Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-20T00:26:45.006Z Has data issue: false hasContentIssue false
  • English
  • Français

The effects of circulating testosterone and pubertal maturation on risk for disordered eating symptoms in adolescent males

Published online by Cambridge University Press:  09 January 2014

K. M. Culbert ,
S. A. Burt ,
C. L. Sisk ,
J. T. Nigg  and
K. L. Klump
K. M. Culbert*
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA
S. A. Burt
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA
C. L. Sisk
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA Neuroscience Program, Michigan State University, East Lansing, MI, USA
J. T. Nigg
Affiliation:
Department of Psychiatry, Oregon Health and Science University, Portland, OR, USA
K. L. Klump
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA
*
*Address for correspondence: K. M. Culbert, Ph.D., Department of Psychology, Michigan State University, 293 Farm Lane, Giltner Hall – Room 354, East Lansing, MI 48824-1116, USA. (Email: culbertk@msu.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Testosterone may be a biological factor that protects males against eating disorders. Elevated prenatal testosterone exposure is linked to lower levels of disordered eating symptoms, but effects emerge only after mid-puberty. Whether circulating levels of testosterone account for decreased risk for disordered eating in boys after mid-puberty is currently unknown; however, animal data support this possibility. In rodents, prenatal testosterone's masculinizing effects on sex-differentiated behaviors emerge during puberty when circulating levels of testosterone increase and ‘activate’ the expression of masculinized phenotypes. This study investigated whether higher levels of circulating testosterone predict lower levels of disordered eating symptoms in adolescent boys, and in particular whether effects are associated with advancing pubertal maturation.

Method

Participants were 213 male twins from the Michigan State University Twin Registry. The Minnesota Eating Behavior Survey and Eating Disorder Examination Questionnaire assessed several disordered eating symptoms. The Pubertal Development Scale assessed pubertal status. Afternoon saliva samples were assayed for testosterone using enzyme immunoassays.

Results

Consistent with animal data, higher levels of circulating testosterone predicted lower levels of disordered eating symptoms in adolescent boys and effects emerged with advancing puberty. Results were not accounted for by several important covariates, including age, adiposity, or mood/anxiety symptoms.

Conclusions

Findings suggest that elevated circulating testosterone may be protective and underlie decreased risk for eating pathology in males during/after puberty, whereas lower levels of testosterone may increase risk and explain why some, albeit relatively few, males develop eating disorders.

Keywords

Adolescencedisordered eatingeating disordersmalespubertytestosterone
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 11 , August 2014 , pp. 2271 - 2286
Copyright
Copyright © Cambridge University Press 2014 

