Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-30T07:33:59.123Z Has data issue: false hasContentIssue false
  • English
  • Français

Association between a marker for prenatal testosterone exposure and externalizing behavior problems in children

Published online by Cambridge University Press:  02 July 2012

Jianghong Liu ,
Jill Portnoy  and
Adrian Raine
Jianghong Liu
Affiliation:
University of Pennsylvania
Jill Portnoy
Affiliation:
University of Pennsylvania
Adrian Raine*
Affiliation:
University of Pennsylvania
*
Address correspondence and reprint requests to: Adrian Raine, Departments of Criminology, Psychiatry, and Psychology, University of Pennsylvania, 3809 Walnut Street, Philadelphia, PA 19104; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Prenatal androgen exposure has been associated with aggressive behavior in adults. It is less clear whether this association holds for childhood externalizing behavior. This study tests the hypothesis that increased prenatal androgen exposure is associated with aggressive behavior and attention problems in childhood. The ratio of the length of the second finger digit relative to the fourth digit, which is a marker for prenatal testosterone exposure, was assessed in 239 male and female fifth grade schoolchildren from Jintan, China, together with parent and teacher ratings of aggression and attention problems. Increased aggression and attention problems were both significantly associated with a lower ratio of the length of the second finger digit relative to the fourth digit ratios in boys but not girls. The effects remained significant after controlling for early adversity. These findings are the first to establish a relationship between an indirect indicator of fetal androgen exposure and any child psychopathology in Chinese children, and the observed effect size in boys was stronger than in male adults in Western studies. The results provide limited cross-cultural support for the importance of prenatal androgen exposure in contributing to the development of externalizing behavior problems in children, and they suggest that such effects may be specific to boys who may be relatively more vulnerable to early prenatal influences.

Type
Articles
Information
Development and Psychopathology , Volume 24 , Issue 3: Multilevel Approaches Toward Understanding Antisocial Behavior: Current Research and Future Directions , August 2012 , pp. 771 - 782
Copyright
Copyright © Cambridge University Press 2012

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

Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18 and 1991 profile. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Achenbach, T. M., & Rescorla, L. (2000). Manual for the ASEBA Preschool Forms, & Profiles. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Archer, J. (2004). Sex differences in aggression in real-world settings: A meta-analytic review. Review of General Psychology, 8, 291–322.CrossRefGoogle Scholar
Austin, E. J., Manning, J. T., McInroy, K., & Mathews, E. (2002). A preliminary investigation of the associations between personality, cognitive ability and digit ratio. Personality and Individual Differences, 33, 1115–1124.CrossRefGoogle Scholar
Bailey, A. A., & Hurd, P. L. (2005). Finger length ratio (2D:4D) correlates with physical aggression in men but not in women. Biological Psychology, 68, 215–222.CrossRefGoogle Scholar
Benderlioglu, Z., & Nelson, R. J. (2004). Digit length ratios predict reactive aggression in women, but not in men. Hormones and Behavior, 46, 558–564.CrossRefGoogle Scholar
Berenbaum, S. A. (1999). Effects of early androgens on sex-typed activities and interests in adolescents with congenital adrenal hyperplasia. Hormones and Behavior, 35, 102–110.CrossRefGoogle ScholarPubMed
