Abstract
Adolescence is a period of social, psychological, and physiological change, including the onset of puberty. Differential pubertal onset has been linked to a myriad of problems, including mental health problems. Therefore, we aim to investigate deviating pubertal development in autism, and whether this is more pronounced in girls than in boys. A total of 68 individuals (nASC = 34, nCOM (comparisons) = 34) aged 12 to 16 years were administered test concerning pubertal development and mental health (i.e., sensory sensitivity, autistic traits, depression, anxiety, and externalizing problems). Frequentist and Bayesian ANOVA was used to examine deviations in pubertal development in ASC and possible sex effects. Regression analyses was used to test whether this asynchronicity was linked to mental health problems. Our (frequentist and Bayesian) analyses revealed earlier onset and slower development of pubertal development in ASC but we did not find any sex differences. Maturation disparity was linked to higher mental health problems in ASC, but not in COM. No sex differences in the relation with mental health outcomes was found. We found evidence for a slower development of “true” puberty in those with ASC compared to those without. Moreover, we show that disparities in pubertal development are related to mental health in ASC, suggesting a greater impact on mental health in autistic than in non-autistic teens. Longitudinal studies are necessary to elucidate important developmental trajectories in puberty in neurodiverse populations.
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Data Availability
Data is available upon reasonable request from the final author (HMG).
References
American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th ed. text rev
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th ed. https://doi.org/10.1176/appi.books.9780890425596
Baron C, Wheelwright S, Skinner R, Martin J, Clubley E (2001) The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31(1):5–17. https://doi.org/10.1023/a:1005653411471
Birmaher B, Khetarpal S, Brent D, Cully M, Balach L, Kaufman J, Neer SM (1997) The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. J Am Acad Child Adolesc Psychiatry 36(4):545–553. https://doi.org/10.1097/00004583-199704000-00018
Bodden DHM, Bögels SM, Muris P (2009) The diagnostic utility of the Screen for Child Anxiety Related Emotional Disorders-71 (SCARED-71). Behav Res Ther 47(5):418–425. https://doi.org/10.1016/j.brat.2009.01.015
Braithwaite D, Moore DH, Lustig RH, Epel ES, Ong KK, Rehkopf DH, Wang MC, Miller SM, Hiatt RA (2009) Socioeconomic status in relation to early menarche among black and white girls. Cancer Causes Control: CCC 20(5):713–720. https://doi.org/10.1007/s10552-008-9284-9
Buck Louis GM, Gray LE, Marcus M, Ojeda SR, Pescovitz OH, Witchel SF, Sippell W, Abbott DH, Soto A, Tyl RW, Bourguignon J-P, Skakkebaek NE, Swan SH, Golub MS, Wabitsch M, Toppari J, Euling SY (2008) Environmental factors and puberty timing: expert panel research needs. Pediatrics 121(3):S192–S207. https://doi.org/10.1542/peds.1813E
Cheng TW, Magis-Weinberg L, Guazzelli Williamson V, Ladouceur CD, Whittle SL, Herting MM, Uban KA, Byrne ML, Barendse MEA, Shirtcliff EA, Pfeifer JH (2021) A researcher’s guide to the measurement and modeling of puberty in the ABCD Study® at baseline. Front Endocrinol 12:608575. https://doi.org/10.3389/fendo.2021.608575
Copeland WE, Worthman C, Shanahan L, Costello EJ, Angold A (2019) Early pubertal timing and testosterone associated with higher levels of adolescent depression in girls. J Am Acad Child Adolesc Psychiatry 58(12):1197–1206. https://doi.org/10.1016/j.jaac.2019.02.007
