Skip to main content Accessibility help
×
Home
Hostname: page-component-568f69f84b-4g88t Total loading time: 0.192 Render date: 2021-09-18T08:52:17.724Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Digit ratio, a proposed marker of the prenatal hormone environment, is not associated with prenatal sex steroids, anogenital distance, or gender-typed play behavior in preschool age children

Published online by Cambridge University Press:  18 December 2020

Emily Barrett*
Affiliation:
Department of Biostatistics and Epidemiology, Rutgers School of Public Health, Piscataway, NJ, USA Environmental and Occupational Health Sciences Institute, Rutgers University, Piscataway, NJ, USA
Sally W. Thurston
Affiliation:
Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
Donald Harrington
Affiliation:
Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
Nicole R. Bush
Affiliation:
Departments of Psychiatry and Pediatrics, University of California, San Francisco School of Medicine, San Francisco, CA, USA
Sheela Sathyanarayana
Affiliation:
Department of Pediatrics, University of Washington, Seattle, WA, USA Center for Child Health, Behavior and Development, Seattle Children’s Research Institute, Seattle, WA, USA
Ruby Nguyen
Affiliation:
Division of Epidemiology and Community Health, University of Minnesota School of Public Health, Minneapolis, MN, USA
Alexis Zavez
Affiliation:
Department of Biostatistics and Computational Biology, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA
Christina Wang
Affiliation:
Lundquist Institute, Harbor-UCLA Medical Center, Los Angeles, CA, USA
Shanna Swan
Affiliation:
Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA
*Corresponding
*Address for correspondence: Emily Barrett, Environmental and Occupational Health Sciences Institute (EOHSI), Rutgers School of Public Health, 170 Frelinghuysen Rd., Piscataway, NJ 08854, USA. Email: emily.barrett@eohsi.rutgers.edu

Abstract

Prenatal hormones have been proposed as key factors impacting child development as well as long-term health and disease. Digit ratio (the ratio of the lengths of the second to fourth digits; 2D:4D) has been proposed as a sexually dimorphic, noninvasive marker of prenatal androgen exposure that can be reliably measured in children and adults. To date, few longitudinal pregnancy cohort studies have examined childhood digit ratio in relation to other relevant measures including prenatal hormones and androgen-sensitive outcomes. To augment the current literature on this topic, we measured right-hand digit ratio in 4-year-old children participating in The Infant Development and the Environment Study, a multicenter longitudinal cohort study that has been following mother–child dyads since the first trimester of pregnancy (n = 321). We assessed sex differences in digit ratio and fit multivariable linear regression models to examine digit ratio in relation to: (1) child sex; (2) maternal sex steroid hormone concentrations in early pregnancy; (3) newborn anogenital distance, another proposed measure of sensitivity to prenatal androgens; and (4) gender-typical play behavior as measured by the Preschool Activities Inventory (PSAI) at age 4. We observed no sex difference in digit ratio; the mean 2D:4D was 0.97 ± 0.05 mm in both sexes. Furthermore, digit ratio was not associated with maternal sex steroid concentrations in early pregnancy, anogenital distance in either sex, or PSAI scores in either sex in covariate-adjusted models. In conclusion, we observed no evidence that early childhood digit ratio was associated with child sex or hormone-sensitive measures in this cohort.

