Abstract
Attention-deficit/hyperactivity disorder (ADHD) is a highly heritable neurodevelopmental disorder. However, no study has examined genetic and environmental influences in the longitudinal developmental course of ADHD symptoms in a non-Western population. This study investigated changes of genetic and environmental influences and their contributions to the stability and change of ADHD symptoms of hyperactivity/impulsivity and inattention in Chinese adolescent twins. A prospective sample of 602 twin pairs (48% male) self-reported both DSM-IV ADHD symptom subscales three times at the approximate age of 12, 13, and 15 years. Longitudinal multivariate genetic analyses through structural equation modelling examined genetic and environmental contributions to the developmental course of ADHD symptoms. From early (time 1 and 2) to middle adolescence (time 3), both symptoms showed modest and non-significant genetic influences that became substantial and significant, whereas shared environmental influences were substantial and significant and became modest and non-significant. The same genetic factors influenced ADHD symptoms throughout adolescence, while shared and non-shared environmental influences largely came from new emerging factors. In early adolescence, genetic factor contributed to the stability of inattention, whereas shared environmental factor contributed to the stability of hyperactivity/impulsivity. Genetic influences of ADHD tended to be smaller, whereas shared environmental influences tended to be larger in Chinese than in Western populations. Genetic factors played a large role in the stability of ADHD throughout adolescence, while shared and non-shared environment primarily contributed to its change. Findings highlight the importance of shared family, neighbourhood, and community experiences on child psychopathology in a collectivistic culture such as the Chinese society.
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References
Merikangas KR, He JP, Burstein M, Swanson SA, Avenevoli S, Cui L, Benjet C, Georgiades K, Swendsen J (2010) Lifetime prevalence of mental disorders in US adolescents: results from the National Comorbidity Survey Replication-Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry 49:980–989
Polanczyk GV, Salum GA, Sugaya LS, Caye A, Rohde LA (2015) Annual Research Review: a meta-analysis of the worldwide prevalence of mental disorders in children and adolescents. J Child Psychol Psychiatry 56:345–365
Polanczyk GV, Willcutt EG, Salum GA, Kieling C, Rohde LA (2014) ADHD prevalence estimates across three decades: an updated systematic review and meta-regression analysis. Int J Epidemiol 43:434–442
Leung PW, Hung SF, Ho TP, Lee CC, Liu WS, Tang CP, Kwong SL (2008) Prevalence of DSM-IV disorders in Chinese adolescents and the effects of an impairment criterion. Eur Child Adolesc Psychiatry 17:452–461
Huang Y, Zheng S, Xu C, Lin K, Wu K, Zheng M, Zhang J, Xu H (2017) Attention-deficit hyperactivity disorder in elementary school students in Shantou, China: prevalence, subtypes, and influencing factors. Neuropsychiatric Dis Treat 13:785–792
Jin W, Du Y, Zhong X, Coghill D (2014) Prevalence and contributing factors to attention deficit hyperactivity disorder: a study of five-to fifteen-year-old children in Zhabei District, Shanghai. Asia Pac Psychiatry 6:397–404
Tong L, Shi HJ, Zang JJ (2013) Prevalence of ADHD in children of China: a systematic review and meta-analysis. Chin J Public Health 29:1279–1283 [In Chinese]
Ramtekkar UP, Reiersen AM, Todorov AA, Todd RD (2010) Sex and age differences in attention-deficit/hyperactivity disorder symptoms and diagnoses: implications for DSM-V and ICD-11. J Am Acad Child Adolesc Psychiatry 49:217–228
Costello EJ, Copeland W, Angold A (2011) Trends in psychopathology across the adolescent years: what changes when children become adolescents, and when adolescents become adults? J Child Psychol Psychiatry 52:1015–1025
Biederman J, Petty CR, Evans M, Small J, Faraone SV (2010) How persistent is ADHD? A controlled 10-year follow-up study of boys with ADHD. Psychiatry Res 177:299–304
Faraone SV, Biederman J, Mick E (2006) The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies. Psychol Med 36:159–165
Willcutt EG, Nigg JT, Pennington BF, Solanto MV, Rohde LA, Tannock R, Loo SK, Carlson CL, McBurnett K, Lahey BB (2012) Validity of DSM-IV attention deficit/hyperactivity disorder symptom dimensions and subtypes. J Abnorm Psychol 121:991–1010
Willoughby MT (2003) Developmental course of ADHD symptomatology during the transition from childhood to adolescence: a review with recommendations. J Child Psychol Psychiatry 44:88–106
Pingault JB, Tremblay RE, Vitaro F, Carbonneau R, Genolini C, Falissard B, Côté SM (2011) Childhood trajectories of inattention and hyperactivity and prediction of educational attainment in early adulthood: a 16-year longitudinal population-based study. Am J Psychiatry 168:1164–1170
Pingault JB, Côté SM, Galéra C, Genolini C, Falissard B, Vitaro F, Tremblay RE (2013) Childhood trajectories of inattention, hyperactivity and oppositional behaviors and prediction of substance abuse/dependence: a 15-year longitudinal population-based study. Mol Psychiatry 18:806–812
Faraone SV, Larsson H (2018) Genetics of attention deficit hyperactivity disorder. Mol Psychiatry. https://doi.org/10.1038/s41380-018-0070-0
Nikolas MA, Burt SA (2010) Genetic and environmental influences on ADHD symptom dimensions of inattention and hyperactivity: a meta-analysis. J Abnorm Psychol 119:1–17
Hay DA, Bennett KS, Levy F, Sergeant J, Swanson J (2007) A twin study of attention-deficit/hyperactivity disorder dimensions rated by the strengths and weaknesses of ADHD-symptoms and normal-behavior (SWAN) scale. Biol Psychiatry 61:700–705
Larsson JO, Larsson H, Lichtenstein P (2004) Genetic and environmental contributions to stability and change of ADHD symptoms between 8 and 13 years of age: a longitudinal twin study. J Am Acad Child Adolesc Psychiatry 43:1267–1275
Larsson H, Lichtenstein P, Larsson JO (2006) Genetic contributions to the development of ADHD subtypes from childhood to adolescence. J Am Acad Child Adolesc Psychiatry 45:973–981
Peng CZ, Grant JD, Heath AC, Reiersen AM, Mulligan RC, Anokhin AP (2016) Familial influences on the full range of variability in attention and activity levels during adolescence: a longitudinal twin study. Dev Psychopathol 28:517–526
Wood AC, Saudino KJ, Rogers H, Asherson P, Kuntsi J (2007) Genetic influences on mechanically-assessed activity level in children. J Child Psychol Psychiatry 48:695–702
Wood AC, Buitelaar J, Rijsdijk F, Asherson P, Kuntsi J (2010) Rethinking shared environment as a source of variance underlying attention-deficit/hyperactivity disorder symptoms: comment on Burt (2009). Psychol Bull 136:331–340
Plomin R (1986) Multivariate analysis and developmental behavioral genetics: developmental change as well as continuity. Behav Genet 16:25–43
Kendler KS, Gardner CO, Lichtenstein P (2008) A developmental twin study of symptoms of anxiety and depression: evidence for genetic innovation and attenuation. Psychol Med 38:1567–1575
Chang Z, Lichtenstein P, Asherson PJ, Larsson H (2013) Developmental twin study of attention problems: high heritabilities throughout development. JAMA Psychiatry 70:311–318
Price TS, Simonoff E, Asherson P, Curran S, Kuntsi J, Waldman I, Plomin R (2005) Continuity and change in preschool ADHD symptoms: longitudinal genetic analysis with contrast effects. Behav Genet 35:121–132
Kuntsi J, Rijsdijk F, Ronald A, Asherson P, Plomin R (2005) Genetic influences on the stability of attention-deficit/hyperactivity disorder symptoms from early to middle childhood. Biol Psychiatry 57:647–654
Rietveld MJ, Hudziak JJ, Bartels M, van Beijsterveldt CEM, Boomsma DI (2003) Heritability of attention problems in children: I. cross-sectional results from a study of twins, age 3–12 years. Am J Med Genet B 117:102–113
Rietveld MJ, Hudziak JJ, Bartels M, van Beijsterveldt CEM, Boomsma DI (2004) Heritability of attention problems in children: longitudinal results from a study of twins, age 3 to 12. J Child Psychol Psychiatry 45:577–588
Derks EM, Hudziak JJ, Dolan CV, van Beijsterveldt TC, Verhulst FC, Boomsma DI (2008) Genetic and environmental influences on the relation between attention problems and attention deficit hyperactivity disorder. Behav Genet 38:11–23
Kan KJ, Dolan CV, Nivard MG, Middeldorp CM, van Beijsterveldt CEM, Willemsen G, Boomsma DI (2013) Genetic and environmental stability in attention problems across the lifespan: evidence from the Netherlands Twin Register. J Am Acad Child Adolesc Psychiatry 52:12–25
Pingault J-B, Viding E, Galéra C, Greven CU, Zheng Y, Plomin R, Rijsdijk F (2015) Genetic and environmental influences on the developmental course of attention-deficit/hyperactivity disorder symptoms from childhood to adolescence. JAMA Psychiatry 72:651–658
Nadder TS, Rutter M, Silberg JL, Maes HH, Eaves LJ (2002) Genetic effects on the variation and covariation of attention deficit-hyperactivity disorder (ADHD) and oppositional-defiant disorder/conduct disorder (ODD/CD) symptomatologies across informant and occasion of measurement. Psychol Med 32:39–53
Chen J, Yu J, Zhang J, McGue M (2015) Investigating genetic and environmental contributions to adolescent externalizing behavior in a collectivistic culture: a multi-informant twin study. Psychol Med 45:1989–1997
Chen TJ, Ji CY, Wang SS, Lichtenstein P, Larsson H, Chang Z (2016) Genetic and environmental influences on the relationship between ADHD symptoms and internalizing problems: a Chinese twin study. Am J Med Genet B Neuropsychiatr Genet 171:931–937
Chen J, Li X (2013) Genetic and environmental influences on adolescent rumination and its association with depressive symptoms. J Abnorm Child Psychol 41:1289–1298
Zheng Y, Rijsdijk F, Pingault J-B, McMahon RJ, Unger JB (2016) Developmental changes in genetic and environmental influences on Chinese child and adolescent anxiety and depression. Psychol Med 46:1829–1838
Kuo PH, Lin CC, Yang HJ, Soong WT, Chen WJ (2004) A twin study of competence and behavioral/emotional problems among adolescents in Taiwan. Behav Genet 34:63–74
Zhu W, Bo Y, Li T, Deng W, Wang Y (2017) A twin study of behavioral problems and relations to genetic and environmental factors in adolescents. Chinese Ment Health J 31:127–132 (In Chinese)
Hur YM (2014) Increasing phenotypic and genetic variations in hyperactivity/inattention problems from age 3 to 13 years: a cross-sectional twin study. Twin Res Hum Genet 17:545–552
Pang Z, Ning F, Unger J, Johnson CA, Wang S, Guo Q, Cao W, Lee L (2006) The Qingdao Twin Registry: a focus on chronic disease research. Twin Res Hum Genet 9:758–762
Duan H, Ning F, Zhang D, Wang S, Zhang D, Tan Q, Tian X, Pang Z (2013) The Qingdao twin registry: a status update. Twin Res Hum Genet 16:79–85
American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington, DC
Rijsdijk FV, Sham PC (2002) Analytic approaches to twin data using structural equation models. Brief Bioinform 3:119–133
Boker S, Neale M, Maes HH, Wilde M, Spiegel M, Brick T, Spies J, Estabrook R, Kenny S, Bates T, Mehta P, Fox J (2011) OpenMx: an open source extended structural equation modeling framework. Psychometrika 76:306–317
Greven CU, Asherson P, Rijsdijk FV, Plomin R (2011) A longitudinal twin study on the association between inattentive and hyperactive-impulsive ADHD symptoms. J Abnorm Child Psychol 39:623–632
Merwood A, Greven CU, Price TS, Rijsdijk F, Kuntsi J, McLoughlin G, Larsson H, Asherson PJ (2013) Different heritabilities but shared etiological influences for parent, teacher and self-ratings of ADHD symptoms: an adolescent twin study. Psychol Med 43:1973–1984
Chen X, Chen H (2010) Children’s social functioning and adjustment in the changing Chinese society. In: Silbereisen RK, Chen X (eds) Social change and human development: concepts and results. Sage, London, pp 209–226
Chen X, French D (2008) Children’s social competence in cultural context. Annu Rev Psychol 59:591–616
Freitag CM, Rohde LA, Lempp T, Romanos M (2010) Phenotypic and measurement influences on heritability estimates in childhood ADHD. Eur Child Adolesc Psychiatry 19:311–323
Nadder TS, Silberg JL, Rutter M, Maes HH, Eaves LJ (2001) Comparison of multiple measures of ADHD symptomatology: a multivariate genetic analysis. J Child Psychol Psychiatry 42:475–486
Knafo A, Jaffee SR (2013) Gene–environment correlation in developmental psychopathology. Dev Psychopathol 25:1–6
Sonuga-Barke EJ (2003) The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev 27:593–604
Sonuga-Barke EJ (2005) Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biol Psychiatry 57:1231–1238
Verhulst B (2017) A power calculator for the classical twin design. Behav Genet 47:255–261
Greven CU, Rijsdijk FV, Plomin R (2011) A twin study of ADHD symptoms in early adolescence: hyperactivity-impulsivity and inattentiveness show substantial genetic overlap but also genetic specificity. J Abnorm Child Psychol 39:265–275
Lichtenstein P, Carlström E, Råstam M, Gillberg C, Anckarsäter H (2010) The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am J Psychiatry 167:1357–1363
Michelini G, Eley TC, Gregory AM, McAdams TA (2015) Aetiological overlap between anxiety and attention deficit hyperactivity symptom dimensions in adolescence. J Child Psychol Psychiatry 56:423–431
Merwood A, Chen W, Rijsdijk F, Skirrow C, Larsson H, Thapar A, Kuntsi J, Asherson P (2014) Genetic associations between the symptoms of attention-deficit/hyperactivity disorder and emotional lability in child and adolescent twins. J Am Acad Child Adolesc Psychiatry 53:209–220
Hudziak JJ, Derks EM, Althoff RR, Rettew DC, Boomsma DI (2005) The genetic and environmental contributions to attention deficit hyperactivity disorder as measured by the Conners' Rating Scales-Revised. Am J Psychiatry 162:1614–1620
Acknowledgements
This research was supported by the National Cancer Institute Grant #5P50CA084735 (to Dr. Unger).
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This work was approved by the appropriate ethics committee. The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. All participants and their parents gave their informed consent prior to their inclusion in the study.
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Zheng, Y., Pingault, JB., Unger, J.B. et al. Genetic and environmental influences on attention-deficit/hyperactivity disorder symptoms in Chinese adolescents: a longitudinal twin study. Eur Child Adolesc Psychiatry 29, 205–216 (2020). https://doi.org/10.1007/s00787-019-01346-0
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DOI: https://doi.org/10.1007/s00787-019-01346-0