Postnatal testosterone levels and disorder relevant behavior in the second year of life

Biological Psychology

Volumn 94, Issue 1, 2013, Pages 152-159

  Saenz, Janet ^a   Alexander, Gerianne M ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Postnatal androgens; Sex differences; Social emotional problems; Testosterone

Indexed keywords

TESTOSTERONE;

AGGRESSION; ARTICLE; AUTISM; BEHAVIOR DISORDER; BRIEF INFANT TODDLER SOCIAL AND EMOTIONAL ASSESSMENT; CHILD; CHILD BEHAVIOR; DISEASE ASSOCIATION; FEMALE; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; PERINATAL PERIOD; PLAY; PREDICTION; PRESCHOOL CHILD; PRIORITY JOURNAL; SALIVA ANALYSIS; SEX DIFFERENCE; TESTOSTERONE BLOOD LEVEL; VERBAL BEHAVIOR;

POSTNATAL ANDROGENS; SEX DIFFERENCES; SOCIAL-EMOTIONAL PROBLEMS; TESTOSTERONE;

AGE FACTORS; AGGRESSION; ANALYSIS OF VARIANCE; CHILD, PRESCHOOL; DEVELOPMENTAL DISABILITIES; FEMALE; FINGERS; HUMANS; INFANT; MALE; REGRESSION ANALYSIS; SALIVA; SEX CHARACTERISTICS; TESTOSTERONE; VERBAL BEHAVIOR;

EID: 84880393718     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2013.05.011     Document Type: Article

References (86)

