Top

Journal of Autism and Developmental Disorders

Gepubliceerd in:

13-08-2019 | Origina lPaper

Early Second Trimester Maternal Serum Steroid-Related Biomarkers Associated with Autism Spectrum Disorder

Auteurs: Deborah A. Bilder, M. Sean Esplin, Hilary Coon, Paul Burghardt, Erin A. S. Clark, Alison Fraser, Ken R. Smith, Whitney Worsham, Katlin Chappelle, Thomas Rayner, Amanda V. Bakian

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 11/2019

Abstract

Epidemiologic studies link increased autism spectrum disorder (ASD) risk to obstetrical conditions associated with inflammation and steroid dysregulation, referred to as prenatal metabolic syndrome (PNMS). This pilot study measured steroid-related biomarkers in early second trimester maternal serum collected during the first and second trimester evaluation of risk study. ASD case and PNMS exposure status of index offspring were determined through linkage with autism registries and birth certificate records. ASD case (N = 53) and control (N = 19) groups were enriched for PNMS exposure. Higher estradiol and lower sex hormone binding globulin (SHBG) were significantly associated with increased ASD risk. Study findings provide preliminary evidence to link greater placental estradiol activity with ASD and support future investigations of the prenatal steroid environment in ASD.

vorige artikel Expression Recognition Difficulty Is Associated with Social But Not Attention-to-Detail Autistic Traits and Reflects Both Alexithymia and Perceptual Difficulty

volgende artikel Correction to: Early Second Trimester Maternal Serum Steroid‑Related Biomarkers Associated with Autism Spectrum Disorder

Alleen toegankelijk voor geautoriseerde gebruikers

Albrecht, E. D., & Pepe, G. J. (1999). Central integrative role of oestrogen in modulating the communication between the placenta and fetus that results in primate fecal-placental development. Placenta, 20(2–3), 129–139.CrossRefPubMed

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Philadelphia: American Psychiatric Association. https://doi.org/10.1176/appi.books.9780890425596.CrossRef

Anderson, J. N., Peck, E. J., & Clark, J. H. (1975). Estrogen-induced uterine responses and growth: Relationship to receptor estrogen binding by uterine nuclei. Endocrinology, 96(1), 160–167. https://doi.org/10.1210/endo-96-1-160.CrossRefPubMed

Andridge, R. R., & Little, R. J. A. (2010). A review of hot deck imputation for survey non-response. International Statistical Review = Revue Internationale de Statistique, 78(1), 40–64. https://doi.org/10.1111/j.1751-5823.2010.00103.x.CrossRefPubMedPubMedCentral

Baio, J., Wiggins, L., Christensen, D. L., Maenner, M. J., Daniels, J., & Warren, Z. (2018). Prevalence of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network, 11 sites, United States, 2014. Morbidity and Mortality Weekly Report. Surveillance Summaries (Washington, D.C.: 2002), 67(6), 1–23. https://doi.org/10.15585/mmwr.ss6706a1.CrossRef

Bakian, A. V., Bilder, D. A., Carbone, P. S., Hunt, T. D., Petersen, B., & Rice, C. E. (2015a). Brief report: independent validation of autism spectrum disorder case status in the Utah Autism and Developmental Disabilities Monitoring (ADDM) network site. Journal of Autism and Developmental Disorders, 45(3), 873–880. https://doi.org/10.1007/s10803-014-2187-6.CrossRefPubMedPubMedCentral

Bakian, A. V., Bilder, D. A., Coon, H., & McMahon, W. M. (2015b). Spatial relative risk patterns of autism spectrum disorders in Utah. Journal of Autism and Developmental Disorders, 45(4), 988–1000. https://doi.org/10.1007/s10803-014-2253-0.CrossRefPubMedPubMedCentral

Baron-Cohen, S., Auyeung, B., Nørgaard-Pedersen, B., Hougaard, D. M., Abdallah, M. W., Melgaard, L., et al. (2015). Elevated fetal steroidogenic activity in autism. Molecular Psychiatry, 20, 369–376.CrossRefPubMed

