicine
Publisher
Informa UK Limited
Published
2008-01
Volume
21
Issue
5
Pages
279-287
ISSN
  • 1476-4954 (ISSN-L)
  • 1476-7058
DOI
10.1080/14767050802034545
PMC
PMC2846114
OpenAlex
W2036421581
Cited by
287
References
59
Citations by year
2026: 5 · 2025: 3 · 2024: 10 · 2023: 8 · 2022: 14 · 2021: 11 · 2020: 8 · 2019: 22 · 2018: 10 · 2017: 16 · 2016: 14 · 2015: 19 · 2014: 22 · 2013: 21 · 2012: 27
FWCI
29.54
Type
journal article
Language
en
Open access
Locations
  • The Journal of Maternal-Fetal & Neonatal Medicine (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • U.S. Department of Health and Human Services
  • National Institutes of Health
  • National Institute of Child Health and Human Development
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (Z01HD002400)
Topics
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
  • Health Sciences › Medicine › Clinical Neurology › Neurological Complications and Syndromes
  • Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Keywords
preeclampsia, small for gestational age, angiogenic factors, anti-angiogenic factors, soluble endoglin, soluble fms-like tyrosine kinase-1, placental growth factor, vascular endothelial growth factor, maternal plasma biomarkers, first and second trimester, risk prediction, pregnancy complications, placental insufficiency, endothelial dysfunction
MeSH terms
Endoglin, Placenta Growth Factor, Adult, Female, Fetal Growth Retardation, Humans, Infant, Newborn, Infant, Small for Gestational Age, Longitudinal Studies, Pre-Eclampsia, Pregnancy, Pregnancy Proteins, Pregnancy Trimester, First, Pregnancy Trimester, Second, Receptors, Cell Surface, Retrospective Studies, Antigens, CD, Linear Models, Risk Assessment, Neovascularization, Physiologic, Vascular Endothelial Growth Factor Receptor-1

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review