1. A.P.A. DSM-IV diagnostic and statistical manual of mental disorders 1994, American Psychiatric Association, Washington, DC. 4th ed.
2. Alexander G.M., Saenz J. Postnatal testosterone levels and temperament in early infancy. Archives of Sexual Behavior 2011, 40:1287-1292.
3. Alexander G.M., Saenz J. Early androgens, activity levels and toy choices of children in the second year of life. Hormones and Behavior 2012, 62(4):500-504. 10.1016/j.yhbeh.2012.08.008.
4. Alexander G.M., Wilcox T., Farmer M.E. Hormone-behavior associations in early infancy. Hormones and Behavior 2009, 56:498-502.
5. Anders S.M.V., Hampson E. Testing the prenatal androgen hypothesis: Measuring digit ratios, sexual orientation, and spatial abilities in adults. Hormones and Behavior 2005, 47:92-98.
6. Andersson A.M., Toppari J., Haavisto A.M., Petersen J.H., Simell T., Simell O., et al. Longitudinal reproductive hormone profiles in infants: Peak of inhibin B levels in infant boys exceeds levels in adult men. Journal of Clinical Endocrinology and Metabolism 1998, 83(2):675-681.
7. Auyeung B., Ahluwalia J., Thomson L., Taylor K., Hackett G., O'Donnell K.J., et al. Prenatal versus postnatal sex steroid hormone effects on autistic traits in children at 18 to 24 months of age. Molecular Autism 2012, 3(1):17-21. 10.1186/2040-2392-3-17.
8. Auyeung B., Baron-Cohen S. Fetal testosterone in mind: Human sex differences and autism 2012, Vol. 1. Harvard University Press, Cambridge, MA, US.
9. Auyeung B., Baron-Cohen S., Wheelwright S., Allison C. The Autism Spectrum Quotient: Children's Version (AQ-Child). Journal of Autism and Developmental Disorders 2008, 38(7):1230-1240. 10.1007/s10803-007-0504-z.
10. Bailey A.A., Hurd P.L. Finger length ratio (2D:4D) correlates with physical aggression in men but not in woman. Biological Psychology 2005, 68:215-222. 10.1016/j.biopsycho.2004.05.001.
11. Baron-Cohen S. The extreme male brain theory of autism. Trends in Cognitive Science 2002, 6(6):248-254. 10.1037/0033-2909.85.4.845.
12. Baron-Cohen S. Empathizing, systemizing, and the extreme male brain theory of autism. Progress in brain research 2010, Vol. 186:167-175. Elsevier, Amsterdam, Netherlands.
13. Baron-Cohen S., Lombardo M.V., Auyeung B., Ashwin E., Chakrabarti B., Knickmeyer R. Why are autism spectrum conditions more prevalent in males?. PLoS Biology 2011, 9(6):1-10.
14. Benderlioglu Z., Nelson R.J. Digit length ratios predict reactive aggression in women, but not in men. Hormones and Behavior 2004, 46:558-564. 10.1016/j.yhbeh.2004.06.004.
15. Berenbaum S.A., Bryk K.K., Nowak N., Quigley C.A., Moffat S. Fingers as a marker of prenatal androgen exposure. Endocrinology 2009, 150(11):5119-5124. 10.1210/en.2009-0774.
16. Berenbaum S.A., Hines M. Early androgens are related to childhood sex-types toy preferences. Psychological Science 1992, 3(3):203-206.
17. Berenbaum S.A., Resnick S.M. Early androgen effects on aggression in children and adults with congenital adrenal hyperplasia. Psychoneuroendocrinology 1997, 22(7):505-515.
18. Bergman K., Glover V., Sarkar P., Abbott D.H., O'Connor T.G. In utero cortisol and testosterone exposure and fear reactivity in infancy. Hormones and Behavior 2010, 57:306-312.
19. Biederman J., Mick E., Faraone S.V., Braaten E., Doyle A., Spencer T., et al. Influence of gender on attention deficit hyperactivity disorder in children referred to a psychiatric clinic. American Journal of Psychiatry 2002, 159(1):36-42.
20. Breedlove S.M., Cooke B.M., Jordan C.L. The orthodox view of brain sexual differentiation. Brain, Behavior & Evolution 1999, 54(1):8-14.
21. Briggs-Gowan M.J., Carter A.S. Brief Infant-Toddler Social and Emotional Assessment (BITSEA) manual, version 2.0 2002, Yale University, New Haven, CT.
22. Briggs-Gowan M.J., Carter A.S. Social-emotional screening status in early childhood predicts elementary school outcomes. Pediatrics 2008, 121(5):957-962. 10.1542/peds.2007-1948.
23. Briggs-Gowan M.J., Carter A.S., Irwin J.R., Wachtel K., Cicchetti D.V. The Brief Infant-Toddler Social and Emotional Assessment: Screening for social-emotional problems and delays in competence. Journal of Pediatric Psychology 2004, 29(2):143.
24. Brown W.M., Hines M., Fane B.A., Breedlove S.M. Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Hormones and Behavior 2002, 42:380-386. 10.1006/hbeh.2002.1830.
25. Buck J.J., Williams R.M., Hughes I.A., Acerini C.L. In-utero androgen exposure and 2nd to 4th digit length ratio-Comparisons between healthy controls and females with classical congenital adrenal hyperplasia. Human Reproduction 2003, 18(5):976-979. 10.1093/humrep/deg198.