Bilder, D. A., Bakian, A. V., Viskochil, J., Clark, E. A. S., Botts, E. L., Smith, K. R., et al. (2013). Maternal prenatal weight gain and autism spectrum disorders. Pediatrics, 132(5), e1276–e1283. https://doi.org/10.1542/peds.2013-1188.CrossRefPubMedPubMedCentral

Brown, A. S., Sourander, A., Hinkka-Yli-Salomäki, S., McKeague, I. W., Sundvall, J., & Surcel, H.-M. (2014). Elevated maternal C-reactive protein and autism in a national birth cohort. Molecular Psychiatry, 19(2), 259–264. https://doi.org/10.1038/mp.2012.197.CrossRefPubMed

Center for Disease Control and Prevention, Autism and Developmental Disabilities Monitoring Network Surveillance Year 2002 Principal Investigators. (2007). Prevalence of Autism Spectrum Disorders—Autism and Developmental Disabilities Monitoring Network, 14 Sites, United States, 2002 (MMWR No. 56) (pp. 12–28)

Corbett, B. A., Mendoza, S., Abdullah, M., Wegelin, J. A., & Levine, S. (2006). Cortisol circadian rhythms and response to stress in children with autism. Psychoneuroendocrinology, 31(1), 59–68. https://doi.org/10.1016/j.psyneuen.2005.05.011.CrossRefPubMed

Coulter, C. L., & Jaffe, R. B. (1998). Functional maturation of the primate fetal adrenal in vivo: 3. Specific zonal localization and developmental regulation of CYP21A2 (P450c21) and CYP11B1/CYP11B2 (P450c11/aldosterone synthase) lead to integrated concept of zonal and temporal steroid biosynthesis. Endocrinology, 139(12), 5144–5150. https://doi.org/10.1210/endo.139.12.6333.CrossRefPubMed

Cunningham, F. G. (2010). Implantation, embryogenesis, and placental development. In F. Cunningham (Ed.), Williams obstetrics, (23rd ed., pp. 36–77) New York: McGraw-Hill. Medical, c2010.

DeLong, E. R., DeLong, D. M., & Clarke-Pearson, D. L. (1988). Comparing the areas under two or more correlated receiver operating characteristic curves: A nonparametric approach. Biometrics, 44(3), 837–845. https://doi.org/10.2307/2531595.CrossRefPubMed

Dobie, S. A., Baldwin, L. M., Rosenblatt, R. A., Fordyce, M. A., & Andrilla, C. H. (1998). How well do birth certificates describe the pregnancies they report? The Washington State experience with low-risk pregnancies. Maternal and Child Health Journal, 2(3), 145–154.CrossRefPubMed

Dodds, L., Fell, D. B., Shea, S., Armson, B. A., Allen, A. C., & Bryson, S. (2011). The role of prenatal, obstetric and neonatal factors in the development of autism. Journal of Autism and Developmental Disorders, 41(7), 891–902.CrossRefPubMed

Falah, N., Torday, J., Quinney, S. K., & Haas, D. M. (2015). Estriol review: Clinical applications and potential biomedical importance. Clinical Research and Trials. https://doi.org/10.15761/crt.1000109.CrossRef

Gillon, T. E. R., Pels, A., Dadelszen, P. V., Macdonell, K., & Magee, L. A. (2014). Hypertensive disorders of pregnancy: A systematic review of international clinical practice guidelines. PLoS ONE. https://doi.org/10.1371/journal.pone.0113715.CrossRefPubMedPubMedCentral

Goebelsmann, U., & Jaffe, R. B. (1971). Oestriol metabolism in pregnant women. Acta Endocrinologica, 66(4), 679–693.CrossRefPubMed

Goines, P. E., Croen, L. A., Braunschweig, D., Yoshida, C. K., Grether, J., Hansen, R., et al. (2011). Increased midgestational IFN-γ, IL-4 and IL-5 in women bearing a child with autism: A case-control study. Molecular Autism, 2, 13. https://doi.org/10.1186/2040-2392-2-13.CrossRefPubMedPubMedCentral