Corbett BA, Muscatello RA, Baldinger C (2019a) Comparing stress and arousal systems in response to different social contexts in children with ASD. Biol Psychol 140:119–130. https://doi.org/10.1016/j.biopsycho.2018.12.010
Corbett BA, Muscatello RA, Tanguturi Y, McGinn E, Ioannou S (2019b) Pubertal development measurement in children with and without autism spectrum disorder: a comparison between physical exam, parent- and self-report. J Autism Dev Disord 49(12):4807–4819. https://doi.org/10.1007/s10803-019-04192-w
Corbett BA, Vandekar S, Muscatello RA, Tanguturi Y (2020) Pubertal timing during early adolescence: advanced pubertal onset in females with autism spectrum disorder. Autism Res 13(12):2202–2215. https://doi.org/10.1002/aur.2406
Deardorff J, Marceau K, Johnson M, Reeves JW, Biro FM, Kubo A, Greenspan LC, Laurent CA, Windham GC, Pinney SM, Kushi LH, Hiatt RA (2021) Girls’ pubertal timing and tempo and mental health: a longitudinal examination in an ethnically diverse sample. J Adolesc Health 68(6):1197–1203. https://doi.org/10.1016/j.jadohealth.2021.01.020
Dorn LD, Dahl RE, Woodward HR, Biro F (2006) Defining the boundaries of early adolescence: a user’s guide to assessing pubertal status and pubertal timing in research with adolescents. Appl Dev Sci 10(1):30–56. https://doi.org/10.1207/s1532480xads1001_3
Fuhrman BJ, Moore SC, Byrne C, Makhoul I, Kitahara CM, Berrington de González A, Linet MS, Weiderpass E, Adami HO, Freedman ND, Liao LM, Matthews CE, Stolzenberg-Solomon RZ, Gaudet MM, Patel AV, Lee IM, Buring JE, Wolk A, Larsson SC, Hoover RN (2021) Association of the age at menarche with site-specific cancer risks in pooled data from nine cohorts. Cancer Res 81(8):2246–2255. https://doi.org/10.1158/0008-5472.CAN-19-3093
Galvao TF, Silva MT, Zimmermann IR, Souza KM, Martins SS, Pereira MG (2014) Pubertal timing in girls and depression: a systematic review. J Affect Disord 155:13–19. https://doi.org/10.1016/j.jad.2013.10.034
Ge X, Kim IJ, Brody GH, Conger RD, Simons RL, Gibbons FX, Cutrona CE (2003) It’s about timing and change: pubertal transition effects on symptoms of major depression among African American youths. Dev Psychol 39(3):430–439. https://doi.org/10.1037/0012-1649.39.3.430
Goodman R (2001) Psychometric properties of the strengths and difficulties questionnaire. J Am Acad Child Adolesc Psychiatry 40(11):1337–1345. https://doi.org/10.1097/00004583-200111000-00015
Hamlat EJ, Snyder HR, Young JF, Hankin BL (2019) Pubertal timing as a transdiagnostic risk for psychopathology in youth. Clin Psychol Sci 7(3):411–429. https://doi.org/10.1177/2167702618810518
Ho TC, Gifuni AJ, Gotlib IH (2022) Psychobiological risk factors for suicidal thoughts and behaviors in adolescence: a consideration of the role of puberty. Mol Psychiatry 27(1):606–623. https://doi.org/10.1038/s41380-021-01171-5
Hoekstra RA, Bartels M, Cath DC, Boomsma DI (2008) Factor structure, reliability and criterion validity of the autism-spectrum quotient (AQ): a study in Dutch population and patient groups. J Autism Dev Disord 38(8):1555–1566
Ingudomnukul E, Baron-Cohen S, Wheelwright S, Knickmeyer R (2007) Elevated rates of testosterone-related disorders in women with autism spectrum conditions. Horm Behav 51(5):597–604. https://doi.org/10.1016/j.yhbeh.2007.02.001
Knickmeyer RC, Wheelwright S, Hoekstra R, Baron-Cohen S (2006) Age of menarche in females with autism spectrum conditions. Dev Med Child Neurol 48(12):1007–1008. https://doi.org/10.1017/S0012162206222229
Kort W, Schittekatte M, Dekker PH, Verhaeghe P, Compaan EL, Bosmans M, Vermeir G (2005) WISC-III NL Wechsler intelligence scale for children. Derde Editie NL. Handleiding en Verantwoording. Amsterdam: Harcourt Test Publishers/Nederlands Instituut voor Psychologen
Kovacs M (1992) Children’s Depression Inventory (CDI). Multi-health Systems Inc, New York