26. Butterworth G., Morissette P. Onset of pointing and the acquisition of language in infancy. Journal of Reproductive and Infant Psychology 1996, 14(3):219.
27. Chapman E., Baron-Cohen S., Auyeung B., Taylor K., Hackett G. Fetal testosterone and empathy: Evidence from the empathy quotient (EQ) and the "Reading the Mind in the Eyes" test. Society for Neuroscience 2006, 1(2):135-148.
28. Chellakootym M., Schmidt I.M., Haavisto A.M., Boisen K.A., Damgaard I.N., Mau C., et al. Inhibin A, inhibin B, follicle-stimulating hormone, luteinizing hormone, estradiol, and sex hormone-binding globulin levels in 473 healthy infant girls. Journal of Clinical Endocrinology and Metabolism 2003, 88(8):3515-3520.
29. Crawford E.D., Barqawi A.B., O'Donnell C., Morgentaler A. The association of time of day and serum testosterone concentration in a large screening population. BJU International 2007, 100(3):509-513.
30. de Bruin E.I., Verheij F., Wiegman T., Ferdinand R.F. Differences in finger length ratio between males with autism, pervasive developmental disorder-not otherwise specified, ADHD, and anxiety disorders. Developmental Medicine and Child Neurology 2006, 48(12):962.
31. de Ronde W., van der Schouw Y.T., Pierik F.H., Pols H.A.P., Muller M., Grobbee D.E., et al. Serum levels of sex hormone-binding globulin (SHBG) are not associated with lower levels of non-SHBG-bound testosterone in male newborns and healthy adult men. Clinical Endocrinology 2005, 62(4):498-503.
32. Engel S.M., Zhu C., Berkowitz G.S., Calafat A.M., Silva M.J., Miodovnik A., et al. Prenatal phthalate exposure and performance on the Neonatal Behavioral Assessment Scale in a multiethnic birth cohort. Neurotoxicology 2009, 30(4):522-528. 10.1016/j.neuro.2009.04.001.
33. Fenson L., Dale P.S., Reznick J.S., Bates E., Thal D.J., Pethick S.J. Variability in early communicative development. Monographs of the Society for Research in Child Development 1994, 59(5):1-173.
34. Fink B., Manning J.T., Williams J.H.G., Podmore-Nappin C. The 2nd to 4th digit ratio and developmental psychopathology in school-aged children. Personality and Individual Differences 2007, 42(2):369-379. 10.1016/j.paid.2006.07.018.
35. Forest M.G., de Peretti E., Bertrand J. Testicular and adrenal androgens and their binding to plasma proteins in the perinatal period: Developmental patterns of plasma testosterone, 4-androstenedione, dehydroepiandrosterone and its sulfate in premature and small for date infants as compared with that of full-term infants. Journal of Steroid Biochemistry 1980, 12(0):25-36. 10.1016/0022-4731(80)90247-2.
36. Forest M.G., Sizonenko F.C., Cathiard A.M., Bertrand J. Hypophyso-gonadal function in humans during the first year of life I. Evidence for testicular activity in early infancy. Journal of Clinical Investigation 1974, 53:819-828.
37. Friederici A.D., Pannekamp A., Partsch C.-J., Ulmen U., Oehler K., Schmutzler R., et al. Sex hormone testosterone affects language organization in the infant brain. NeuroReport 2008, 19(3):283-286.
38. Guatelli-Steinberg D., Boyce J. The postnatal endocrine surge and its effects on subsequent sexual growth. Handbook of growth and growth monitoring in health and disease 2012, Vol. 1:663-680. Springer, New York, NY.
39. Haapsamo H., Ebeling H., Soini H., Joskitt L., Larinen K., Penninkilampi-Kerola V., et al. Screening infants with social and emotional problems: A pilot study of the brief infant toddler social and emotional assessment (BITSEA) in Northern Finland. International Journal of Circumpolar Health 2009, 68(4):386.
40. Haapsamo H., Kuusikko-Gauffin S., Carter A.S., Pollock-Wurman R., Ebeling H., Joskitt L., et al. A pilot longitudinal follow-up study of the Brief Infant Toddler Social-Emotional Assessment (BITSEA) in Northern Finland: Examining toddlers' social-emotional, behavioural and communicative development. Early Child Development and Care 2011, 1-16. 10.1080/03004430.2011.622756.
41. Hartung C.M., Widiger T.A. Gender differences in the diagnosis of mental disorders: Conclusions and controversies of the DSM-IV. Psychological Bulletin 1998, 123(3):260.
42. Hines M. Sexual differentiation of the human brain and behavior. Hormones, Brain and Behavior 2002, Elsevier Science, San Diego. D.W. Pfaff, A.P. Arnold, A.M. Arnold, A.M. Etgen, S.E. Fahrback, R.T. Ruben (Eds.).
43. Hines M. Brain gender 2004, Oxford University Press, New York, NY, US.