Type
Original Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Schooling, CM, Houghton, LC, Terry, MB. Potential intervention targets in utero and early life for prevention of hormone related cancers. Pediatrics. 2016; 138(Suppl 1), S22S33.CrossRefGoogle ScholarPubMed
Hines, M. Human gender development. Neurosci Biobehav Rev. 2020; 118, 8996.CrossRefGoogle ScholarPubMed
Nattero-Chávez, L, Luque-Ramírez, M, Escobar-Morreale, HF. Systemic endocrinopathies (thyroid conditions and diabetes): impact on postnatal life of the offspring. Fertil Steril. 2019; 111(6), 10761091.CrossRefGoogle ScholarPubMed
Schepanski, S, Buss, C, Hanganu-Opatz, IL, Arck, PC. Prenatal immune and endocrine modulators of offspring’s brain development and cognitive functions later in life. Front Immunol. 2018; 9, 2186.CrossRefGoogle ScholarPubMed
Auyeung, B, Ahluwalia, J, Thomson, L, et al. Prenatal versus postnatal sex steroid hormone effects on autistic traits in children at 18 to 24 months of age. Mol Autism. 2012; 3(1), 17.CrossRefGoogle ScholarPubMed
Sarkar, P, Bergman, K, O’Connor, TG, Glover, V. Maternal antenatal anxiety and amniotic fluid cortisol and testosterone: possible implications for foetal programming. J Neuroendocrinol. 2008; 20(4), 489496.CrossRefGoogle ScholarPubMed
O’Connor, TG, Barrett, ES. Mechanisms of prenatal programing: identifying and distinguishing the impact of steroid hormones. Front Endocrinol (Lausanne). 2014; 5, 52.Google ScholarPubMed
de Sanctis, V, Soliman, AT, Elsedfy, H, Soliman, N, Elalaily, R, Di Maio, S. Is the second to fourth digit ratio (2d:4d) a biomarker of sex-steroids activity? Pediatr Endocrinol Rev. 2017; 14(4), 378386.Google ScholarPubMed
Abbott, AD, Colman, RJ, Tiefenthaler, R, Dumesic, DA, Abbott, DH. Early-to-mid gestation fetal testosterone increases right hand 2D:4D finger length ratio in polycystic ovary syndrome-like monkeys. PLoS One. 2012; 7(8), e42372.CrossRefGoogle ScholarPubMed
Talarovicová, A, Krsková, L, Blazeková, J. Testosterone enhancement during pregnancy influences the 2D:4D ratio and open field motor activity of rat siblings in adulthood. Horm Behav. 2009; 55(1), 235239.CrossRefGoogle ScholarPubMed
Zheng, Z, Cohn, MJ. Developmental basis of sexually dimorphic digit ratios. Proc Natl Acad Sci USA. 2011; 108(39), 1628916294.CrossRefGoogle ScholarPubMed
Berenbaum, SA, Bryk, KK, Nowak, N, Quigley, CA, Moffat, S. Fingers as a marker of prenatal androgen exposure. Endocrinology. 2009; 150(11), 51195124.CrossRefGoogle ScholarPubMed
Brown, WM, Hines, M, Fane, BA, Breedlove, SM. Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Horm Behav. 2002; 42(4), 380386.CrossRefGoogle ScholarPubMed
Manning, JT, Kilduff, LP, Trivers, R. Digit ratio (2D:4D) in Klinefelter’s syndrome. Andrology. 2013; 1(1), 9499.CrossRefGoogle Scholar
van Hemmen, J, Cohen-Kettenis, PT, Steensma, TD, Veltman, DJ, Bakker, J. Do sex differences in CEOAEs and 2D:4D ratios reflect androgen exposure? A study in women with complete androgen insensitivity syndrome. Biol Sex Differ. 2017; 8, 11.CrossRefGoogle ScholarPubMed
Rivas, MP, Moreira, LM, Santo, LD, Marques, AC, El-Hani, CN, Toralles, MB. New studies of second and fourth digit ratio as a morphogenetic trait in subjects with congenital adrenal hyperplasia. Am J Hum Biol. 2014; 26(4), 559561.CrossRefGoogle ScholarPubMed
