Study protocol: Imaging brain development in the Childhood to Adolescence Transition Study (iCATS)

BMC Pediatrics

Nicholas B Allen⁴  Marc L Seal¹  Lisa K Mundy⁶  Michelle L Byrne⁴  Craig Olsson⁵  Paul Dudgeon⁴  George C Patton¹  Sarah L Whittle²  Julian G Simmons³ 

[1] Department of Paediatrics, The University of Melbourne, Melbourne, Australia;Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, 1-100 Grattan Street, Parkville, VIC 3010, Australia;Murdoch Childrens Research Institute, Melbourne, Australia;Melbourne School of Psychological Sciences, The University of Melbourne, VIC 3010, Australia;Deakin University, Melbourne, Australia;Centre for Adolescent Health, The Royal Children’s Hospital, Melbourne, Australia

关键词: Gonadarche;    MRI;    Protocol;    Brain development;    Adolescence;    Adrenarche;    Hormones;    Puberty;   

Others  :  1138879
DOI  :  10.1186/1471-2431-14-115

 received in 2014-02-21, accepted in 2014-04-09,  发布年份 2014

【 摘 要 】

Background

Puberty is a critical developmental phase in physical, reproductive and socio-emotional maturation that is associated with the period of peak onset for psychopathology. Puberty also drives significant changes in brain development and function. Research to date has focused on gonadarche, driven by the hypothalamic-pituitary-gonadal axis, and yet increasing evidence suggests that the earlier pubertal stage of adrenarche, driven by the hypothalamic-pituitary-adrenal axis, may play a critical role in both brain development and increased risk for disorder. We have established a unique cohort of children who differ in their exposure to adrenarcheal hormones. This presents a unique opportunity to examine the influence of adrenarcheal timing on brain structural and functional development, and subsequent health outcomes. The primary objective of the study is to explore the hypothesis that patterns of structural and functional brain development will mediate the relationship between adrenarcheal timing and indices of affect, self-regulation, and mental health symptoms collected across time (and therefore years of development).

Methods/Design

Children were recruited based upon earlier or later timing of adrenarche, from a larger cohort, with 128 children (68 female; M age 9.51 years) and one of their parents taking part. Children completed brain MRI structural and functional sequences, provided saliva samples for adrenarcheal hormones and immune biomarkers, hair for long-term cortisol levels, and completed questionnaires, anthropometric measures and an IQ test. Parents completed questionnaires reporting on child behaviour, development, health, traumatic events, and parental report of family environment and parenting style.

Discussion

This study, by examining the neurobiological and behavioural consequences of relatively early and late exposure to adrenarche, has the potential to significantly impact our understanding of pubertal risk processes.

