Maternal Factors Associated with Fetal Growth and Birthweight Are Independent Determinants of Placental Weight and Exhibit Differential Effects by Fetal Sex

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Abstract

Introduction

Maternal nutritional and metabolic factors influence the developmental environment of the fetus. Virtually any nutritional factor in the maternal blood has to pass the placental membranes to reach the fetal blood. Placental weight is a commonly used measure to summarize placental growth and function. Placental weight is an independent determinant of fetal growth and birthweight and modifies the associations between maternal metabolic factors and fetal growth. We hypothesized that maternal factors known to be related to fetal growth, newborn size and body composition are determinants of placental weight and that effects of maternal metabolic factors on placental weight differ between the genders.

Methods

The STORK study is a prospective longitudinal study including 1031 healthy pregnant women of Scandinavian heritage with singleton pregnancies. Maternal determinants (parity, body mass index, gestational weight gain and fasting plasma glucose) of placental weight were explored by linear regression models, stratified by fetal sex.

Results

Parity, maternal BMI, gestational weight gain and fasting glucose had positive effects on placental weight. There was a sex specific effect in these associations. Fasting glucose was significantly associated with placental weight in females but not in males.

Conclusion

Maternal factors known to influence fetal growth, birthweight and neonatal body composition are determinants of placental weight. The effect of maternal factors on placental weight is influenced by sex as illustrated in the relation between maternal glucose and placental weight.

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Most cited references 28

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Placental hormones and the control of maternal metabolism and fetal growth.

Dorothee Newbern, Michael Freemark (2011)

To examine the roles of the placental and pituitary hormones in the control of maternal metabolism and fetal growth. In addition to promoting growth of maternal tissues, placental growth hormone (GH-V) induces maternal insulin resistance and thereby facilitates the mobilization of maternal nutrients for fetal growth. Human placental lactogen (hPL) and prolactin increase maternal food intake by induction of central leptin resistance and promote maternal beta-cell expansion and insulin production to defend against the development of gestational diabetes mellitus. The effects of the lactogens are mediated by diverse signaling pathways and are potentiated by glucose. Pathologic conditions of pregnancy are associated with dysregulation of GH-V and hPL gene expression. The somatogenic and lactogenic hormones of the placenta and maternal pituitary gland integrate the metabolic adaptations of pregnancy with the demands of fetal and neonatal development. Dysregulation of placental growth hormone and/or placental lactogen in pathologic conditions of pregnancy may adversely impact fetal growth and postnatal metabolic function.

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Gene expression patterns in human placenta.

Bradley Brown, Ruchira Sood, James L. Zehnder … (2006)

The placenta is the principal metabolic, respiratory, excretory, and endocrine organ for the first 9 months of fetal life. Its role in fetal and maternal physiology is remarkably diverse. Because of the central role that the placenta has in fetal and maternal physiology and development, the possibility that variation in placental gene expression patterns might be linked to important abnormalities in maternal or fetal health, or even variations in later life, warrants investigation. As an initial step, we used DNA microarrays to analyze gene expression patterns in 72 samples of amnion, chorion, umbilical cord, and sections of villus parenchyma from 19 human placentas from successful full-term pregnancies. The umbilical cord, chorion, amnion, and villus parenchyma samples were readily distinguished by differences in their global gene-expression patterns, many of which seemed to be related to physiology and histology. Differentially expressed genes have roles that include placental trophoblast secretion, signal transduction, metabolism, immune regulation, cell adhesion, and structure. We found interindividual differences in expression patterns in villus parenchyma and systematic differences between the maternal, fetal, and intermediate layers. A group of genes that was expressed in both the maternal and fetal villus parenchyma sections of placenta included genes that may be associated with preeclampsia. We identified sets of genes whose expression in placenta was significantly correlated with the sex of the fetus. This study provides a rich and diverse picture of the molecular variation in the placenta from healthy pregnancies.

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Hyperglycaemia and Adverse Pregnancy Outcome (HAPO) Study: associations with maternal body mass index.

(2010)

To determine whether higher maternal body mass index (BMI), independent of maternal glycaemia, is associated with adverse pregnancy outcomes. Observational cohort study. Fifteen centres in nine countries. Eligible pregnant women. A 75-g 2-hour oral glucose tolerance test (OGTT) was performed between 24 and 32 weeks of gestation in all participants. Maternal BMI was calculated from height and weight measured at the OGTT. Fetal adiposity was assessed using skinfold measurements and percentage of body fat was calculated. Associations between maternal BMI and pregnancy outcomes were assessed using multiple logistic regression analyses, with adjustment for potential confounders. Predefined primary outcomes were birthweight >90th percentile, primary caesarean section, clinical neonatal hypoglycaemia and cord serum C-peptide >90th percentile. Secondary outcomes included pre-eclampsia, preterm delivery (before 37 weeks) and percentage of body fat >90th percentile. Among 23 316 blinded participants, with control for maternal glycaemia and other potential confounders, higher maternal BMI was associated (odds ratio [95% confidence interval] for highest {> or =42.0 kg/m(2)} versus lowest { 90th percentile (3.52 [2.48-5.00]) and percentage of body fat >90th percentile (3.28 [2.28-4.71]), caesarean section (2.23 [1.66-2.99]), cord C-peptide >90th percentile (2.33 [1.58-3.43]) and pre-eclampsia (14.14 [9.44-21.17]). Preterm delivery was less frequent with higher BMI (0.48 [0.31-0.74]). Associations with fetal size tended to plateau in the highest maternal BMI categories. Higher maternal BMI, independent of maternal glycaemia, is strongly associated with increased frequency of pregnancy complications, in particular those related to excess fetal growth and adiposity and to pre-eclampsia.

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Author and article information

Contributors

Victor Sanchez-Margalet: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2014

Publication date (Electronic): 6 February 2014

Volume: 9

Issue: 2

Electronic Location Identifier: e87303

Affiliations

[1 ]Department of Obstetrics, Oslo University Hospital, Oslo, Norway

[2 ]Department of Specialized Endocrinology, Oslo University Hospital, Oslo, Norway

[3 ]University of Oslo, Oslo, Norway

Virgen Macarena University Hospital, School of Medicine, University of Seville, Spain

Author notes

* E-mail: mcpaasche@ 123456hotmail.com

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: MCR CF KG JB GH TH. Performed the experiments: MCR CF KG. Analyzed the data: MCR CF. Contributed reagents/materials/analysis tools: KG. Wrote the paper: MCR CF KG JB GH TH.

Article

Publisher ID: PONE-D-13-37254

DOI: 10.1371/journal.pone.0087303

PMC ID: 3916298

PubMed ID: 24516548

SO-VID: f4c16c8d-80fe-4cdb-b86b-93b1c70f0402

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 10 September 2013

Date accepted : 24 December 2013

Page count

Pages: 5

Funding

The work has been supported by the Norwegian Extrafoundation For Health and Research, The Norwegian Health Association and the University of Oslo. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Maternal Factors Associated with Fetal Growth and Birthweight Are Independent Determinants of Placental Weight and Exhibit Differential Effects by Fetal Sex

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Abstract

Introduction

Methods

Results

Conclusion

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PLOS Climate

Most cited references 28

Placental hormones and the control of maternal metabolism and fetal growth.

Gene expression patterns in human placenta.

Hyperglycaemia and Adverse Pregnancy Outcome (HAPO) Study: associations with maternal body mass index.

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