Guller, S., Bulletti, C., Biener, A., & Gurpide, E. (1984). Relative distribution of estrone, estradiol and estriol between fetal and maternal perfusates during perfusions of human term placentas with labelled C19 precursors. Journal of Steroid Biochemistry, 20(4B), 975–979.CrossRefPubMed

Hammond, G. L. (2011). Diverse roles for sex hormone-binding globulin in reproduction. Biology of Reproduction, 85(3), 431–441. https://doi.org/10.1095/biolreprod.111.092593.CrossRefPubMedPubMedCentral

Helzlsouer, K. J., Alberg, A. J., Gordon, G. B., Longcope, C., Bush, T. L., Hoffman, S. C., et al. (1995). Serum gonadotropins and steroid hormones and the development of ovarian cancer. JAMA, 274(24), 1926–1930.CrossRefPubMed

Hisle-Gorman, E., Susi, A., Stokes, T., Gorman, G., Erdie-Lalena, C., & Nylund, C. M. (2018). Prenatal, perinatal, and neonatal risk factors of autism spectrum disorder. Pediatric Research, 84(2), 190–198. https://doi.org/10.1038/pr.2018.23.CrossRefPubMed

Holl, K., Lundin, E., Kaasila, M., Grankvist, K., Afanasyeva, Y., Hallmans, G., et al. (2008). Effect of long-term storage on hormone measurements in samples from pregnant women: The experience of the Finnish Maternity Cohort. Acta Oncologica (Stockholm, Sweden), 47(3), 406–412. https://doi.org/10.1080/02841860701592400.CrossRef

Howland, M. A., Sandman, C. A., & Glynn, L. M. (2017). Developmental origins of the human hypothalamic-pituitary-adrenal axis. Expert Review of Endocrinology & Metabolism, 12(50), 321–339. https://doi.org/10.1080/17446651.2017.1356222.CrossRef

Ishimoto, H., & Jaffe, R. B. (2011). Development and function of the human fetal adrenal cortex: A key component in the feto-placental unit. Endocrine Reviews, 32(3), 317–355. https://doi.org/10.1210/er.2010-0001.CrossRefPubMed

Jobe, S. O., Tyler, C. T., & Magness, R. R. (2013). Aberrant synthesis, metabolism, and plasma accumulation of circulating estrogens and estrogen metabolites in preeclampsia implications for vascular dysfunction. Hypertension (Dallas, Tex.: 1979), 61(2), 480–487. https://doi.org/10.1161/hypertensionaha.111.201624.CrossRef

Jones, K. L., Croen, L. A., Yoshida, C. K., Heuer, L., Hansen, R., Zerbo, O., et al. (2017). Autism with intellectual disability is associated with increased levels of maternal cytokines and chemokines during gestation. Molecular Psychiatry, 22(2), 273–279. https://doi.org/10.1038/mp.2016.77.CrossRefPubMed

Kallen, C. B. (2004). Steroid hormone synthesis in pregnancy. Obstetrics and Gynecology Clinics of North America, 31(4), 795–816. https://doi.org/10.1016/j.ogc.2004.08.009.CrossRefPubMed

Kinnunen, T. I., Luoto, R., Gissler, M., Hemminki, E., & Hilakivi-Clarke, L. (2004). Pregnancy weight gain and breast cancer risk. BMC Womens Health, 4(1), 7.CrossRefPubMedPubMedCentral

Krakowiak, P., Walker, C. K., Bremer, A. A., Baker, A. S., Ozonoff, S., Hansen, R. L., et al. (2012). Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics, 129(5), e1121–e1128. https://doi.org/10.1542/peds.2011-2583.CrossRefPubMedPubMedCentral

Lawrence, J. M., Contreras, R., Chen, W., & Sacks, D. A. (2008). Trends in the prevalence of preexisting diabetes and gestational diabetes mellitus among a racially/ethnically diverse population of pregnant women, 1999–2005. Diabetes Care, 31(5), 899–904. https://doi.org/10.2337/dc07-2345.CrossRefPubMed