44. Hines M., Kaufman F.R. Androgen and the development of human sex-typical behavior: Rough-and-tumble play and sex of preferred playmates in children with congenital adrenal hyperplasia (CAH). Child Development 1994, 65:1042-1053.
45. Hönekopp J., Bartholdt L., Beler L., Liebert A. Second to fourth digit length ratio (2D:4D) and adult sex hormone levels: New data and a meta-analytic review. Psychoneuroendocrinology 2007, 32(4):313-321. 10.1016/j.psyneuen.2007.01.007.
46. Hönekopp J., Thierfelder C. Relationships between digit ratio (2D:4D) and sex-typed play behavior in pre-school children. Personality and Individual Differences 2009, 47:706-710.
47. Huhtaniemi I.T., Dunkel L., Perheentupa J. The transient increase in postnatal testicular activity is not revealed by longitudinal measurements of salivary testosterone. Pediatric Research 1986, 20:1324-1327.
48. Karabekiroglu K., Briggs-Gowan M.J., Carter A.S., Rodopman-Arman A., Akbas S. The clinical validity and reliability of the Brief Infant-Toddler Social and Emotional Assessment (BITSEA). Infant Behavior and Development 2010, 33(4):503-509. 10.1016/j.infbeh.2010.07.001.
49. Karabekiroglu K., Rodopman-Arman A., Ay P., Ozkesen M., Akbas S., Tasdemir G.N., et al. The reliability and validity of the Turkish version of the brief infant-toddler social emotional assessment (BITSEA). Infant Behavior and Development 2009, 32(3):291-297. 10.1016/j.infbeh.2009.03.003.
50. Knickmeyer R., Baron-Cohen S., Fane B.A., Wheelwright S., Mathews G.A., Conway G.S., et al. Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia. Hormones and Behavior 2006, 50(1):148-153. 10.1016/j.yhbeh.2006.02.006.
51. Knickmeyer R., Baron-Cohen S., Raggatt P., Taylor K., Hackett G. Fetal testosterone and empathy. Hormones and Behavior 2006, 49(3):282-292.
52. Knickmeyer R., Woolson S., Hamer R.M., Konneker T., Gilmore J.H. 2D:4D ratios in the first 2 years of life: Stability and relation to testosterone exposure and sensitivity. Hormones and Behavior 2011, 60:256-263.
53. Kobrosly R.W., Parlett L.E., Stahlhut R.W., Barrett E.S., Swan S.H. Socioeconomic factors and phthalate metabolite concentrations among United States women of reproductive age. Environmental Research 2012, 115(0):11-17. 10.1016/j.envres.2012.03.008.
54. Koo J.-W., Parham F., Kohn M.C., Masten S.A., Brock J.W., Needham L.L., et al. The association between biomarker-based exposure estimates for phthalates and demographic factors in a human reference population. Environmental Health Perspectives 2002, 110(4.).
55. Kuiri-Hänninen T., Seuri R., Tyrväinen E., Turpeinen U., Hämäläinen E., Stenman U.-H.k., et al. Increased activity of the hypothalamic-pituitary-testicular axis in infancy results in increased androgen action in premature boys. Journal of Clinical Endocrinology and Metabolism 2011, 96(1):98.
56. Lamminmäki A., Hines M., Kuiri-Hänninen T., Kilpeläinen L., Dunkel L., Sankilampi U. Testosterone measured in infancy predicts subsequent sex-typed behavior in boys and in girls. Hormones and Behavior 2012, 61(4):611-616. 10.1016/j.yhbeh.2012.02.013.
57. Leveroni C.L., Berenbaum S.A. Early androgen effects on interest in infants: Evidence from children with congenital adrenal hyperplasia. Developmental Neuropsychology 1998, 14(2-3):321-340. 10.1080/87565649809540714.
58. Loeber R., Burke J.D., Lahey B.B., Winters A., Zera M. Oppositional defiant and conduct disorder: A review of the past 10 years, part I. Journal of the American Academy of Child & Adolescent Psychiatry 2000, 39(12):1468.
59. Lutchmaya S., Baron-Cohen S., Raggatt P. Foetal testosterone and eye contact in 12-month-old human infants. Infant Behavior and Development 2002, 25:327-335.
60. Lutchmaya S., Baron-Cohen S., Raggatt P. Foetal testosterone and vocabulary size in 18- and 24-month-old infants. Infant Behavior and Development 2002, 24:418-424.
61. Lutchmaya S., Baron-Cohen S., Raggatt P., Knickmeyer R., Manning J.T. 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Human Development 2004, 77:23-28.
62. Luxen M.F., Buunk B.P. Second-to-fourth digit ratio related to Verbal and Numerical Intelligence and the Big Five. Personality and Individual Differences 2005, 39:959-966. 10.1016/j.paid.2005.03.016.
63. Main K.M., Schmidt I.M., Skakkebæk N.E. A possible role for reproductive hormones in newborn boys: Progressive hypogonadism without the postnatal testosterone peak. Journal of Clinical Endocrinology and Metabolism 2000, 85(12):4905-4907. 10.1210/jc.85.12.4905.