【 授权许可】

   
2014 Simmons et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE: Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005, 62(6):593-602.
• [2]Allen NB, Sheeber L (Eds): Adolescent emotional development and the emergence of depressive disorders. London, UK: Cambridge University Press; 2009.
• [3]Patton GC, Viner R: Pubertal transitions in health. Lancet 2007, 369(9567):1130-1139.
• [4]Angold A, Costello EJ: Puberty and depression. Child Adolesc Psychiatr Clin N Am 2006, 15(4):919-937. ix
• [5]Mendle J, Harden KP, Brooks-Gunn J, Graber JA: Development’s tortoise and hare: pubertal timing, pubertal tempo, and depressive symptoms in boys and girls. Dev Psychol 2010, 46(5):1341-1353.
• [6]Graber JA, Lewinsohn PM, Seeley JR, Brooks-Gunn J: Is psychopathology associated with the timing of pubertal development? J Am Acad Child Adolesc Psychiatry 1997, 36(12):1768-1776.
• [7]Kaltiala-Heino R, Kosunen E, Rimpela M: Pubertal timing, sexual behaviour and self-reported depression in middle adolescence. J Adolesc 2003, 26(5):531-545.
• [8]Graber JA: Pubertal and neuroendocrine development and risk for depression. In Adolescent emotional development and the emergence of depressive disorders. Edited by Allen NB, Sheeber L. London, UK: Cambridge University Press; 2009.
• [9]Patton GC, Olsson C, Bond L, Toumbourou JW, Carlin JB, Hemphill SA, Catalano RF: Predicting female depression across puberty: a two-nation longitudinal study. J Am Acad Child Adolesc Psychiatry 2008, 47(12):1424-1432.
• [10]Hemphill SA, Kotevski A, Herrenkohl TI, Toumbourou JW, Carlin JB, Catalano RF, Patton GC: Pubertal stage and the prevalence of violence and social/relational aggression. Pediatrics 2010, 126(2):e298-e305.
• [11]Dorn LD, Biro FM: Puberty and its measurement: a decade in review. J Res Adolesc 2011, 21(1):180-195.
• [12]Dorn LD, Hitt SF, Rotenstein D: Biopsychological and cognitive differences in children with premature vs. on-time adrenarche. Arch Pediatr Adolesc Med 1999, 153(2):137-146.
• [13]Behringer V, Hohmann G, Stevens JM, Weltring A, Deschner T: Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels. J Endocrinol 2012, 214(1):55-65.
• [14]Mundy LK, Simmons JG, Allen NB, Viner RM, Bayer JK, Olds T, Williams J, Olsson C, Romaniuk H, Mensah F, Sawyer SM, Degenhardt L, Alati R, Wake M, Jacka F, Patton GC: Study protocol: the Childhood to Adolescence Transition Study (CATS). BMC Pediatr 2013, 13(1):160. BioMed Central Full Text
• [15]Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL: Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999, 2(10):861-863.
• [16]Blakemore SJ, Burnett S, Dahl RE: The role of puberty in the developing adolescent brain. Hum Brain Mapp 2010, 31(6):926-933.
• [17]McEwen BS: Steroid hormone actions on the brain: when is the genome involved? Horm Behav 1994, 28(4):396-405.
• [18]Campbell B: Adrenarche in comparative perspective. Am J Hum Biol 2011, 23(1):44-52.
• [19]Peper JS, Brouwer RM, Schnack HG, van Baal GC, van Leeuwen M, van den Berg SM, de Waal HA D-V, Boomsma DI, Kahn RS, Hulshoff Pol HE: Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 2009, 34(3):332-342.
• [20]Neufang S, Specht K, Hausmann M, Gunturkun O, Herpertz-Dahlmann B, Fink GR, Konrad K: Sex differences and the impact of steroid hormones on the developing human brain. Cereb Cortex 2009, 19(2):464-473.
• [21]Nguyen TV, McCracken JT, Ducharme S, Cropp BF, Botteron KN, Evans AC, Karama S: Interactive effects of dehydroepiandrosterone and testosterone on cortical thickness during early brain development. J Neurosci 2013, 33(26):10840-10848.
• [22]Perrin JS, Herve PY, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T: Growth of white matter in the adolescent brain: role of testosterone and androgen receptor. J Neurosci 2008, 28(38):9519-9524.
• [23]Forbes EE: Healthy adolescents’ neural response to reward: associations with puberty, positive affect, and depressive symptoms. J Am Acad Child Adolesc Psychiatry 2010, 49(2):162-172. e1-5
• [24]Whittle S, Yucel M, Lorenzetti V, Byrne ML, Simmons JG, Wood SJ, Pantelis C, Allen NB: Pituitary volume mediates the relationship between pubertal timing and depressive symptoms during adolescence. Psychoneuroendocrinology 2012, 37(7):881-891.
• [25]Kaess M, Simmons JG, Whittle S, Jovev M, Chanen AM, Yucel M, Pantelis C, Allen NB: Sex-specific prediction of hypothalamic-pituitary-adrenal axis activity by pituitary volume during adolescence: a longitudinal study from age 12–17 years. Psychoneuroendocrinology 2013, 38:2694-2704.
• [26]Shirtcliff EA, Dahl RE, Pollak SD: Pubertal development: correspondence between hormonal and physical development. Child Dev 2009, 80(2):327-337.
• [27]Bordini B, Rosenfield RL: Normal pubertal development: part I: the endocrine basis of puberty. Pediatr Rev 2011, 32(6):223-229.
• [28]Rege J, Rainey WE: The steroid metabolome of adrenarche. J Endocrinol 2012, 214(2):133-143.
• [29]Hammer LD, Kraemer HC, Wilson DM, Ritter PL, Dornbusch SM: Standardized percentile curves of body-mass index for children and adolescents. Am J Dis Child 1991, 145(3):259-263.
• [30]Gaffrey MS, Barch DM, Singer J, Shenoy R, Luby JL: Disrupted amygdala reactivity in depressed 4- to 6-year-old children. J Am Acad Child Adolesc Psychiatry 2013, 52(7):737-746.
• [31]Granger DA, Kivlighan KT, Fortunato C, Harmon AG, Hibel LC, Schwartz EB, Whembolua GL: Integration of salivary biomarkers into developmental and behaviorally-oriented research: problems and solutions for collecting specimens. Physiol Behav 2007, 92(4):583-590.
• [32]Byrne ML, O'Brien-Simpson NM, Reynolds EC, Walsh KA, Laughton K, Waloszek JM, Woods MJ, Trinder J, Allen NB: Acute phase protein and cytokine levels in serum and saliva: a comparison of detectable levels and correlations in a depressed and healthy adolescent sample. Brain Behav Immun 2013, 34:164-175.
• [33]Stalder T, Kirschbaum C: Analysis of cortisol in hair - State of the art and future directions. Brain Behav Immun 2012, 26(7):1019-1029.
• [34]Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS: Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen Comp Endocrinol 2006, 147(3):255-261.
• [35]Cole TJ, Bellizzi MC, Flegal KM, Dietz WH: Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 2000, 320(7244):1240-1243.
• [36]Taylor RW, Jones IE, Williams SM, Goulding A: Evaluation of waist circumference, waist-to-hip ratio, and the conicity index as screening tools for high trunk fat mass, as measured by dual-energy X-ray absorptiometry, in children aged 3–19 y. Am J Clin Nutr 2000, 72(2):490-495.
• [37]Petersen AC, Crockett L, Richards M, Boxer A: A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc 1988, 17(2):117-133.
• [38]Bond L, Clements J, Bertalli N, Evans-Whipp T, McMorris BJ, Patton GC, Toumbourou JW, Catalano RF: A comparison of self-reported puberty using the pubertal development scale and the sexual maturation scale in a school-based epidemiologic survey. J Adolesc 2006, 29(5):709-720.
• [39]Morris NM, Udry JR: Validation of a self-administered instrument to assess stage of adolescent development. J Youth Adolesc 1980, 9(3):271-280.
• [40]Achenbach TM: Child Behavior Checklist. In Encyclopedia of Psychology. Edited by Kazdin AE. New York: Oxford University Press; 1999.
• [41]Greenwald R, Rubin A: Brief assessment of children’s post-traumatic symptoms: development and preliminary validation of parent and child scales. Res Soc Work Pract 1999, 9:61-65.
• [42]Shelton KK, Frick PJ, Wootton J: Assessment of parenting practices in families of elementary school-age children. J Clin Child Psychol 1996, 25(3):317-329.
• [43]Essau CA, Sasagawa S, Frick PJ: Psychometric properties of the Alabama parenting questionnaire. J of Child and Fam Studies 2006, 15(5):595-614.
• [44]Dadds MR, Maujean A, Fraser JA: Parenting and conduct problems in children: Australian data and psychometric properties of the Alabama parenting questionnaire. Aust Psychol 2003, 38(3):238-241.
• [45]Kantor GK, Holt M, Straus MA: The parent-report multidimensional neglectful behaviour scale. Durham: NH: Family Research Laboratory; 2004.
• [46]Kantor GK, Holt MK, Mebert CJ, Straus MA, Drach KM, Ricci LR, MacAllum CA, Brown W: Development and preliminary psychometric properties of the multidimensional neglectful behavior scale-child report. Child Maltreat 2004, 9(4):409-428.
• [47]Kovaks M: Children’s depression inventory. Toronto, Canada: Multi-Health Systems; 2004.
• [48]Spence SH: Structure of anxiety symptoms among children: a confirmatory factor-analytic study. J Abnorm Psychol 1997, 106(2):280-297.
• [49]Spence SH: A measure of anxiety symptoms among children. Behav Res Ther 1998, 36(5):545-566.
• [50]Laurent J, Catanzaro SJ, Joiner TE Jr: Development and preliminary validation of the physiological hyperarousal scale for children. Psychol Assess 2004, 16(4):373-380.
• [51]Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9(1):97-113.
• [52]Faul F, Erdfelder E, Lang AG, Buchner A: G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007, 39(2):175-191.
• [53]Fritz MS, Mackinnon DP: Required sample size to detect the mediated effect. Psychol Sci 2007, 18(3):233-239.
• [54]Tournier JD, Calamante F, Connelly A: Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 2007, 35(4):1459-1472.