Lumey, L. H. (1998). Prenatal oestrogens and breast cancer. Paediatric and Perinatal Epidemiology, 12(4), 361–365.CrossRefPubMed

Magness, R. R., & Rosenfeld, C. R. (1989). Local and systemic estradiol-17 beta: effects on uterine and systemic vasodilation. The American Journal of Physiology, 256(4 Pt 1), E536–E542. https://doi.org/10.1152/ajpendo.1989.256.4.E536.CrossRefPubMed

Malone, F. D., Canick, J. A., Ball, R. H., Nyberg, D. A., Comstock, C. H., Bukowski, R., … First- and second-trimester evaluation of risk (FASTER) research consortium. (2005). First-trimester or second-trimester screening, or both, for Down’s syndrome. The New England Journal of Medicine, 353(19), 2001–2011. https://doi.org/10.1056/nejmoa043693

Martin, J. N., & Cowan, B. D. (1990). Biochemical assessment and prediction of gestational well-being. Obstetrics and Gynecology Clinics of North America, 17(1), 81–93.PubMed

Mesiano, S., & Jaffe, R. B. (1997). Developmental and functional biology of the primate fetal adrenal cortex. Endocrine Reviews, 18(3), 378–403. https://doi.org/10.1210/edrv.18.3.0304.CrossRefPubMed

Moisiadis, V. G., & Matthews, S. G. (2014). Glucocorticoids and fetal programming part 1: Outcomes. Nature Reviews Endocrinology, 10(7), 391–402. https://doi.org/10.1038/nrendo.2014.73.CrossRefPubMed

Montenegro, Y. H. A., Nascimento, D. Q., Assis, T. O., & Santos-Lopes, S. S. D. (2019). The epigenetics of the hypothalamic-pituitary-adrenal axis in fetal development. Annals of Human Genetics, 83(4), 195–213. https://doi.org/10.1111/ahg.12306.CrossRefPubMed

Murphy, V. E., Smith, R., Giles, W. B., & Clifton, V. L. (2006). Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocrine Reviews, 27(2), 141–169. https://doi.org/10.1210/er.2005-0011.CrossRefPubMed

Nahum Sacks, K., Friger, M., Shoham-Vardi, I., Abokaf, H., Spiegel, E., Sergienko, R., et al. (2016). Prenatal exposure to gestational diabetes mellitus as an independent risk factor for long-term neuropsychiatric morbidity of the offspring. American Journal of Obstetrics and Gynecology, 215(3), 380.e1–380.e7. https://doi.org/10.1016/j.ajog.2016.03.030.CrossRef

Ng, P. C. (2000). The fetal and neonatal hypothalamic–pituitary–adrenal axis. Archives of Disease in Childhood—Fetal and Neonatal Edition, 82(3), F250–F254. https://doi.org/10.1136/fn.82.3.F250.CrossRefPubMedPubMedCentral

Palmer, S. K., Zamudio, S., Coffin, C., Parker, S., Stamm, E., & Moore, L. G. (1992). Quantitative estimation of human uterine artery blood flow and pelvic blood flow redistribution in pregnancy. Obstetrics and Gynecology, 80(6), 1000–1006.PubMed

Pepe, G., & Albrecht, E. (1995). Actions of placental and fetal adrenal steroid hormones in primate pregnancy. Endocrine Reviews, 16(5), 608–645.PubMed

Pepe, G. J., Waddell, B. J., & Albrecht, E. D. (1990). Activation of the baboon fetal hypothalamic-pituitary-adrenocortical axis at midgestation by estrogen-induced changes in placental corticosteroid metabolism. Endocrinology, 127(6), 3117–3123. https://doi.org/10.1210/endo-127-6-3117.CrossRefPubMed

Petridou, E., Katsouyanni, K., Hsieh, C. C., Antsaklis, A., & Trichopoulos, D. (1992). Diet, pregnancy estrogens and their possible relevance to cancer risk in the offspring. Oncology, 49(2), 127–132.CrossRefPubMed