Berenbaum, S. A., & Resnick, S. M. (1997). Early androgen effects on aggression in children and adults with congenital adrenal hyperplasia. Psychoneuroendocrinology, 22, 505–515.CrossRefGoogle ScholarPubMed
Breedlove, S. M. (1994). Sexual differentiation of the human nervous system. Annual Review of Psychology, 45, 389–418.CrossRefGoogle ScholarPubMed
Brennan, P. A., Grekin, E. R., Mortensen, E. L., & Mednick, S. A. (2002). Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring. American Journal of Psychiatry, 159, 48–54.CrossRefGoogle ScholarPubMed
Brown, W. M., Hines, M., Fane, B. A., & Breedlove, S. M. (2002). Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Hormones and Behavior, 42, 380–386.CrossRefGoogle ScholarPubMed
Burriss, R. P., Little, A. C., & Nelson, E. C. (2007). 2D : 4D and sexually dimorphic facial characteristics. Archives of Sexual Behavior, 36, 377–384.CrossRefGoogle ScholarPubMed
Butovskaya, M. L., Burkova, V., & Mabulla, A. (2010). Sex differences in 2D : 4D ratio, aggression and conflict resolution in African children and adolescents: A cross-cultural study. Journal of Aggression, Conflict and Peace Research, 2, 17–31.CrossRefGoogle Scholar
Cicchetti, D. (2010). Resilience under conditions of extreme stress: A multilevel perspective. World Psychiatry, 9, 145–154.CrossRefGoogle Scholar
Cousins, A. J., Fugere, M. A., & Franklin, M. (2009). Digit ratio (2D:4D), mate guarding, and physical aggression in dating couples. Personality and Individual Differences, 46, 709–713.CrossRefGoogle Scholar
Coyne, S. M., Manning, J. T., Ringer, L., & Bailey, L. (2007). Directional asymmetry (right–left differences) in digit ratio (2D:4D) predict indirect aggression in women. Personality and Individual Differences, 43, 865–872.CrossRefGoogle Scholar
Csathó, Á., Osváth, A., Karádi, K., Bicsák, É., Manning, J., & Kállai, J. (2001). Spatial navigation related to the ratio of second to fourth digit length in women. Learning and Individual Differences, 13, 239–249.CrossRefGoogle Scholar
Dietrich, K. N., Ris, M. D., Succop, P. A., Berger, O. G., & Bornschein, R. L. (2001). Early exposure to lead and juvenile delinquency. Neurotoxicology and Teratology, 23, 511–518.CrossRefGoogle ScholarPubMed
Dogan, A., Barut, C., Konuk, N., & Bilge, Y. (2008). Relation of 2D : 4D ratio to aggression and anger. Neurology Psychiatry and Brain Research, 14, 151–158.Google Scholar
Ekblad, S. (1990). The Children's Behaviour Questionnaire for completion by parents and teachers in a Chinese sample. Journal of Child Psychology and Psychiatry, 31, 775–791.CrossRefGoogle Scholar
Fairchild, G., Passamonti, L., Hurford, G., Hagan, C. C., von dem Hagen, E. A., van Goozen, S. H., et al. (2011). Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. American Journal of Psychiatry, 168, 624–633.CrossRefGoogle ScholarPubMed
Fink, B., Manning, J. T., Williams, J. H. G., & Podmore-Nappin, C. (2007). The 2nd to 4th digit ratio and developmental psychopathology in school-aged children. Personality and Individual Differences, 42, 369–379.CrossRefGoogle Scholar
Finkelstein, J. W., Susman, E. J., Chinchilli, V., Schwab, J., Demers, L., Liben, L., et al. (1995). Testosterone (T) or conjugated estrogen (E) cause increases in aggressive behavior in hypogonadal boys or girls. Pediatric Research, 37, A88.Google Scholar
Gao, Y., Raine, A., Venables, P. H., Dawson, M. E., & Mednick, S. A. (2010). Association of poor childhood fear conditioning and adult crime. American Journal of Psychiatry, 167, 56–60.CrossRefGoogle ScholarPubMed
George, R. (1930). Human finger types. Anatomical Record, 46, 199–204.CrossRefGoogle Scholar