Bunevicius, A. The association of digit ratio (2D:4D) with cancer: a systematic review and meta-analysis. Dis Markers. 2018; 2018, 7698193.CrossRefGoogle ScholarPubMed
Manning, JT, Bundred, PE, Kasielska-Trojan, A, Smith-Straney, T, Mason, L. Digit ratio (2D:4D), myocardial infarction and fibrinogen in men. Early Hum Dev. 2019; 133, 1822.CrossRefGoogle Scholar
Wang, L, Huo, Z, Lu, H, Bai, C, Li, K, Ma, W. Digit ratio (2D:4D) and coronary artery disease in north Chinese women. Early Hum Dev. 2018; 116, 6467.CrossRefGoogle ScholarPubMed
Kim, TB, Kim, KH. Why is digit ratio correlated to sports performance? J Exerc Rehabil. 2016; 12(6), 515519.CrossRefGoogle ScholarPubMed
Frick, NA, Hull, MJ, Manning, JT, Tomkinson, GR. Relationships between digit ratio (2D:4D) and basketball performance in Australian men. Am J Hum Biol. 2017; 29(3). doi: 10.1002/ajhb.22937 CrossRefGoogle ScholarPubMed
Xu, Y, Zheng, Y. The relationship between digit ratio (2D:4D) and sexual orientation in men from China. Arch Sex Behav. 2016; 45(3), 735741.CrossRefGoogle ScholarPubMed
Martin, JT, Puts, DA, Breedlove, SM. Hand asymmetry in heterosexual and homosexual men and women: relationship to 2D:4D digit ratios and other sexually dimorphic anatomical traits. Arch Sex Behav. 2008; 37(1), 119132.CrossRefGoogle ScholarPubMed
Aycinena, D, Rentschler, L. Discounting and digit ratio: low 2D:4D predicts patience for a sample of females. Front Behav Neurosci. 2017; 11, 257.CrossRefGoogle ScholarPubMed
Neyse, L, Bosworth, S, Ring, P, Schmidt, U. Overconfidence, incentives and digit ratio. Sci Rep. 2016; 6, 23294.CrossRefGoogle ScholarPubMed
Richards, G, Gomes, M, Ventura, T. Testosterone measured from amniotic fluid and maternal plasma shows no significant association with directional asymmetry in newborn digit ratio (2D:4D). J Dev Orig Health Dis. 2019; 10(3), 362367.CrossRefGoogle Scholar
Ventura, T, Gomes, MC, Pita, A, Neto, MT, Taylor, A. Digit ratio (2D:4D) in newborns: influences of prenatal testosterone and maternal environment. Early Hum Dev. 2013; 89(2), 107112.CrossRefGoogle ScholarPubMed
Lutchmaya, S, Baron-Cohen, S, Raggatt, P, Knickmeyer, R, Manning, JT. 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Hum Dev. 2004; 77(1–2), 2328.CrossRefGoogle ScholarPubMed
Mitsui, T, Araki, A, Imai, A, et al. Effects of prenatal Leydig cell function on the ratio of the second to fourth digit lengths in school-aged children. PLoS One. 2015; 10(3), e0120636.CrossRefGoogle ScholarPubMed
Hollier, LP, Keelan, JA, Jamnadass, ES, Maybery, MT, Hickey, M, Whitehouse, AJ. Adult digit ratio (2D:4D) is not related to umbilical cord androgen or estrogen concentrations, their ratios or net bioactivity. Early Hum Dev. 2015; 91(2), 111117.CrossRefGoogle ScholarPubMed
Hickey, M, Doherty, DA, Hart, R, et al. Maternal and umbilical cord androgen concentrations do not predict digit ratio (2D:4D) in girls: a prospective cohort study. Psychoneuroendocrinology. 2010; 35(8), 12351244.CrossRefGoogle Scholar
Barrett, ES, Mbowe, O, Thurston, SW, et al. Predictors of steroid hormone concentrations in early pregnancy: results from a multi-center cohort. Matern Child Health J. 2019; 23(3), 397407.CrossRefGoogle ScholarPubMed
Sathyanarayana, S, Grady, R, Redmon, JB, et al. Anogenital distance and penile width measurements in The Infant Development and the Environment Study (TIDES): methods and predictors. J Pediatr Urol. 2015; 11(2), 76.e176.e6.CrossRefGoogle ScholarPubMed
