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Associations of maternal glucose markers in pregnancy with cord blood glucocorticoids and child hair cortisol levels

Published online by Cambridge University Press:  08 July 2022

Nathan Cohen
Affiliation:
College of Public Health, University of South Florida, Tampa, FL, USA
Sabrina Faleschini
Affiliation:
Division of Chronic Disease Research Across the Lifecourse, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
Sheryl L. Rifas-Shiman
Affiliation:
Division of Chronic Disease Research Across the Lifecourse, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
Luigi Bouchard
Affiliation:
Centre de recherche du Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke, Quebec, Canada Department of Biochemistry and Functional Genomics, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Quebec, Canada Clinical Department of Laboratory medicine, Centre intégré universitaire de santé et de services sociaux (CIUSSS) du Saguenay–Lac-St-Jean – Hôpital Universitaire de Chicoutimi, Saguenay, Quebec, Canada
Myriam Doyon
Affiliation:
Centre de recherche du Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke, Quebec, Canada
Olivier Simard
Affiliation:
Department of Biochemistry and Functional Genomics, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Quebec, Canada
Melina Arguin
Affiliation:
Centre de recherche du Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke, Quebec, Canada
Guy Fink
Affiliation:
Department of Medical Biology, University Health and Social Service Center of the Estrie, Fleurimont, Quebec, Canada
Amy C. Alman
Affiliation:
College of Public Health, University of South Florida, Tampa, FL, USA
Russell Kirby
Affiliation:
College of Public Health, University of South Florida, Tampa, FL, USA
Henian Chen
Affiliation:
College of Public Health, University of South Florida, Tampa, FL, USA
Ronee Wilson
Affiliation:
College of Public Health, University of South Florida, Tampa, FL, USA
Kimberly Fryer
Affiliation:
Department of Obstetrics and Gynecology, Morsani College of Medicine, University of South Florida, Tampa, FL, USA
Patrice Perron
Affiliation:
Centre de recherche du Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke, Quebec, Canada Department of Medicine, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Quebec, Canada
Emily Oken
Affiliation:
Division of Chronic Disease Research Across the Lifecourse, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Marie-France Hivert*
Affiliation:
Division of Chronic Disease Research Across the Lifecourse, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA Massachusetts General Hospital, Diabetes Unit, Boston, MA, USA
*
Address for correspondence: Marie-France Hivert, Division of Chronic Disease Research Across the Lifecourse, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA. Email: mhivert@partners.org

Abstract

Exposure to maternal hyperglycemia in utero has been associated with adverse metabolic outcomes in offspring. However, few studies have investigated the relationship between maternal hyperglycemia and offspring cortisol levels. We assessed associations of gestational diabetes mellitus (GDM) with cortisol biomarkers in two longitudinal prebirth cohorts: Project Viva included 928 mother–child pairs and Gen3G included 313 mother–child pairs. In Project Viva, GDM was diagnosed in N = 48 (5.2%) women using a two-step procedure (50 g glucose challenge test, if abnormal followed by 100 g oral glucose tolerance test [OGTT]), and in N = 29 (9.3%) women participating in Gen3G using one-step 75 g OGTT. In Project Viva, we measured cord blood glucocorticoids and child hair cortisol levels during mid-childhood (mean (SD) age: 7.8 (0.8) years) and early adolescence (mean (SD) age: 13.2 (0.9) years). In Gen3G, we measured hair cortisol at 5.4 (0.3) years. We used multivariable linear regression to examine associations of GDM with offspring cortisol, adjusting for child age and sex, maternal prepregnancy body mass index, education, and socioeconomic status. We additionally adjusted for child race/ethnicity in the cord blood analyses. In both Project Viva and Gen3G, we observed null associations of GDM and maternal glucose markers in pregnancy with cortisol biomarkers in cord blood at birth (β = 16.6 nmol/L, 95% CI −60.7, 94.0 in Project Viva) and in hair samples during childhood (β = −0.56 pg/mg, 95% CI −1.16, 0.04 in Project Viva; β = 0.09 pg/mg, 95% CI −0.38, 0.57 in Gen3G). Our findings do not support the hypothesis that maternal hyperglycemia is related to hypothalamic–pituitary–adrenal axis activity.