Lee MD, Wagenmakers E-J (2014) Bayesian cognitive modeling: a practical course. Cambridge University Press
Lynch SJ, Sunderland M, Newton NC, Chapman C (2021) A systematic review of transdiagnostic risk and protective factors for general and specific psychopathology in young people. Clin Psychol Rev 87:102036. https://doi.org/10.1016/j.cpr.2021.102036
May T, Pang KC, O’Connell MA, Williams K (2017) Typical pubertal timing in an Australian population of girls and boys with autism spectrum disorder. J Autism Dev Disord 47(12):3983–3993. https://doi.org/10.1007/s10803-017-3281-3
Mensah FK, Bayer JK, Wake M, Carlin JB, Allen NB, Patton GC (2013) Early puberty and childhood social and behavioral adjustment. J Adolesc Health 53(1):118–124. https://doi.org/10.1016/j.jadohealth.2012.12.018
Minshew NJ, Hobson JA (2008) Sensory sensitivities and performance on sensory perceptual tasks in high-functioning individuals with autism. J Autism Dev Disord 38(8):1485–1498. https://doi.org/10.1007/s10803-007-0528-4
Morey RD, Rouder JN, Jamil T, Urbanek S, Forner K, Ly A (2018). Bayes factor: computation of Bayes factors for common designs (0.9.12–4.2) [Computer software]. https://CRAN.R-project.org/package=BayesFactor
Petersen AC, Crockett L, Richards M, Boxer A (1988) A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc 17(2):117–133. https://doi.org/10.1007/BF01537962
Pohl A, Cassidy S, Auyeung B, Baron-Cohen S (2014) Uncovering steroidopathy in women with autism: a latent class analysis. Molecular Autism 5(1):27. https://doi.org/10.1186/2040-2392-5-27
Reiter EO, Fuldauer VG, Root AW (1977) Secretion of the adrenal androgen, dehydroepiandrosterone sulfate, during normal infancy, childhood, and adolescence, in sick infants, and in children with endocrinologic abnormalities. J Pediatr 90(5):766–770. https://doi.org/10.1016/s0022-3476(77)81244-4
RStudio Team. (2015). RStudio: Integrated Development Environment for R. http://www.rstudio.com/
Shirtcliff EA, Dahl RE, Pollak SD (2009) Pubertal development: correspondence between hormonal and physical development. Child Dev 80(2):327–337. https://doi.org/10.1111/j.1467-8624.2009.01263.x
Slappendel G, Mandy W, van der Ende J, Verhulst FC, van der Sijde A, Duvekot J, Skuse D, Greaves-Lord K (2016) Utility of the 3Di short version for the diagnostic assessment of autism spectrum disorder and compatibility with DSM-5. J Autism Dev Disord 46(5):1834–1846. https://doi.org/10.1007/s10803-016-2713-9
Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417–463. https://doi.org/10.1016/s0149-7634(00)00014-2
Timbremont B, Braet C, Roelofs J (2002) Children’s depression inventory: Nederlandstalige versie [Children’s Depression Inventory: Dutch version]. Swets & Zeitlinger, In Lisse
Tordjman S, Ferrari P, Sulmont V, Duyme M, Roubertoux P (1997) Androgenic activity in autism. Am J Psychiatry 154(11):1626. https://doi.org/10.1176/ajp.154.11.1626-a
Acknowledgements
We would like to thank Linda Olde Dubbelink and Sanne van den Bergh for their help in coordinating the study and data collection. Furthermore, we want to thank the clinics and schools involved and all participants for the time and energy they put into this research.
Funding
This work was supported by Leo Kannerhuis, institute for specialized care across the lifespan for autistic individuals, and authors APG and HMG were funded by Innovational Research Incentives Scheme VICI (NWO) awarded to HMG (grant number 453–16-006).
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Groenman, A.P., van der Oord, S. & Geurts, H.M. Navigating adolescence: pubertal development in autism spectrum conditions and its relation to mental health. Arch Womens Ment Health (2024). https://doi.org/10.1007/s00737-023-01414-0
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DOI: https://doi.org/10.1007/s00737-023-01414-0