Mack, LA, Lay, DC Jr., Eicher, SD, Johnson, AK, Richert, BT, Pajor, EA. Growth and reproductive development of male piglets are more vulnerable to midgestation maternal stress than that of female piglets. J Anim Sci. 2014; 92(2), 530548.CrossRefGoogle ScholarPubMed
Bánszegi, O, Altbäcker, V, Dúcs, A, Bilkó, A. Testosterone treatment of pregnant rabbits affects sexual development of their daughters. Physiol Behav. 2010; 101(4), 422427.CrossRefGoogle ScholarPubMed
Ophir, AG, Delbarco-Trillo, J. Anogenital distance predicts female choice and male potency in prairie voles. Physiol Behav. 2007; 92(3), 533540.CrossRefGoogle ScholarPubMed
Hotchkiss, AK, Vandenbergh, JG. The anogenital distance index of mice (Mus musculus domesticus): an analysis. Contemp Top Lab Anim Sci. 2005; 44(4), 4648.Google ScholarPubMed
van den Driesche, S, Kilcoyne, KR, Wagner, I, et al. Experimentally induced testicular dysgenesis syndrome originates in the masculinization programming window. JCI Insight. 2017; 2(6), e91204.CrossRefGoogle ScholarPubMed
Foster, PM. Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. Int J Androl. 2006; 29(1), 140147.CrossRefGoogle ScholarPubMed
Cobb, J, Duboule, D. Comparative analysis of genes downstream of the Hoxd cluster in developing digits and external genitalia. Development. 2005; 132(13), 30553067.CrossRefGoogle ScholarPubMed
Mortlock, DP, Innis, JW. Mutation of HOXA13 in hand-foot-genital syndrome. Nat Genet. 1997; 15(2), 179180.CrossRefGoogle ScholarPubMed
Dean, A, Sharpe, RM. Clinical review: anogenital distance or digit length ratio as measures of fetal androgen exposure: relationship to male reproductive development and its disorders. J Clin Endocrinol Metab. 2013; 98(6), 22302238.CrossRefGoogle ScholarPubMed
Arbuckle, TE, Agarwal, A, MacPherson, SH, et al. Prenatal exposure to phthalates and phenols and infant endocrine-sensitive outcomes: the MIREC study. Environ Int. 2018; 120, 572583.CrossRefGoogle ScholarPubMed
Auyeung, B, Baron-Cohen, S, Ashwin, E, et al. Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychol Sci. 2009; 20(2), 144148.CrossRefGoogle ScholarPubMed
Hines, M. Prenatal testosterone and gender-related behaviour. Eur J Endocrinol. 2006; 155(Suppl 1), S115S121.CrossRefGoogle ScholarPubMed
Pellis, SM. Sex differences in play fighting revisited: traditional and nontraditional mechanisms of sexual differentiation in rats. Arch Sex Behav. 2002; 31(1), 1726.CrossRefGoogle ScholarPubMed
Goy, RW, Bercovitch, FB, McBrair, MC. Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm Behav. 1988; 22(4), 552571.CrossRefGoogle ScholarPubMed
Körner, LM, Schaper, ML, Pause, BM, Heil, M. Parent-reports of sex-typed play preference in preschool children: relationships to 2D:4D digit ratio and older siblings’ sex. Arch Sex Behav. 2020; 49(7), 27152724.CrossRefGoogle ScholarPubMed
Wong, WI, Hines, M. Interpreting digit ratio (2D:4D)-behavior correlations: 2D:4D sex difference, stability, and behavioral correlates and their replicability in young children. Horm Behav. 2016; 78, 8694.CrossRefGoogle ScholarPubMed
Mitsui, T, Araki, A, Miyashita, C, et al. The relationship between the second-to-fourth digit ratio and behavioral sexual dimorphism in school-aged children. PLoS One. 2016; 11(1), e0146849.CrossRefGoogle ScholarPubMed