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

Asarian, L, Geary, N (2006). Modulation of appetite by gonadal steroid hormones. Philosophical Transactions of the Royal Society of London, SeriesB: Biological Sciences 361, 1251–1263.CrossRefGoogle ScholarPubMed
Baker, JH, Girdler, SS, Bulik, CM (2012). The role of reproductive hormones in the development and maintenance of eating disorders. Expert Review of Obstetrics and Gynecology 7, 573–583.CrossRefGoogle ScholarPubMed
Baker, JH, Lichtenstein, P, Kendler, KS (2009). Intrauterine testosterone exposure and risk for disordered eating. British Journal of Psychiatry 194, 375–376.CrossRefGoogle ScholarPubMed
Beumont, PJV, Beardwood, CJ, Russell, GFM (1972). The occurrence of the syndrome of anorexia nervosa in male subjects. Psychological Medicine 2, 216–231.CrossRefGoogle ScholarPubMed
Breedlove, SM (1994). Sexual differentiation of the human nervous system. Annual Review of Psychology 45, 389–418.CrossRefGoogle ScholarPubMed
Burt, SA, Klump, KL (2013). The Michigan State University Twin Registry (MSUTR): an update. Twin Research and Human Genetics 16, 344–350.CrossRefGoogle ScholarPubMed
Carskadon, MA, Acebo, C (1993). A self-administered rating scale for pubertal development. Journal of Adolescent Health 14, 190–195.CrossRefGoogle ScholarPubMed
Carter, JC, Stewart, DA, Fairburn, CG (2001). Eating Disorder Examination Questionnaire: norms for young adolescent girls. Behaviour Research and Therapy 39, 625–632.CrossRefGoogle ScholarPubMed
Chai, JK, Blaha, V, Meguid, MM, Laviano, A, Yang, ZJ, Varma, M (1999). Use of orchiectomy and testosterone replacement to explore meal number-to-meal size relationship in male rats. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 276, R1366–R1373.Google ScholarPubMed
Crisp, AH, Hsu, LKG, Chen, CN, Wheeler, M (1982). Reproductive hormone profiles in male anorexia nervosa before, during and after restoration of body weight to normal. A study of twelve patients. International Journal of Eating Disorders 1, 3–9.3.0.CO;2-I>CrossRefGoogle Scholar
Culbert, KM, Breedlove, SM, Burt, SA, Klump, KL (2008). Prenatal hormone exposure and risk for eating disorders: a comparison of opposite-sex and same-sex twins. Archives of General Psychiatry 65, 329–336.CrossRefGoogle ScholarPubMed
Culbert, KM, Breedlove, SM, Sisk, CL, Burt, SA, Klump, KL (2013). The emergence of sex differences in risk for disordered eating attitudes during puberty: a role for prenatal testosterone exposure. Journal of Abnormal Psychology 122, 420–432.CrossRefGoogle ScholarPubMed
Culbert, KM, Burt, SA, McGue, M, Iacono, WG, Klump, KL (2009). Puberty and the genetic diathesis of disordered eating attitudes and behaviors. Journal of Abnormal Psychology 118, 788–796.CrossRefGoogle ScholarPubMed
Dorn, LD, Biro, FM (2011). Puberty and its measurement: a decade in review. Journal of Research on Adolescence 21, 180–195.CrossRefGoogle Scholar
Fairburn, CG, Beglin, SJ (1994). Assessment of eating disorders: interview or self-report questionnaire? International Journal of Eating Disorders 16, 363–370.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Ferreiro, F, Seoane, G, Senra, C (2011). Gender-related risk and protective factors for depressive symptoms and disordered eating in adolescence: a 4-year longitudinal study. Journal of Youth and Adolescence 41, 607–622.CrossRefGoogle ScholarPubMed
Granger, DA, Schwartz, EB, Booth, A, Arentz, M (1999). Salivary testosterone determination in studies of child health and development. Hormones and Behavior 35, 18–27.CrossRefGoogle ScholarPubMed
Granger, DA, Shirtcliff, EA, Booth, A, Kivlighan, KT, Schwartz, EB (2004). The ‘trouble’ with salivary testosterone. Psychoneuroendocrinology 29, 1229–1240.CrossRefGoogle ScholarPubMed
Granger, DA, Shirtcliff, EA, Zahn-Waxler, C, Usher, B, Klimes-Dougan, B, Hastings, P (2003). Salivary testosterone diurnal variation and psychopathology in adolescent males and females: individual differences and developmental effects. Development and Psychopathology 15, 431–449.CrossRefGoogle ScholarPubMed
Grumbach, MM, Styne, DM (1998). Puberty: Ontogeny, Neuroendocrinology, Physiology, and Disorders. W. B. Saunders Company: Philadelphia, PA.Google Scholar
Houtkooper, LB, Lohman, TG, Going, SB, Howell, WH (1996). Why bioelectrical impedance analysis should be used for estimating adiposity. American Journal of Clinical Nutrition 64, 436S–448S.CrossRefGoogle ScholarPubMed
Hudson, JI, Hiripi, E, Pope, HG, Kessler, RC (2007). The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biological Psychiatry 61, 348–358.CrossRefGoogle ScholarPubMed
Jacobi, C, Hayward, C, de Zwaan, M, Kraemer, HC, Stewart, A (2004). Coming to terms with risk factors for eating disorders: application of risk terminology and suggestions for a general taxonomy. Psychological Bulletin 130, 19–65.CrossRefGoogle ScholarPubMed
Kenny, DA, Kashy, DA, Cook, WL (2006). Dyadic Data Analysis. Guilford Press: New York.Google Scholar
Klump, KL (2013). Puberty as a critical risk period for eating disorders: a review of human and animal studies. Hormones and Behavior 64, 399–410.CrossRefGoogle ScholarPubMed
Klump, KL, Burt, SA (2006). The Michigan State University Twin Registry (MSUTR): genetic, environmental and neurobiological influences on behavior across development. Twin Research and Human Genetics 9, 971–977.CrossRefGoogle ScholarPubMed
