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Open Access 01-07-2016 | Original Contribution

The influence of comorbid oppositional defiant disorder on white matter microstructure in attention-deficit/hyperactivity disorder

Authors: Hanneke van Ewijk, Siri D. S. Noordermeer, Dirk J. Heslenfeld, Marjolein Luman, Catharina A. Hartman, Pieter J. Hoekstra, Stephen V. Faraone, Barbara Franke, Jan K. Buitelaar, J. Oosterlaan

Published in: European Child & Adolescent Psychiatry | Issue 7/2016

Abstract

Attention-deficit/hyperactivity disorder (ADHD) and oppositional defiant disorder (ODD) are highly comorbid disorders. ADHD has been associated with altered white matter (WM) microstructure, though the literature is inconsistent, which may be due to differences in the in- or exclusion of participants with comorbid ODD. WM abnormalities in ODD are still poorly understood, and it is unclear whether comorbid ODD in ADHD may have confounded the current ADHD literature. Diffusion Tensor Imaging (DTI) was used to compare fractional anisotropy (FA) and mean diffusivity (MD) between ADHD patients with (n = 42) and without (n = 117) comorbid ODD. All participants were between 8–25 years and groups did not differ in mean age or gender. Follow-up analyses were conducted to examine the role of antisocial behaviour (conduct problems) on FA and MD values in both groups. Comorbid ODD in ADHD was associated with lower FA in left frontotemporal WM, which appeared independent of ADHD symptoms. FA was negatively associated with antisocial behaviour in ADHD + ODD, but not in ADHD-only. Comorbid ODD is associated with WM abnormalities in individuals with ADHD, which appears to be independent of ADHD symptoms. Altered WM microstructure in comorbid ODD may play a role in inconsistencies in the current DTI literature in ADHD. Altered development of these tracts may contribute to social-emotional and cognitive problems in children with oppositional and antisocial behaviour.

American Psychiatric Association (2013) The Diagnostic and statistical manual of mental disorders: DSM 5. Bookpoint, US

Connor DF, Steeber J, McBurnett K (2010) A review of attention-deficit/hyperactivity disorder complicated by symptoms of oppositional defiant disorder or conduct disorder. J Dev Behav Pediatr 31(5):427–440. doi:10.1097/DBP.0b013e3181e121bd CrossRefPubMed

Nakao T, Radua J, Rubia K, Mataix-Cols D (2011) Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry 168(11):1154–1163. doi:10.1176/appi.ajp.2011.11020281 CrossRefPubMed

Cortese S, Kelly C, Chabernaud C, Proal E, Di Martino A, Milham MP, Castellanos FX (2012) Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. Am J Psychiatry 169(10):1038–1055CrossRefPubMed

van Ewijk H, Heslenfeld DJ, Zwiers MP, Faraone SV, Luman M, Hartman CA, Hoekstra P, Franke B, Buitelaar JK, Oosterlaan J (2014) Different mechanisms of white matter abnormalities in attention-deficit/hyperactivity disorder: a diffusion tensor imaging study. J Am Acad Child Adolesc Psychiatry 53(7):790.e793–799.e793. doi:10.1016/j.jaac.2014.05.001

van Ewijk H, Heslenfeld DJ, Zwiers MP, Buitelaar JK, Oosterlaan J (2012) Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neurosci Biobehav Rev 36(4):1093–1106. doi:10.1016/j.neubiorev.2012.01.003 CrossRefPubMed

Durston S, van Belle J, de Zeeuw P (2011) Differentiating frontostriatal and fronto-cerebellar circuits in attention-deficit/hyperactivity disorder. Biol Psychiatry 69(12):1178–1184CrossRefPubMed

Cortese S, Imperati D, Zhou J, Proal E, Klein RG, Mannuzza S, Ramos-Olazagasti MA, Milham MP, Kelly C, Castellanos FX (2013) White matter alterations at 33-year follow-up in adults with childhood attention-deficit/hyperactivity disorder. Biol Psychiatry 74(8):591–598. doi:10.1016/j.biopsych.2013.02.025 CrossRefPubMedPubMedCentral

de Zeeuw P, Mandl RC, Hulshoff Pol HE, van Engeland H, Durston S (2012) Decreased frontostriatal microstructural organization in attention deficit/hyperactivity disorder. Hum Brain Mapp 33(8):1941–1951. doi:10.1002/hbm.21335 CrossRefPubMed

10.

Matthys W, Vanderschuren LJ, Schutter DJ (2013) The neurobiology of oppositional defiant disorder and conduct disorder: altered functioning in three mental domains. Dev Psychopathol 25(01):193–207CrossRefPubMed

11.