Honekopp, J, Thierfelder, C. Relationships between digit ratio (2D:4D) and sex-typed play behavior in pre-school children. Pers Individ Differ. 2009; 47, 706710.CrossRefGoogle Scholar
Barrett, ES, Sathyanarayana, S, Janssen, S, et al. Environmental health attitudes and behaviors: findings from a large pregnancy cohort study. Eur J Obstetr Gynecol Reprod Biol. 2014; 176, 119125.CrossRefGoogle ScholarPubMed
Golombok, S, Rust, J. The measurement of gender role behaviour in pre-school children: a research note. J Child Psychol Psychiatry. 1993; 34(5), 805811.CrossRefGoogle ScholarPubMed
Sathyanarayana, S, Butts, S, Wang, C, et al. Early prenatal phthalate exposure, sex steroid hormones, and birth outcomes. J Clin Endocrinol Metab. 2017; 102(6), 18701878.CrossRefGoogle ScholarPubMed
Qoubaitary, A, Meriggiola, C, Ng, CM, et al. Pharmacokinetics of testosterone undecanoate injected alone or in combination with norethisterone enanthate in healthy men. J Androl. 2006; 27(6), 853867.CrossRefGoogle ScholarPubMed
WHO. WHO Child Growth Standards: Growth Velocity Based on Weight, Length, and Head Circumference, 2009. Geneva, Switzerland: WHO Press.Google Scholar
Swan, SH, Sathyanarayana, S, Barrett, ES, et al. First trimester phthalate exposure and anogenital distance in newborns. Human Reprod (Oxford, Engl). 2015; 30(4), 963972.CrossRefGoogle ScholarPubMed
Manning, JT, Scutt, D, Wilson, J, Lewis-Jones, DI. The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reprod (Oxford, Engl). 1998; 13(11), 30003004.CrossRefGoogle ScholarPubMed
Scutt, D, Manning, JT. Symmetry and ovulation in women. Human Reprod (Oxford, Engl). 1996; 11(11), 24772480.CrossRefGoogle ScholarPubMed
Barrett, ES, Redmon, JB, Wang, C, Sparks, A, Swan, SH. Exposure to prenatal life events stress is associated with masculinized play behavior in girls. Neurotoxicology. 2014; 41, 2027.CrossRefGoogle ScholarPubMed
Swan, SH, Liu, F, Hines, M, et al. Prenatal phthalate exposure and reduced masculine play in boys. Int J Androl. 2010; 33(2), 259269.CrossRefGoogle ScholarPubMed
Manning, JT, Fink, B. Sexual dimorphism in the ontogeny of second (2D) and fourth (4D) digit lengths, and digit ratio (2D:4D). Am J Hum Biol. 2018; 30(4), e23138.CrossRefGoogle Scholar
Mitsui, T, Araki, A, Goudarzi, H, et al. Effects of adrenal androgens during the prenatal period on the second to fourth digit ratio in school-aged children. Steroids. 2016; 113, 4651.CrossRefGoogle ScholarPubMed
Slama, N, Warner, M, Mocarelli, P, Brambilla, P, Eskenazi, B. The 2nd to 4th digit length ratio (2D:4D) among children of Seveso women exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Early Hum Dev. 2019; 131, 4550.CrossRefGoogle ScholarPubMed
Knickmeyer, RC, Woolson, S, Hamer, RM, Konneker, T, Gilmore, JH. 2D:4D ratios in the first 2 years of life: Stability and relation to testosterone exposure and sensitivity. Horm Behav. 2011; 60(3), 256263.CrossRefGoogle ScholarPubMed
McIntyre, MH, Cohn, BA, Ellison, PT. Sex dimorphism in digital formulae of children. Am J Phys Anthropol. 2006; 129(1), 143150.CrossRefGoogle ScholarPubMed
McIntyre, MH. The use of digit ratios as markers for perinatal androgen action. Reprod Biol Endocrinol. 2006; 4, 10.CrossRefGoogle ScholarPubMed