Geschwind, N., & Galaburda, A. M. (1985). Cerebral lateralization: Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Archives of Neurology, 42, 428–459.CrossRefGoogle Scholar
Giedd, J. N., Clasen, L. S., Lenroot, R., Greenstein, D., Wallace, G. L., Ordaz, S., et al. (2006). Puberty-related influences on brain development. Molecular and Cellular Endocrinology, 254, 154–162.CrossRefGoogle ScholarPubMed
Gobrogge, K. L., Breedlove, S. M., & Klump, K. L. (2008). Genetic and environmental influences on 2D : 4D finger length ratios: A study of monozygotic and dizygotic male and female twins. Archives of Sexual Behavior, 37, 112–118.CrossRefGoogle ScholarPubMed
Goodman, R. (1991). Developmental disorders and structural brain development. In Rutter, M. & Caesar, P. (Eds.), Biological risk factors for psychosocial disorders (pp. 20–49). Cambridge: Cambridge University Press.Google Scholar
Hampson, E., Ellis, C. L., & Tenk, C. M. (2008). On the relation between 2D : 4D and sex-dimorphic personality traits. Archives of Sexual Behavior, 37, 133–144.CrossRefGoogle ScholarPubMed
Harris, J. A., Rushton, J. P., Hampson, E., & Jackson, D. N. (1996). Salivary testosterone and self-report aggressive and pro-social personality characteristics in men and women. Aggressive Behavior, 22, 321–331.3.0.CO;2-M>CrossRefGoogle Scholar
Honekopp, J., & Watson, S. (2011). Meta-analysis of the relationship between digit-ratio 2D:4D and aggression. Personality and Individual Differences, 51, 381–386.CrossRefGoogle Scholar
Hyde, J. S. (1986). Gender differences in aggression. In Hyde, J. S. & Linn, M. C. (Eds.), The psychology of gender: Advances through meta-analysis (pp. 51–66). Baltimore, MD: Johns Hopkins University Press.Google Scholar
James, W. H. (2008). Further evidence that some male-based neurodevelopmental disorders are associated with high intrauterine testosterone concentrations. Developmental Medicine and Child Neurology, 50, 15–18.CrossRefGoogle ScholarPubMed
Knickmeyer, R. C., Woolson, S., Hamer, R. M., Konneker, T., & Gilmore, J. H. (2011). 2D:4D ratios in the first 2 years of life: Stability and relation to testosterone exposure and sensitivity. Hormones and Behavior, 60, 256–263.CrossRefGoogle Scholar
Kondo, T., Zakany, J., Innis, J. W., & Duboule, D. (1997). Of fingers, toes and penises. Nature, 390(6655), 29.CrossRefGoogle ScholarPubMed
Lemiere, J., Boets, B., & Danckaerts, M. (2010). No association between the 2D : 4D fetal testosterone marker and multidimensional attentional abilities in children with ADHD. Developmental Medicine & Child Neurology, 52, e202–e208.CrossRefGoogle ScholarPubMed
Levy, J., & Heller, W. (1992). Gender differences in human neuropsychological function. In Arnold, A., Moltz, H. & Ward, I. (Eds.), Sexual differentiation (pp. 245–274). New York: Plenum Press.CrossRefGoogle Scholar
Liu, J., Cheng, H., & Leung, P. W. (2011). The application of the preschool Child Behavior Checklist and the Caregiver–Teacher Report Form to mainland Chinese children: Syndrome structure, gender differences, country effects, and inter-informant agreement. Journal of Abnormal Child Psychology, 39, 251–264.CrossRefGoogle ScholarPubMed
Liu, J., McCauley, L. A., Zhao, Y., Zhang, H., & Pinto-Martin, J. (2010). Cohort profile: The China Jintan Child Cohort Study. International Journal of Epidemiology, 39, 668–674.CrossRefGoogle ScholarPubMed
Lutchmaya, S., Baron-Cohen, S., Raggatt, P., Knickmeyer, R., & Manning, J. T. (2004). 2nd to 4th digit ratios, fetal testosterone and estradiol. Early Human Development, 77, 23–28.CrossRefGoogle Scholar