Resko, J. A., Pleom, J. G., & Stadelman, H. L. (1975). Estrogens in fetal and maternal plasma of the rhesus monkey. Endocrinology, 97(2), 425–430. https://doi.org/10.1210/endo-97-2-425.CrossRefPubMed

Resnik, R., Killam, A. P., Battaglia, F. C., Makowski, E. L., & Meschia, G. (1974). The stimulation of uterine blood flow by various estrogens. Endocrinology, 94(4), 1192–1196. https://doi.org/10.1210/endo-94-4-1192.CrossRefPubMed

Reynolds, R. M. (2013). Glucocorticoid excess and the developmental origins of disease: Two decades of testing the hypothesis–2012 Curt Richter Award Winner. Psychoneuroendocrinology, 38(1), 1–11. https://doi.org/10.1016/j.psyneuen.2012.08.012.CrossRefPubMed

Shin, Y. Y., Jeong, J. S., Park, M.-N., Lee, J.-E., An, S.-M., Cho, W.-S., et al. (2018). Regulation of steroid hormones in the placenta and serum of women with preeclampsia. Molecular Medicine Reports, 17(2), 2681–2688. https://doi.org/10.3892/mmr.2017.8165.CrossRefPubMed

Simpson, E. R., & MacDonald, P. C. (1981). Endocrine physiology of the placenta. Annual Review of Physiology, 43, 163–188. https://doi.org/10.1146/annurev.ph.43.030181.001115.CrossRefPubMed

Smith, K. R. (2019). Pedigree and population resource: Utah population database. Retrieved from https://healthcare.utah.edu/huntsmancancerinstitute/research/updb/

Spratt, E. G., Nicholas, J. S., Brady, K. T., Carpenter, L. A., Hatcher, C. R., Meekins, K. A., et al. (2012). Enhanced cortisol response to stress in children in autism. Journal of Autism and Developmental Disorders, 42(1), 75–81. https://doi.org/10.1007/s10803-011-1214-0.CrossRefPubMedPubMedCentral

Strauss, J., Barbieri, R., & Gargiulo, A. (2018). Yen & Jaffe’s reproductive endocrinology (8th ed.). Philadelphia, PA: Elsevier. Retrieved from https://www.elsevier.com/books/yen-and-jaffes-reproductive-endocrinology/9780323479127

Taylor, J. L., & Corbett, B. A. (2014). A review of rhythm and responsiveness of cortisol in individuals with autism spectrum disorders. Psychoneuroendocrinology, 49, 207–228. https://doi.org/10.1016/j.psyneuen.2014.07.015.CrossRefPubMedPubMedCentral

Tomarken, A. J., Han, G. T., & Corbett, B. A. (2015). Temporal patterns, heterogeneity, and stability of diurnal cortisol rhythms in children with autism spectrum disorder. Psychoneuroendocrinology, 62, 217–226.CrossRefPubMedPubMedCentral

Tordjman, S., Anderson, G. M., Kermarrec, S., Bonnot, O., Geoffray, M.-M., Brailly-Tabard, S., et al. (2014). Altered circadian patterns of salivary cortisol in low-functioning children and adolescents with autism. Psychoneuroendocrinology, 50, 227–245. https://doi.org/10.1016/j.psyneuen.2014.08.010.CrossRefPubMed

Tulchinsky, D., & Hobel, C. J. (1973). Plasma human chorionic gonadotropin, estrone, estradiol, estriol, progesterone, and 17α-hydroxyprogesterone in human pregnancy. American Journal of Obstetrics and Gynecology, 117(7), 884–893.CrossRefPubMed

Tulchinsky, D., & Korenman, S. G. (1971). The plasma estradiol as an index of fetoplacental function. Journal of Clinical Investigation, 50(7), 1490–1497.CrossRefPubMedPubMedCentral

van de Beek, C., Thijssen, J. H. H., Cohen-Kettenis, P. T., van Goozen, S. H. M., & Buitelaar, J. K. (2004). Relationships between sex hormones assessed in amniotic fluid, and maternal and umbilical cord serum: What is the best source of information to investigate the effects of fetal hormonal exposure? Hormones and Behavior, 46(5), 663–669. https://doi.org/10.1016/j.yhbeh.2004.06.010.CrossRefPubMed