Klump, KL, Culbert, KM, Slane, JD, Burt, SA, Sisk, CL, Nigg, JT (2012). The effects of puberty on genetic risk for disordered eating: evidence for a sex difference. Psychological Medicine 42, 627–637.CrossRefGoogle ScholarPubMed
Klump, KL, Gobrogge, KL, Perkins, P, Thorne, D, Sisk, CL, Breedlove, SM (2006). Preliminary evidence that gonadal hormones organize and activate disordered eating. Psychological Medicine 12, 539–546.CrossRefGoogle Scholar
Klump, KL, Perkins, PS, Burt, SA, McGue, M, Iacono, WG (2007). Puberty moderates genetic influences on disordered eating. Psychological Medicine 37, 627–634.CrossRefGoogle ScholarPubMed
Kostanski, M, Gullone, E (1998). Adolescent body image dissatisfaction: relationships with self-esteem, anxiety, and depression controlling for body mass. Journal of Child Psychology and Psychiatry 39, 255–262.Google ScholarPubMed
Kovacs, M (1985). The Children's Depression Inventory (CDI). Psychopharmacology Bulletin 21, 995–998.Google ScholarPubMed
Lavender, JM, De Young, KP, Anderson, DA (2010). Eating Disorder Examination Questionnaire (EDE-Q): norms for undergraduate men. Eating Behaviors 11, 119–121.CrossRefGoogle ScholarPubMed
Lemaire, A, Ardaens, K, Lepretre, J, Racadot, A, Buvat-Herbaut, M, Buvat, J (1983). Gonadal hormones in male anorexia nervosa. International Journal of Eating Disorders 2, 135–144.3.0.CO;2-Y>CrossRefGoogle Scholar
Lydecker, JA, Pisetsky, EM, Mitchell, KS, Thornton, LM, Kendler, KS, Reichborn-Kjennerud, T, Lichtenstein, P, Bulik, CM, Mazzeo, SE (2012). Association between co-twin sex and eating disorders in opposite sex twin pairs: evaluations in North American, Norwegian, and Swedish samples. Journal of Psychosomatic Research 72, 73–77.CrossRefGoogle ScholarPubMed
March, JS, Parker, J, Sullivan, K, Stallings, P, Conners, CK (1997). The Multidimensional Anxiety Scale for Children (MASC): factor structure, reliability, and validity. Journal of the American Academy of Child and Adolescent Psychiatry 36, 554–565.CrossRefGoogle ScholarPubMed
McCabe, MP, Vincent, MA (2003). The role of biodevelopmental and psychological factors in disordered eating among adolescent males and females. European Eating Disorders Review 11, 315–328.CrossRefGoogle Scholar
Miller, KK, Deckersbach, T, Rauch, SL, Fischman, AJ, Grieco, KA, Herzog, DB, Klibanski, A (2004). Testosterone administration attenuates regional brain hypometabolism in women with anorexia nervosa. Psychiatry Research: Neuroimaging 132, 197–207.CrossRefGoogle ScholarPubMed
Oinonen, KA, Bird, JL (2012). Age at menarche and digit ratio (2D:4D): relationships with body dissatisfaction, drive for thinness, and bulimia symptoms in women. Body Image 9, 302–306.CrossRefGoogle Scholar
Olivardia, R, Pope, HG, Mangweth, B, Hudson, JI (1995). Eating disorders in college men. American Journal of Psychiatry 152, 1279–1285.Google ScholarPubMed
Peper, JS, Hulshoff Pol, HE, Crone, EA, Van Honk, J (2011). Sex steroids and brain structure in pubertal boys and girls: a mini-review of neuroimaging studies. Neuroscience 191, 28–37.CrossRefGoogle ScholarPubMed
Petersen, AC, Richards, M, Boxer, A (1988). A self-report measure of pubertal status: reliability, validity, and initial norms. Journal of Youth and Adolescence 17, 117–133.CrossRefGoogle ScholarPubMed
Romeo, RD, Richardson, HN, Sisk, CL (2002). Puberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential. Neuroscience and Biobehavioral Reviews 26, 381–391.CrossRefGoogle ScholarPubMed
Rubinow, DR, Schmidt, PJ (1996). Androgens, brain, and behavior. American Journal of Psychiatry 153, 974–984.Google ScholarPubMed
Schulz, KM, Molenda-Figueira, HA, Sisk, CL (2009). Back to the future: the organizational–activational hypothesis adapted to puberty and adolescence. Hormones and Behavior 55, 597–604.CrossRefGoogle Scholar
Schulz, KM, Richardson, HN, Zehr, JL, Ostek, AJ, Menard, TA, Sisk, CL (2004). Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syrian hamster. Hormones and Behavior 45, 242–249.CrossRefGoogle ScholarPubMed
Shirtcliff, EA, Dahl, RE, Pollak, SD (2009). Pubertal development: correspondence between hormonal and physical development. Child Development 80, 327–337.CrossRefGoogle ScholarPubMed
Shirtcliff, EA, Granger, DA, Schwartz, E, Curran, MJ (2001). Use of salivary biomarkers in biobehavioral research: cotton-based sample collection methods can interfere with salivary immunoassay results. Psychoneuroendocrinology 26, 165–173.CrossRefGoogle ScholarPubMed
Smith, AR, Hawkeswood, SE, Joiner, TE (2010). The measure of a man: associations between digit ratio and disordered eating in males. International Journal of Eating Disorders 43, 543–548.CrossRefGoogle Scholar
Swanson, SA, Crow, SJ, Le Grange, D, Swendsen, J, Merikangas, KR (2011). Prevalence and correlates of eating disorders in adolescents: results from the National Comorbidity Survey Replication Adolescent Supplement. Archives of General Psychiatry 68, 714–723.CrossRefGoogle ScholarPubMed
Vining, RF, McGinley, RA, Symons, RG (1983). Hormones in saliva: mode of entry and consequent implications for clinical interpretation. Clinical Chemistry 29, 1752–1756.CrossRefGoogle ScholarPubMed
Von Ranson, KM, Klump, KL, Iacono, WG, McGue, M (2005). The Minnesota Eating Behavior Survey: a brief measure of disordered eating attitudes and behaviors. Eating Behaviors 4, 373–392.CrossRefGoogle Scholar