Lyon, G., & Gadisseux, J. F. (1991). Structural abnormalities of the brain in developmental disorders. In Rutter, M. & Caesar, P. (Eds.), Biological risk factors for psychosocial disorders (pp. 1–19). Cambridge: Cambridge University Press.Google Scholar
Malas, M. A., Dogan, S., Evcil, E. H., & Desdicioglu, K. (2006). Fetal development of the hand, digits and digit ratio (2D:4D). Early Human Development, 82, 469–475.CrossRefGoogle Scholar
Manning, J. (2002). Digit ratio: A pointer to fertility, behavior and health. New Brunswick, NJ: Rutgers University Press.Google Scholar
Manning, J. T., Baron-Cohen, S., Wheelwright, S., & Sanders, G. (2001). The 2nd to 4th digit ratio and autism. Developmental Medicine and Child Neurology, 43, 160–164.CrossRefGoogle ScholarPubMed
Manning, J. T., Fink, B., Neave, N., & Caswell, N. (2005). Photocopies yield lower digit ratios (2D : 4D) than direct finger measurements. Archives of Sexual Behavior, 34, 329–333.CrossRefGoogle ScholarPubMed
Manning, J. T., Scutt, D., Wilson, J., & Lewis-Jones, D. I. (1998). The ratio of 2nd to 4th digit length: A predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction, 13, 3000–3004.CrossRefGoogle ScholarPubMed
Manning, J. T., Stewart, A., Bundred, P. E., & Trivers, R. L. (2004). Sex and ethnic differences in 2nd to 4th digit ratio of children. Early Human Development, 80, 161–168.CrossRefGoogle ScholarPubMed
Manning, J. T., & Taylor, R. P. (2001). Second to fourth digit ratio and male ability in sport: Implications for sexual selection in humans. Evolution and Human Behavior, 22, 61–69.CrossRefGoogle ScholarPubMed
Manning, J. T., Trivers, R. L., Singh, D., & Thornhill, R. (1999). The mystery of female beauty. Nature, 399(6733), 214–215.CrossRefGoogle ScholarPubMed
Martel, M. M. (2009). Conscientiousness as a mediator of the association between masculinized finger-length ratios and attention-deficit/hyperactivity disorder (ADHD). Journal of Child Psychology and Psychiatry, 50, 790–798.CrossRefGoogle ScholarPubMed
Martel, M. M., Gobrogge, K. L., Breedlove, S. M., & Nigg, J. T. (2008). Masculinized finger-length ratios of boys, but not girls, are associated with attention-deficit/hyperactivity disorder. Behavioral Neuroscience, 122, 273–281.CrossRefGoogle Scholar
Martel, M. M., Klump, K., Nigg, J. T., Breedlove, S. M., & Sisk, C. L. (2009). Potential hormonal mechanisms of attention-deficit/hyperactivity disorder and major depressive disorder: A new perspective. Hormones and Behavior, 55, 465–479.CrossRefGoogle ScholarPubMed
McIntyre, M. H., Barrett, E. S., McDermott, R., Johnson, D. D. P., Cowden, J., & Rosen, S. P. (2007). Finger length ratio (2D : 4D) and sex differences in aggression during a simulated war game. Personality and Individual Differences, 42, 755–764.CrossRefGoogle Scholar
McIntyre, M. H., Ellison, P. T., Lieberman, D. E., Demerath, E., & Towne, B. (2005). The development of sex differences in digital formula from infancy in the Fels Longitudinal Study. Proceedings of the Royal Society B: Biological Sciences, 272(1571), 1473.Google ScholarPubMed
McManus, I., & Bryden, M. (1991). Geschwind's theory of cerebral lateralization: Developing a formal, causal model. Psychological Bulletin, 110, 237.CrossRefGoogle ScholarPubMed
Moffitt, T. E. (1990). Juvenile delinquency and attention deficit disorder: Boys' developmental trajectories from age 3 to age 15. Child Development, 61, 893–910.CrossRefGoogle ScholarPubMed
Neugebauer, R., Hoek, H. W., & Susser, E. (1999). Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. Journal of the American Medical Association, 282, 455–462.CrossRefGoogle ScholarPubMed
Okten, A., Kalyoncu, M., & Yaris, N. (2002). The ratio of second- and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Human Development, 70, 47–54.CrossRefGoogle ScholarPubMed
Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65, 369–382.CrossRefGoogle ScholarPubMed
PopeH. G., Jr. H. G., Jr., Kouri, E. M., & Hudson, J. I. (2000). Effects of supraphysiologic doses of testosterone on mood and aggression in normal men: A randomized controlled trial. Archives of General Psychiatry, 57, 133–140.CrossRefGoogle ScholarPubMed
Raine, A. (2008). From genes to brain to antisocial behavior. Current Directions in Psychological Science, 17, 323–328.CrossRefGoogle Scholar
Raine, A. (2011). An amygdala structural abnormality common to two subtypes of conduct disorder: A neurodevelopmental conundrum. American Journal of Psychiatry, 168, 569–571.CrossRefGoogle ScholarPubMed
Raine, A., Venables, P. H., & Williams, M. (1996). Better autonomic conditioning and faster electrodermal half-recovery time at age 15 years as possible protective factors against crime at age 29 years. Developmental Psychology, 32, 624–630.CrossRefGoogle Scholar
Rubia, K. (2011). “Cool” inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus “hot” ventromedial orbitofrontal–limbic dysfunction in conduct disorder: A review. Biological Psychiatry, 69(12), e69–87.CrossRefGoogle ScholarPubMed
Rutter, M., Hersov, L. A., & Shaffer, D. (1978). Aggression and anti-social behavior in childhood and adolescence. In Rutter, M., Hersov, L. A. & Shaffer, D. (Eds.), Family, area, and school influences in the genesis of conduct disorder (pp. 95–113). New York: Wiley.Google Scholar
Tomaszycki, M. L., Gouzoules, H., & Wallen, K. (2005). Sex differences in juvenile rhesus macaque (Macaca mulatta) agonistic screams: Life history differences and effects of prenatal androgens. Devlopmental Psychobiology, 47, 318–327.CrossRefGoogle ScholarPubMed
Trivers, R., Manning, J., & Jacobson, A. (2006). A longitudinal study of digit ratio (2D:4D) and other finger ratios in Jamaican children. Hormones and Behavior, 49, 150–156.CrossRefGoogle Scholar
Van Goozen, S. H. M., Cohen-Kettenis, P. T., Gooren, L. J. G., Frijda, N. H., & Van De Poll, N. E. (1995). Gender differences in behaviour: Activating effects of cross-sex hormones. Psychoneuroendocrinology, 20, 343–363.CrossRefGoogle ScholarPubMed
Vermeersch, H., T'Sjoen, G., Kaufman, J. M., & Vincke, J. (2008). 2D:4D, sex steroid hormones and human psychological sex differences. Hormones and Behavior, 54, 340–346.CrossRefGoogle Scholar
Voracek, M., Manning, J. T., & Ponocny, I. (2005). Digit ratio (2D : 4D) in homosexual and heterosexual men from Austria. Archives of Sexual Behavior, 34, 335–340.CrossRefGoogle ScholarPubMed
Weine, A. M., Phillips, J. S., & Achenbach, T. M. (1995). Behavioral and emotional problems among Chinese American children: Parent and teacher reports for ages 6 to 13. Journal of Abnormal Child Psychology, 23, 619–639.CrossRefGoogle ScholarPubMed
Williams, J. H. G., Greenhalgh, K. D., & Manning, J. T. (2003). Second to fourth finger ratio and possible precursors of developmental psychopathology in preschool children. Early Human Development, 72, 57–65.CrossRefGoogle ScholarPubMed
Yang, C. F. J., Gray, P. B., Zhang, J. X., & Pope, H. G. (2009). Second to fourth digit ratios, sex differences, and behavior in Chinese men and women. Social Neuroscience, 4, 49–59.CrossRefGoogle ScholarPubMed
Yu, L., & Winter, S. (2011). Gender atypical behavior in Chinese school-aged children: Its prevalence and relation to sex, age, and only-child status. Journal of Sex Research, 48, 334–348.CrossRefGoogle ScholarPubMed
Zheng, Z. G., & Cohn, M. J. (2011). Developmental basis of sexually dimorphic digit ratios. Proceedings of the National Academy of Sciences of the United States of America, 108, 16289–16294.CrossRefGoogle ScholarPubMed