Trivers, R, Manning, J, Jacobson, A. A longitudinal study of digit ratio (2D:4D) and other finger ratios in Jamaican children. Horm Behav. 2006; 49(2), 150156.CrossRefGoogle ScholarPubMed
Velez, MP, Arbuckle, TE, Monnier, P, Fraser, WD. Is maternal periconceptional smoking associated with 2D:4D digit ratio in their children? J Dev Orig Health Dis. 2017; 8(5), 597603.CrossRefGoogle ScholarPubMed
Da Silva, S, Moreira, B, Da Costa, N Jr. 2D:4D digit ratio predicts delay of gratification in preschoolers. PLoS One. 2014; 9(12), e114394.CrossRefGoogle ScholarPubMed
Saenz, J, Alexander, GM. Digit ratios (2D:4D), postnatal testosterone and eye contact in toddlers. Biol Psychol. 2013; 94(1):106108.CrossRefGoogle Scholar
Allaway, HC, Bloski, TG, Pierson, RA, Lujan, ME. Digit ratios (2D:4D) determined by computer-assisted analysis are more reliable than those using physical measurements, photocopies, and printed scans. Am J Hum Biol. 2009; 21(3), 365370.CrossRefGoogle ScholarPubMed
Caswell, N, Manning, JT. A comparison of finger 2D:4D by self-report direct measurement and experimenter measurement from photocopy: methodological issues. Arch Sex Behav. 2009; 38(1), 143148.CrossRefGoogle ScholarPubMed
Manning, JT, Fink, B, Neave, N, Caswell, N. Photocopies yield lower digit ratios (2D:4D) than direct finger measurements. Arch Sex Behav. 2005; 34(3), 329333.CrossRefGoogle ScholarPubMed
Galis, F, Ten Broek, CM, Van Dongen, S, Wijnaendts, LC. Sexual dimorphism in the prenatal digit ratio (2D:4D). Arch Sex Behav. 2010; 39(1), 5762.CrossRefGoogle Scholar
Jain, VG, Goyal, V, Chowdhary, V, et al. Anogenital distance is determined during early gestation in humans. Human Reprod (Oxford, Engl). 2018; 33(9), 16191627.CrossRefGoogle ScholarPubMed
Kim, JH, Lee, YA, Lim, YH, et al. Changes in adrenal androgens and steroidogenic enzyme activities from ages 2, 4, to 6 years: a prospective cohort study. J Clin Endocrinol Metab. 2020; 105(10), 32653272.CrossRefGoogle ScholarPubMed
Mouritsen, A, Søeborg, T, Hagen, CP, et al. Longitudinal changes in serum concentrations of adrenal androgen metabolites and their ratios by LC-MS/MS in healthy boys and girls. Clin Chim Acta. 2015; 450, 370375.CrossRefGoogle ScholarPubMed
Kuiri-Hänninen, T, Seuri, R, Tyrväinen, E, et al. Increased activity of the hypothalamic-pituitary-testicular axis in infancy results in increased androgen action in premature boys. J Clin Endocrinol Metab. 2011; 96(1), 98105.CrossRefGoogle ScholarPubMed
Kuiri-Hänninen, T, Kallio, S, Seuri, R, et al. Postnatal developmental changes in the pituitary-ovarian axis in preterm and term infant girls. J Clin Endocrinol Metab. 2011; 96(11), 34323439.CrossRefGoogle ScholarPubMed
Bergadá, I, Milani, C, Bedecarrás, P, et al. Time course of the serum gonadotropin surge, inhibins, and anti-Müllerian hormone in normal newborn males during the first month of life. J Clin Endocrinol Metab. 2006; 91(10), 40924098.CrossRefGoogle ScholarPubMed
Nishimura, Y, Moriya, K, Kobayashi, S, et al. Association between ESR1 polymorphisms and second to fourth digit ratio in school-aged children in the Hokkaido study. Steroids. 2019; 141, 5562.CrossRefGoogle ScholarPubMed
Nishimura, Y, Moriya, K, Kobayashi, S, et al. Association of exposure to prenatal phthalate esters and bisphenol A and polymorphisms in the ESR1 gene with the second to fourth digit ratio in school-aged children: data from the Hokkaido study. Steroids. 2020; 159, 108637.CrossRefGoogle ScholarPubMed