64. Manning J.T., Baron-Cohen S., Wheelwright S., Sanders G. The 2nd to 4th ratio and autism. Developmental Medicine and Child Neurology 2001, 43(3):160-164.
65. Manning J.T., Bundred P.E., Newton D.J., Flanagan B.F. The second to fourth digit ratio and variation in the androgen receptor gene. Evolution and Human Behavior 2003, 24:399-405.
66. Martel M.M. Conscientiousness as a mediator of the association between masculinized finger-length ratios and attention-deficit/hyperactivity disorder (ADHD). Journal of Child Psychology and Psychiatry and Allied Disciplines 2009, 50(7):790-798.
67. McIntyre M.H., Alexander G.M. Sex differences in the fingers of 3 to 5 month old infants do not predict concurrent salivary testosterone levels. Early Human Development 2011, 87:349-351.
68. Meltzer H., Gatward R., Goodman R., Ford T. Mental health of children and adolescents in Great Britain. International Review of Psychiatry 2003, 15(1/2):185.
69. Merke D.P., Camacho C.A. Novel basic and clinical aspects of congenital adrenal hyperplasia. Reviews in Endocrine and Metabolic Disorders 2001, 2(3):289-296. 10.1023/a:1011520600476.
70. Milne E., White S., Campbell R., Swettenham J., Hansen P., Ramus F. Motion and form coherence detection in autistic spectrum disorder: relationship to motor control and 2:4 digit ratio. Journal of Autism and Developmental Disorders 2006, 36(2):225-237. 10.1007/s10803-005-0052-3.
71. Okten A., Kalyoncu M., Yaris N. The ratio of second- and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Human Development 2002, 70(1-2):47-54.
72. Pang S., Levine L.S., Cederqvist L.L., Fuentes M., Riccardi V., Holcombe M.J.H., et al. Amniotic fluid concentrations of delta-5 steroids and delta-4 steroids in fetuses with congenital adrenal hyperplasia due to 21 hydroxylase deficiency and anencephalic fetuses. Journal of Clinical Endocrinology and Metabolism 1980, 51(2):223.
73. Pasterski V., Geffner M.E., 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 Development 2005, 76:264-278.
74. Pasterski V., Mindmarsh P., Geffner M., Brook C., Brain C., Hines M. Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH). Hormones and Behavior 2007, 52:368-374.
75. Quinton S.J., Smith A.R., Joiner T. The 2nd to 4th digit ratio (2D:4D) and eating disorder diagnosis in women. Personality and Individual Differences 2011, 51(4):402-405. 10.1016/j.paid.2010.07.024.
76. Reinisch J.M. Prenatal exposure to synthetic progestins increases potential for aggression in humans. Science 1981, 211(13):1171-1173.
77. Schettler T.E.D. Human exposure to phthalates via consumer products. International Journal of Andrology 2006, 29(1):134-139. 10.1111/j.1365-2605.2005.00567.x.
78. Shaw D.S., Keenan K., Vondra J.I. Developmental precursors of externalizing behavior: Ages 1 to 3. Developmental Psychology 1994, 30(3):355-364.
79. Swan S.H., Liu F., Hines M., Kruse R.L., Wang C., Redmon J.B., et al. Prenatal phthalate exposure and reduced masculine play in boys. International Journal of Andrology 2010, 33(2):259-269.
80. Swan S.H., Main K.M., Liu F., Stewart S.L., Kruse R.L., Calafat A.M., et al. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environmental Health Perspectives 2005, 113(8.).
81. Tapanainen J., Koivisto M., Vihko R., Huhtaniemi I. Enhanced activity of the pituitary-gonadal axis in premature human infants. Journal of Clinical Endocrinology and Metabolism 1981, 52(2):235-238.
82. Venkatasubramanian G., Arasappa R., Rao N.P., Gangadhar B.N. Digit ratio (2D:4D) asymmetry and Schneiderian first rank symptoms: Implications for cerebral lateralisation theories of schizophrenia. Laterality 2011, 16(4):499.
83. Whitehouse A.J.O., Maybery M.T., Hart R., Mattes E., Newnham J.P., Sloboda D.M., et al. Fetal androgen exposure and pragmatic language ability of girls in middle childhood: Implications for the extreme male-brain theory of autism. Psychoneuroendocrinology 2010, 35:1259-1264.
84. Williams J.H.G., Greenhalgh K.D., Manning J.T. Second to fourth finger ratio and possible precursors of developmental psychopathology in preschool children. Early Human Development 2003, 72(1):57-65. 10.1016/S0378-3782(03)00012-4.
85. Zahn-Waxler C. Warriors and worriers: Gender and psychopathology. Development and Psychopathology 1993, 5(1-2):79.
86. Zucker K.J., Bradley S.J., Oliver G., Blake J., Fleming S., Hood J. Psychosexual development of women with congenital adrenal hyperplasia. Hormones and Behavior 1996, 30(4):300-318. 10.1006/hbeh.1996.0038.