Walsh, S. W., Wolf, R. C., & Robinson, J. A. (1979). Estrogens in the uteroovarian, uterine, and peripheral plasma in pregnant rhesus monkeys’. Biology of Reproduction, 20, 606–610.CrossRefPubMed

Wang, C., Geng, H., Liu, W., & Zhang, G. (2017). Prenatal, perinatal, and postnatal factors associated with autism: A meta-analysis. Medicine (Baltimore), 96(18), e6696. https://doi.org/10.1097/MD.0000000000006696.CrossRef

Watterberg, Kristi L. (2004). Adrenocortical function and dysfunction in the fetus and neonate. Seminars in Neonatology: SN, 9(1), 13–21. https://doi.org/10.1016/j.siny.2003.08.003.CrossRefPubMed

Watterberg, K. L., Scott, S. M., & Naeye, R. L. (1997). Chorioamnionitis, cortisol, and acute lung disease in very low birth weight infants. Pediatrics, 99(2), E6.CrossRefPubMed

Windham, G. C., Lyall, K., Anderson, M., & Kharrazi, M. (2016). Autism spectrum disorder risk in relation to maternal mid-pregnancy serum hormone and protein markers from prenatal screening in California. Journal of Autism and Developmental Disorders, 46(2), 478–488. https://doi.org/10.1007/s10803-015-2587-2.CrossRefPubMed

Yeargin-Allsopp, M., Rice, C., Karapurkar, T., Doernberg, N., Boyle, C., & Murphy, C. (2003). Prevalence of autism in a US metropolitan area. JAMA, 289(1), 49–55.CrossRefPubMed

Zerbo, O., Traglia, M., Yoshida, C., Heuer, L. S., Ashwood, P., Delorenze, G. N., et al. (2016). Maternal mid-pregnancy C-reactive protein and risk of autism spectrum disorders: The early markers for autism study. Translational Psychiatry, 6(4), e783. https://doi.org/10.1038/tp.2016.46.CrossRefPubMedPubMedCentral

Zinke, K., Fries, E., Kliegel, M., Kirschbaum, C., & Dettenborn, L. (2010). Children with high-functioning autism show a normal cortisol awakening response (CAR). Psychoneuroendocrinology, 35(10), 1578–1582. https://doi.org/10.1016/j.psyneuen.2010.03.009.CrossRefPubMed

Titel: Early Second Trimester Maternal Serum Steroid-Related Biomarkers Associated with Autism Spectrum Disorder
Auteurs: Deborah A. Bilder
M. Sean Esplin
Hilary Coon
Paul Burghardt
Erin A. S. Clark
Alison Fraser
Ken R. Smith
Whitney Worsham
Katlin Chappelle
Thomas Rayner
Amanda V. Bakian
Publicatiedatum: 13-08-2019
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 11/2019
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-019-04162-2

Bohn Stafleu van Loghum

Deel dit onderdeel of sectie (kopieer de link)

Abstract

Log in om toegang te krijgen

Andere artikelen Uitgave 11/2019

Screening of Broader Autism Phenotype Symptoms in Siblings: Support for a Distinct Model of Symptomatology

Spanish Validation of the Autism Quotient Short Form Questionnaire for Adults with Autism Spectrum Disorder

Factors Influencing the Use of Cognitive–Behavioral Therapy with Autistic Adults: A Survey of Community Mental Health Clinicians

The Animal in Me: Enhancing Emotion Recognition in Adolescents with Autism Using Animal Filters

A Pilot Study Investigating the Feasibility and Acceptability of a Parent-Only Behavioral Weight-Loss Treatment for Children with Autism Spectrum Disorder

Clinical Profile of Autism Spectrum Disorder in a Pediatric Population from Northern Mexico