Barrett, ES, Sathyanarayana, S, Mbowe, O, et al. First-trimester urinary bisphenol A concentration in relation to anogenital distance, an androgen-sensitive measure of reproductive development, in infant girls. Environ Health Perspect. 2017; 125(7), 077008.CrossRefGoogle ScholarPubMed
Kuijper, EA, Ket, JC, Caanen, MR, Lambalk, CB. Reproductive hormone concentrations in pregnancy and neonates: a systematic review. Reprod Biomed Online. 2013; 27(1), 3363.CrossRefGoogle ScholarPubMed
Hickey, M, Hart, R, Keelan, JA. The relationship between umbilical cord estrogens and perinatal characteristics. Cancer Epidemiol Biomarkers Prev. 2014; 23(6), 946952.CrossRefGoogle ScholarPubMed
Clifton, VL, Bisits, A, Zarzycki, PK. Characterization of human fetal cord blood steroid profiles in relation to fetal sex and mode of delivery using temperature-dependent inclusion chromatography and principal component analysis (PCA). J Chromatogr B Analyt Technol Biomed Life Sci. 2007; 855(2), 249254.CrossRefGoogle Scholar
Percy, Z, Xu, Y, Sucharew, H, et al. Gestational exposure to phthalates and gender-related play behaviors in 8-year-old children: an observational study. Environ Health. 2016; 15(1), 87.CrossRefGoogle ScholarPubMed
Adgent, MA, Daniels, JL, Edwards, LJ, Siega-Riz, AM, Rogan, WJ. Early-life soy exposure and gender-role play behavior in children. Environ Health Perspect. 2011; 119(12), 18111816.CrossRefGoogle ScholarPubMed
Vreugdenhil, HJ, Slijper, FM, Mulder, PG, Weisglas-Kuperus, N. Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age. Environ Health Perspect. 2002; 110(10), A593A598.CrossRefGoogle ScholarPubMed
Pasterski, VL, Geffner, ME, Brain, C, Hindmarsh, P, Brook, C, Hines, M. Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Dev. 2005; 76(1), 264278.CrossRefGoogle ScholarPubMed
Berenbaum, SA, Hines, M. Early androgens are related to childhood sex-typed toy preferences. Psychol Sci. 1992; 3, 203206.CrossRefGoogle Scholar
Mitsui, T, Araki, A, Miyashita, C, et al. Effects of prenatal sex hormones on behavioral sexual dimorphism. Pediatr Int. 2019; 61(2), 140146.CrossRefGoogle ScholarPubMed
Uludag, A, Tekin, M, Ertekin, YH, et al. Second to fourth digit ratio, sex differences and antropometric measuments: their relationship in children. Minerva Pediatr. 2017; 69(2), 106112.Google ScholarPubMed
Supplementary material: File

Barrett et al. supplementary material

Tables S1-S4 and Figure S1

Download Barrett et al. supplementary material(File)
File 66 KB
3
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Digit ratio, a proposed marker of the prenatal hormone environment, is not associated with prenatal sex steroids, anogenital distance, or gender-typed play behavior in preschool age children
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Digit ratio, a proposed marker of the prenatal hormone environment, is not associated with prenatal sex steroids, anogenital distance, or gender-typed play behavior in preschool age children
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Digit ratio, a proposed marker of the prenatal hormone environment, is not associated with prenatal sex steroids, anogenital distance, or gender-typed play behavior in preschool age children
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *