Androgen Concentrations in Umbilical Cord Blood and Their Association with Maternal, Fetal and Obstetric Factors

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Abstract

The aim of this study was to measure umbilical blood androgen concentrations in a birth cohort using a highly specific liquid chromatography-tandem mass spectrometry (LC-MS/MS) assay and assesses the effects of sex, labor, and gestational age on fetal androgen levels at birth. We performed a prospective cohort study of androgen concentrations in mixed arterial and venous umbilical cord serum from 803 unselected singleton pregnancies from a general obstetric population in Western Australia. Total testosterone (TT), Δ4-androstenedione, and dehydroepiandrosterone were extracted from archived cord serum samples and measured using LC-MS/MS. SHBG was measured by ELISA; free testosterone (FT) and bioavailable testosterone (BioT) values were also calculated. Median values for all three androgens were generally lower than previously published values. Levels of TT, FT, BioT, and SHBG were significantly higher in male verses female neonates (P<0.0001), while dehydroepiandrosterone levels were higher in females (P<0.0001). Labor was associated with a significant (∼15–26%) decrease in median cord blood TT and FT levels (both sexes combined), but a modest (∼16–31%) increase in SHBG, Δ4-androstenedione, and dehydroepiandrosterone concentrations. TT and FT were significantly negatively correlated with gestational age at delivery, while SHBG, Δ4-androstenedione, and dehydroepiandrosterone were positively correlated. Antenatal glucocorticoid administration also had a significant effect in the multiple regression models. This is the first study to report umbilical cord androgen levels in a large unselected population of neonates using LC-MS/MS. Our findings suggest that previous studies have over-estimated cord androgen levels, and that fetal, maternal, and obstetric factors influence cord androgen levels differentially. Caution should be exercised when interpreting previously-published data that have not taken all of these factors into account.

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Position statement: Utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement.

William Rosner, Richard Auchus, Ricardo Azziz … (2007)

The objective of the study was to evaluate the current state of clinical assays for total and free testosterone. The five participants were appointed by the Council of The Endocrine Society and charged with attaining the objective using published data and expert opinion. Data were gleaned from published sources via online databases (principally PubMed, Ovid MEDLINE, Google Scholar), the College of American Pathologists, and the clinical and laboratory experiences of the participants. The statement was an effort of the committee and was reviewed in detail by each member. The Council of The Endocrine Society reviewed a late draft and made specific recommendations. Laboratory proficiency testing should be based on the ability to measure accurately and precisely samples containing known concentrations of testosterone, not only on agreement with others using the same method. When such standardization is in place, normative values for total and free testosterone should be established for both genders and children, taking into account the many variables that influence serum testosterone concentration.

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Elevated rates of testosterone-related disorders in women with autism spectrum conditions.

Erin Ingudomnukul, Simon Baron-Cohen, Sally Wheelwright … (2007)

The androgen theory of autism proposes that autism spectrum conditions (ASC) are in part due to elevated fetal testosterone (FT) levels, which are positively correlated with a number of autistic traits and inversely correlated with social development and empathy. A medical questionnaire was completed by n=54 women with ASC, n=74 mothers of children with ASC, and n=183 mothers of typically developing children to test whether women with ASC have an increased rate of testosterone-related medical conditions, and to see whether mothers of children with ASC show similar abnormalities, as part of the 'broader autism phenotype'. Compared to controls, significantly more women with ASC reported (a) hirsutism, (b) bisexuality or asexuality, (c) irregular menstrual cycle, (d) dysmenorrhea, (e) polycystic ovary syndrome, (f) severe acne, (g) epilepsy, (h) tomboyism, and (i) family history of ovarian, uterine, and prostate cancers, tumors, or growths. Compared to controls, significantly more mothers of ASC children reported (a) severe acne, (b) breast and uterine cancers, tumors, or growths, and (c) family history of ovarian and uterine cancers, tumors, or growths. These results suggest current hormone abnormalities in women with ASC and their mothers. Direct investigations of serum testosterone levels and genetic susceptibility to high testosterone production or sensitivity in women with ASC would illuminate the origin of these conditions. The relationship between FT and current testosterone levels also needs to be clarified. The present results may be relevant to understanding the increased male risk to developing autism.

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Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys.

Bonnie Auyeung, Simon Baron-Cohen, Emma Ashwin … (2009)

Mammals, including humans, show sex differences in juvenile play behavior. In rodents and nonhuman primates, these behavioral sex differences result, in part, from sex differences in androgens during early development. Girls exposed to high levels of androgen prenatally, because of the genetic disorder congenital adrenal hyperplasia, show increased male-typical play, suggesting similar hormonal influences on human development, at least in females. Here, we report that fetal testosterone measured from amniotic fluid relates positively to male-typical scores on a standardized questionnaire measure of sex-typical play in both boys and girls. These results show, for the first time, a link between fetal testosterone and the development of sex-typical play in children from the general population, and are the first data linking high levels of prenatal testosterone to increased male-typical play behavior in boys.

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Author and article information

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: 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: 2012

Publication date (Electronic): 20 August 2012

Volume: 7

Issue: 8

Electronic Location Identifier: e42827

Affiliations

[1 ]School of Women's and Infants' Health, King Edward Memorial Hospital, University of Western Australia, Perth, Western Australia, Australia

[2 ]Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth, Western Australia, Australia

[3 ]CPR Pharma Services Pty Ltd, BioSA Incubator, Thebarton, South Australia, Australia

[4 ]Department of Obstetrics and Gynaecology, University of Melbourne, The Women's Hospital, Melbourne, Victoria, Australia

Fudan University, China

Author notes

* E-mail: jeff.keelan@ 123456uwa.edu.au

Competing Interests: HWT and AD received payment for the LC-MS/MS analysis via their employment with CPR Pharma. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials. There are no other conflicts of interest.

Conceived and designed the experiments: EM MH JPN. Performed the experiments: JAK HT AD. Analyzed the data: JAK EM AJOW PJ. Contributed reagents/materials/analysis tools: HT AD. Wrote the paper: JAK EM JPN PJ MH.

Article

Publisher ID: PONE-D-11-24502

DOI: 10.1371/journal.pone.0042827

PMC ID: 3423422

PubMed ID: 22916165

SO-VID: 072705f7-150f-46b8-89bd-3277fe51a8a8

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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 : 5 December 2011

Date accepted : 12 July 2012

Page count

Pages: 10

Funding

This study was funded by a competitive grant to EM and MH from Rotary Mental Health Australia. The Raine Study is funded by the Raine Medical Research Foundation at The University of Western Australia (UWA), the National Health and Medical Research Council of Australia (NHMRC), the Telstra Foundation, the Women and Infants Research Foundation, Curtin University, and the UWA Faculty of Medicine, Dentistry and Health Sciences. JAK is funded by the Women and Infants Research Foundation; MH is funded by an NHMRC Clinical Career Development Award; and AJOW is funded by a NHMRC Career Development Fellowship (#1004065). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Androgen Concentrations in Umbilical Cord Blood and Their Association with Maternal, Fetal and Obstetric Factors

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Most cited references 54

Position statement: Utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement.

Elevated rates of testosterone-related disorders in women with autism spectrum conditions.

Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys.

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