Noordermeer SDS, Luman M, Oosterlaan J (Submitted) Neuroimaging in oppositional defiant disorder and conduct disorder with and without comorbid attention deficit hyperactivity disorder: a systematic review and meta-analysis (under review)

12.

Haney-Caron E, Caprihan A, Stevens MC (2014) DTI-measured white matter abnormalities in adolescents with conduct disorder. J Psychiatr Res 48(1):111–120. doi:10.1016/j.jpsychires.2013.09.015 CrossRefPubMed

13.

Passamonti L, Fairchild G, Fornito A, Goodyer IM, Nimmo-Smith I, Hagan CC, Calder AJ (2012) Abnormal anatomical connectivity between the amygdala and orbitofrontal cortex in conduct disorder. PLoS One 7(11):e48789. doi:10.1371/journal.pone.0048789 CrossRefPubMedPubMedCentral

14.

Sarkar S, Craig MC, Catani M, Dell’acqua F, Fahy T, Deeley Q, Murphy DG (2013) Frontotemporal white-matter microstructural abnormalities in adolescents with conduct disorder: a diffusion tensor imaging study. Psychol Med 43(2):401–411. doi:10.1017/S003329171200116X CrossRefPubMed

15.

Li TQ, Mathews VP, Wang Y, Dunn D, Kronenberger W (2005) Adolescents with disruptive behavior disorder investigated using an optimized MR diffusion tensor imaging protocol. Ann N Y Acad Sci 1064:184–192. doi:10.1196/annals.1340.034 CrossRefPubMed

16.

Wang Y, Horst KK, Kronenberger WG, Hummer TA, Mosier KM, Kalnin AJ, Dunn DW, Mathews VP (2012) White matter abnormalities associated with disruptive behavior disorder in adolescents with and without attention-deficit/hyperactivity disorder. Psychiatry Res 202(3):245–251. doi:10.1016/j.pscychresns.2012.01.005 CrossRefPubMed

17.

Burke JD, Loeber R, Birmaher B (2002) Oppositional defiant disorder and conduct disorder: a review of the past 10 years, part II. J Am Acad Child Adolesc Psychiatry 41(11):1275–1293. doi:10.1097/00004583-200211000-00009 CrossRefPubMed

18.

von Rhein D, Mennes M, van Ewijk H, Groenman AP, Zwiers MP, Oosterlaan J, Heslenfeld D, Franke B, Hoekstra PJ, Faraone SV (2014) The NeuroIMAGE study: a prospective phenotypic, cognitive, genetic and MRI study in children with attention-deficit/hyperactivity disorder. Design and descriptives. Eur Child Adolesc Psychiatry. doi:10.1007/s00787-014-0573-4

19.

Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36(7):980–988. doi:10.1097/00004583-199707000-00021 CrossRefPubMed

20.

Conners CK, Erhardt D, Sparrow EP (1999) Conner’s Adult ADHD Rating Scales: CAARS. Multi-Health Systems, North Tonawanda

21.

Conners CK, Sitarenios G, Parker JDA, Epstein JN (1998) Revision and restandardization of the Conners Teacher Rating Scale (CTRS-R): factor structure, reliability, and criterion validity. J Abnorm Child Psychol 26(4):279–291CrossRefPubMed

22.

Geluk CA, Jansen L, Vermeiren R, Doreleijers TA, van Domburgh L, de Bildt A, Twisk JW, Hartman CA (2012) Autistic symptoms in childhood arrestees: longitudinal association with delinquent behavior. J Child Psychol Psychiatry 53(2):160–167CrossRefPubMed

23.

Loeber R, Stouthamer-Loeber M, Van Kammen WB, Farrington DP (1989) Development of a new measure of self-reported antisocial behaviour for young children: prevalence and reliability. In: Klein M (ed) Cross-national research in self-reported crime and delinquency. Kluwer-Nijhoff, Boston, pp 203–225CrossRef

24.

Gons RA, van Norden AG, de Laat KF, van Oudheusden LJ, van Uden IW, Zwiers MP, Norris DG, de Leeuw FE (2011) Cigarette smoking is associated with reduced microstructural integrity of cerebral white matter. Brain 134(Pt 7):2116–2124. doi:10.1093/brain/awr145 CrossRefPubMed

25.

van Ewijk H, Groenman AP, Zwiers MP, Heslenfeld DJ, Faraone SV, Hartman CA, Luman M, Greven CU, Hoekstra PJ, Franke B (2015) Smoking and the developing brain: altered white matter microstructure in attention‐deficit/hyperactivity disorder and healthy controls. Hum Brain Mapp 36(3):1180–1189CrossRefPubMed

26.

Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31(4):1487–1505. doi:10.1016/j.neuroimage.2006.02.024 CrossRefPubMed

27.

Cooper M, Thapar A, Jones DK (2014) White matter microstructure predicts autistic traits in attention-deficit/hyperactivity disorder. J Autism Dev Disord 44(11):2742–2754. doi:10.1007/s10803-014-2131-9 CrossRefPubMedPubMedCentral

28.

Schmithorst VJ, Wilke M, Dardzinski BJ, Holland SK (2005) Cognitive functions correlate with white matter architecture in a normal pediatric population: a diffusion tensor MRI study. Hum Brain Mapp 26(2):139–147CrossRefPubMedPubMedCentral

29.

Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254. doi:10.1016/j.neuroimage.2012.06.081 CrossRefPubMed

30.

Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4(3):316–329CrossRefPubMedPubMedCentral

31.

Vloet TD, Konrad K, Huebner T, Herpertz S, Herpertz-Dahlmann B (2008) Structural and functional MRI-findings in children and adolescents with antisocial behavior. Behav Sci Law 26(1):99–111CrossRefPubMed

32.

Rubia K (2011) “Cool” inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus “hot” ventromedial orbitofrontal-limbic dysfunction in conduct disorder: a review. Biol Psychiatry 69(12):e69–e87. doi:10.1016/j.biopsych.2010.09.023 CrossRefPubMed

33.

Finger EC, Marsh AA, Blair KS, Reid ME, Sims C, Ng P, Pine DS, Blair RJR (2011) Disrupted reinforcement signaling in the orbitofrontal cortex and caudate in youths with conduct disorder or oppositional defiant disorder and a high level of psychopathic traits. Am J Psychiatry 168(2):152–162CrossRefPubMed

34.

Blair RJ (2005) The roles of orbital frontal cortex in the modulation of antisocial behavior. Brain Cogn 55(1):198–208. doi:10.1016/S0278-2626(03)00276-8 CrossRef

35.

Von Der Heide RJ, Skipper LM, Klobusicky E, Olson IR (2013) Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. Brain 136(Pt 6):1692–1707. doi:10.1093/brain/awt094 CrossRef

36.

Loeber R, Burke JD, Lahey BB, Winters A, Zera M (2000) Oppositional defiant and conduct disorder: a review of the past 10 years, part I. J Am Acad Child Adolesc Psychiatry 39(12):1468–1484CrossRefPubMed

37.

Paus T, Pesaresi M, French L (2014) White matter as a transport system. Neuroscience. doi:10.1016/j.neuroscience.2014.01.055 PubMed

38.

Hogan AE (1999) Cognitive functioning in children with oppositional defiant disorder and conduct disorder. In: Quay HC, Hogan AE (eds) Handbook of disruptive behavior disorders. Springer, New York, pp 317–335

39.

Kim J, Kim YW, Park CI, Park ES, Kim HH, Lee SK, Kim DI (2006) Diffusion-tensor magnetic resonance imaging in children with language impairment. NeuroReport 17(12):1279–1282. doi:10.1097/01.wnr.0000230516.86090.67 CrossRefPubMed

40.

Fryer SL, Frank LR, Spadoni AD, Theilmann RJ, Nagel BJ, Schweinsburg AD, Tapert SF (2008) Microstructural integrity of the corpus callosum linked with neuropsychological performance in adolescents. Brain Cogn 67(2):225–233. doi:10.1016/j.bandc.2008.01.009 CrossRefPubMedPubMedCentral

41.

Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128(Pt 4):797–810. doi:10.1093/brain/awh423 CrossRefPubMed

42.

Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houde O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30(4):1414–1432. doi:10.1016/j.neuroimage.2005.11.002 CrossRefPubMed

Title: The influence of comorbid oppositional defiant disorder on white matter microstructure in attention-deficit/hyperactivity disorder
Authors: Hanneke van Ewijk
Siri D. S. Noordermeer
Dirk J. Heslenfeld
Marjolein Luman
Catharina A. Hartman
Pieter J. Hoekstra
Stephen V. Faraone
Barbara Franke
Jan K. Buitelaar
J. Oosterlaan
Publication date: 01-07-2016
Publisher: Springer Berlin Heidelberg
Published in: European Child & Adolescent Psychiatry / Issue 7/2016
Print ISSN: 1018-8827
Electronic ISSN: 1435-165X
DOI: https://doi.org/10.1007/s00787-015-0784-3

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The influence of comorbid oppositional defiant disorder on white matter microstructure in attention-deficit/hyperactivity disorder

Abstract

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