Type
Original Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Casagrande, SS, Linder, B, Cowie, CC. Prevalence of gestational diabetes and subsequent Type 2 diabetes among U.S. women. Diabetes Res Clin Pract. 2018; 141(8), 200208.CrossRefGoogle ScholarPubMed
Landon, MB, Gabbe, SG. Gestational diabetes mellitus. Obstet Gynecol. 2011; 118(6), 13791393.CrossRefGoogle ScholarPubMed
Chen, P, Wang, S, Ji, J, et al. Risk factors and management of gestational diabetes. Cell Biochem Biophys. 2015; 71(2), 689694.CrossRefGoogle ScholarPubMed
Lavery, JA, Friedman, AM, Keyes, KM, Wright, JD, Ananth, CV. Gestational diabetes in the United States: temporal changes in prevalence rates between 1979 and 2010. BJOG. 2017; 124(5), 804813.CrossRefGoogle ScholarPubMed
Getahun, D, Nath, C, Ananth, CV, Chavez, MR, Smulian, JC. Gestational diabetes in the United States: temporal trends 1989 through 2004. Am J Obstet Gynecol. 2008; 198(5), 525.e521–525.CrossRefGoogle ScholarPubMed
He, XJ, Qin, FY, Hu, CL, Zhu, M, Tian, CQ, Li, L. Is gestational diabetes mellitus an independent risk factor for macrosomia: a meta-analysis? Arch Gynecol Obstet. 2015; 291(4), 729735.CrossRefGoogle ScholarPubMed
Rice, MM, Landon, MB. What we have learned about treating mild gestational diabetes mellitus. Semin Perinatol. 2016; 40(5), 298302.CrossRefGoogle ScholarPubMed
Damm, P, Houshmand-Oeregaard, A, Kelstrup, L, Lauenborg, J, Mathiesen, ER, Clausen, TD. Gestational diabetes mellitus and long-term consequences for mother and offspring: a view from Denmark. Diabetologia. 2016; 59(7), 13961399.CrossRefGoogle Scholar
Wright, CS, Rifas-Shiman, SL, Rich-Edwards, JW, Taveras, EM, Gillman, MW, Oken, E. Intrauterine exposure to gestational diabetes, child adiposity, and blood pressure. Am J Hypertens. 2009; 22(2), 215220.CrossRefGoogle ScholarPubMed
Regnault, N, Gillman, MW, Rifas-Shiman, SL, Eggleston, E, Oken, E. Sex-specific associations of gestational glucose tolerance with childhood body composition. Diabetes Care. 2013; 36(10), 30453053.CrossRefGoogle ScholarPubMed
O'Donnell, KJ, Meaney, MJ. Fetal origins of mental health: the developmental origins of health and disease hypothesis. Am J Psychiatry. 2017; 174(4), 319328.CrossRefGoogle ScholarPubMed
Reynolds, RM. Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis--2012 Curt Richter Award Winner. Psychoneuroendocrinology. 2013; 38(1), 111.CrossRefGoogle ScholarPubMed
Moisiadis, VG, Matthews, SG. Glucocorticoids and fetal programming part 1: outcomes. Nat Rev Endocrinol. 2014; 10(7), 391402.CrossRefGoogle ScholarPubMed
Vieau, D, Sebaai, N, Léonhardt, M, et al. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology. 2007; 32 Suppl 1, S16S20.CrossRefGoogle ScholarPubMed
Sullivan, EL, Riper, KM, Lockard, R, Valleau, JC. Maternal high-fat diet programming of the neuroendocrine system and behavior. Horm Behav. 2015; 76(Suppl. 1), 153161.CrossRefGoogle ScholarPubMed
Kajantie, E, Feldt, K, Räikkönen, K, et al. Body size at birth predicts hypothalamic-pituitary-adrenal axis response to psychosocial stress at age 60 to 70 years. J Clin Endocrinol Metab. 2007; 92(11), 40944100.CrossRefGoogle ScholarPubMed
Krishnaveni, GV, Srinivasan, K. Maternal nutrition and offspring stress response-implications for future development of non-communicable disease: a perspective from India. Front Psychiatry. 2019; 10, 795.CrossRefGoogle ScholarPubMed
Jones, A, Godfrey, KM, Wood, P, Osmond, C, Goulden, P, Phillips, DI. Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab. 2006; 91(5), 18681871.CrossRefGoogle ScholarPubMed
Nazzari, S, Fearon, P, Rice, F, et al. Beyond the HPA-axis: exploring maternal prenatal influences on birth outcomes and stress reactivity. Psychoneuroendocrinology. 2019; 101(10), 253262.CrossRefGoogle ScholarPubMed
Laurent, H. Early calibration of the HPA axis by maternal psychopathology. Psychoneuroendocrinology. 2017; 78, 177184.CrossRefGoogle ScholarPubMed
Davis, EP, Waffarn, F, Sandman, CA. Prenatal treatment with glucocorticoids sensitizes the hpa axis response to stress among full-term infants. Dev Psychobiol. 2011; 53(2), 175183.CrossRefGoogle ScholarPubMed
Hami, J, Sadr-Nabavi, A, Sankian, M, Balali-Mood, M, Haghir, H. The effects of maternal diabetes on expression of insulin-like growth factor-1 and insulin receptors in male developing rat hippocampus. Brain Struct Funct. 2013; 218(1), 7384.CrossRefGoogle ScholarPubMed
Piazza, FV, Segabinazi, E, de Meireles, ALF, et al. Severe uncontrolled maternal hyperglycemia induces microsomia and neurodevelopment delay accompanied by apoptosis, cellular survival, and neuroinflammatory deregulation in rat offspring hippocampus. Cell Mol Neurobiol. 2019; 39(3), 401414.CrossRefGoogle ScholarPubMed
Jacobson, L, Sapolsky, R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev. 1991; 12(2), 118134.CrossRefGoogle ScholarPubMed
Jack-Roberts, C, Maples, P, Kalkan, B, et al. Gestational diabetes status and dietary intake modify maternal and cord blood allostatic load markers. BMJ Open Diabetes Res Care. 2020; 8(1), e001468.CrossRefGoogle ScholarPubMed
Chen, L, Guilmette, J, Luo, ZC, et al. Placental 11β-HSD2 and cardiometabolic health indicators in infancy. Diabetes Care. 2019; 42(5), 964971.CrossRefGoogle ScholarPubMed
Berglund, SK, García-Valdés, L, Torres-Espinola, FJ, et al. Maternal, fetal and perinatal alterations associated with obesity, overweight and gestational diabetes: an observational cohort study (PREOBE). BMC Public Health. 2016; 16(1), 207.CrossRefGoogle ScholarPubMed
Ma, R, Liu, J, Wu, L, et al. Differential expression of placental 11β-hydroxysteroid dehydrogenases in pregnant women with diet-treated gestational diabetes mellitus. Steroids. 2012; 77(7), 798805.CrossRefGoogle ScholarPubMed
Van Dam, JM, Garrett, AJ, Schneider, LA, et al. Reduced cortical excitability, neuroplasticity, and salivary cortisol in 11-13-year-old children born to women with gestational diabetes mellitus. EBioMedicine. 2018; 31(1), 143149.CrossRefGoogle ScholarPubMed
Krishnaveni, GV, Veena, SR, Jones, A, et al. Exposure to maternal gestational diabetes is associated with higher cardiovascular responses to stress in adolescent indians. J Clin Endocrinol Metab. 2015; 100(3), 986993.CrossRefGoogle ScholarPubMed
Mina, TH, Lahti, M, Drake, AJ, et al. Maternal lipids in pregnancy are associated with increased offspring cortisol reactivity in childhood. Psychoneuroendocrinology. 2017; 83(2), 7983.CrossRefGoogle ScholarPubMed
Oken, E, Baccarelli, AA, Gold, DR, et al. Cohort profile: Project Viva. Int J Epidemiol. 2015; 44(1), 3748.CrossRefGoogle ScholarPubMed
Loussouarn, G. African hair growth parameters. Br J Dermatol. 2001; 145(2), 294297.CrossRefGoogle ScholarPubMed
Guillemette, L, Allard, C, Lacroix, M, et al. Genetics of Glucose regulation in Gestation and Growth (Gen3G): a prospective prebirth cohort of mother-child pairs in Sherbrooke, Canada. BMJ Open. 2016; 6(2), e010031.CrossRefGoogle ScholarPubMed
Carpenter, MW, Coustan, DR. Criteria for screening tests for gestational diabetes. Am J Obstet Gynecol. 1982; 144(7), 768773.CrossRefGoogle ScholarPubMed
Metzger, BE, Gabbe, SG, Persson, B, et al. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care. 2010; 33(3), 676682.CrossRefGoogle ScholarPubMed
Huh, SY, Andrew, R, Rich-Edwards, JW, Kleinman, KP, Seckl, JR, Gillman, MW. Association between umbilical cord glucocorticoids and blood pressure at age 3 years. BMC Med. 2008; 6(1), 25.CrossRefGoogle ScholarPubMed
Petimar, J, Rifas-Shiman, SL, Hivert, MF, Fleisch, AF, Tiemeier, H, Oken, E. Childhood hair cortisol concentration and early teen cardiometabolic outcomes. Pediatr Obes. 2020; 15(3), e12592.CrossRefGoogle Scholar
Petimar, J, Rifas-Shiman, SL, Hivert, MF, Fleisch, AF, Tiemeier, H, Oken, E. Prenatal and childhood predictors of hair cortisol concentration in mid-childhood and early adolescence. PLoS One. 2020; 15(2), e0228769.CrossRefGoogle ScholarPubMed
Gao, W, Stalder, T, Foley, P, Rauh, M, Deng, H, Kirschbaum, C. Quantitative analysis of steroid hormones in human hair using a column-switching LC-APCI-MS/MS assay. J Chromatogr B Analyt Technol Biomed Life Sci. 2013; 928(7), 18.CrossRefGoogle ScholarPubMed
Russell, E, Koren, G, Rieder, M, Van Uum, S. Hair cortisol as a biological marker of chronic stress: current status, future directions and unanswered questions. Psychoneuroendocrinology. 2012; 37(5), 589601.CrossRefGoogle ScholarPubMed
Cohen, S, Schwartz, JE, Epel, E, Kirschbaum, C, Sidney, S, Seeman, T. Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) study. Psychosom Med. 2006; 68(1), 4150.CrossRefGoogle ScholarPubMed
Castro-Diehl, C, Diez Roux, AV, Seeman, T, Shea, S, Shrager, S, Tadros, S. Associations of socioeconomic and psychosocial factors with urinary measures of cortisol and catecholamines in the Multi-Ethnic Study of Atherosclerosis (MESA). Psychoneuroendocrinology. 2014; 41, 132141.CrossRefGoogle ScholarPubMed
Liao, J, Brunner, EJ, Kumari, M. Is there an association between work stress and diurnal cortisol patterns? Findings from the Whitehall II study. PLoS One. 2013; 8(12), e81020.CrossRefGoogle ScholarPubMed
Bleker, LS, Roseboom, TJ, Vrijkotte, TG, Reynolds, RM, de Rooij, SR. Determinants of cortisol during pregnancy - the ABCD cohort. Psychoneuroendocrinology. 2017; 83(2), 172181.CrossRefGoogle ScholarPubMed
Gray, NA, Dhana, A, Van Der Vyver, L, Van Wyk, J, Khumalo, NP, Stein, DJ. Determinants of hair cortisol concentration in children: a systematic review. Psychoneuroendocrinology. 2018; 87(3–4), 204214.CrossRefGoogle ScholarPubMed
Rosmalen, JG, Oldehinkel, AJ, Ormel, J, de Winter, AF, Buitelaar, JK, Verhulst, FC. Determinants of salivary cortisol levels in 10-12 year old children; a population-based study of individual differences. Psychoneuroendocrinology. 2005; 30(5), 483495.CrossRefGoogle ScholarPubMed
Yuan, YC. Multiple imputation for missing data: concepts and new development. In: Proceedings of the Twenty-Fifth Annual SAS Users Group International Conference, 2000, Cary (NC).Google Scholar
Puhakka, IJA, Peltola, MJ. Salivary cortisol reactivity to psychological stressors in infancy: a meta-analysis. Psychoneuroendocrinology. 2020; 115(12), 104603.CrossRefGoogle ScholarPubMed
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