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Child and Adolescent Psychiatry and Mental Health

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Open Access 01-12-2017 | Review

Tourette syndrome and other neurodevelopmental disorders: a comprehensive review

Authors: Elena Cravedi, Emmanuelle Deniau, Marianna Giannitelli, Jean Xavier, Andreas Hartmann, David Cohen

Published in: Child and Adolescent Psychiatry and Mental Health | Issue 1/2017

Abstract

Gilles de la Tourette syndrome (TS) is a complex developmental neuropsychiatric condition in which motor manifestations are often accompanied by comorbid conditions that impact the patient’s quality of life. In the DSM-5, TS belongs to the “neurodevelopmental disorders” group, together with other neurodevelopmental conditions, frequently co-occurring. In this study, we searched the PubMed database using a combination of keywords associating TS and all neurodevelopmental diagnoses. From 1009 original reports, we identified 36 studies addressing TS and neurodevelopmental comorbidities. The available evidence suggests the following: (1) neurodevelopmental comorbidities in TS are the rule, rather than the exception; (2) attention deficit/hyperactivity disorder (ADHD) is the most frequent; (3) there is a continuum from a simple (TS + ADHD or/and learning disorder) to a more complex phenotype (TS + autism spectrum disorder). We conclude that a prompt diagnosis and a detailed description of TS comorbidities are necessary not only to understand the aetiological basis of neurodevelopmental disorders but also to address specific rehabilitative and therapeutic approaches.

American Psychiatric Association. DSM-V. St. Louis: American Psychiatric Association; 2013. https://doi.org/10.1176/appi.books.9780890425596.744053.

Robertson MM. A personal 35 year perspective on Gilles de la Tourette syndrome: prevalence, phenomenology, comorbidities, and coexistent psychopathologies. Lancet Psychiatry. 2015;2:68–87. https://doi.org/10.1016/S2215-0366(14)00132-1.CrossRefPubMed

Scharf JM, Miller LL, Gauvin CA, et al. Population prevalence of Tourette syndrome: a systematic review and meta-analysis. Mov Disord. 2015;30:221–8. https://doi.org/10.1002/mds.26089.CrossRefPubMed

Tagwerker Gloor F, Walitza S. Tic disorders and Tourette syndrome: current concepts of etiology and treatment in children and adolescents. Neuropediatrics. 2016;47:84–96. https://doi.org/10.1055/s-0035-1570492.CrossRefPubMed

Forde NJ, Kanaan AS, Widomska J, et al. TS-EUROTRAIN: a European-wide investigation and training network on the etiology and pathophysiology of Gilles de la Tourette syndrome. Front Neurosci. 2016;10:384. https://doi.org/10.3389/fnins.2016.00384.CrossRefPubMedPubMedCentral

Worbe Y, Marrakchi-Kacem L, Lecomte S, et al. Altered structural connectivity of cortico-striato-pallido-thalamic networks in Gilles de la Tourette syndrome. Brain. 2015;138:472–82. https://doi.org/10.1093/brain/awu311.CrossRefPubMed

Georgitsi M, Willsey AJ, Mathews CA, et al. The genetic etiology of Tourette syndrome: large-scale collaborative efforts on the precipice of discovery. Front Neurosci. 2016;10:351. https://doi.org/10.3389/fnins.2016.00351.CrossRefPubMedPubMedCentral

Martino D, Zis P, Buttiglione M. The role of immune mechanisms in Tourette syndrome. Brain Res. 2015;1617:126–43. https://doi.org/10.1016/j.brainres.2014.04.027.CrossRefPubMed

Hirschtritt ME, Lee PC, Pauls DL, et al. Lifetime prevalence, age of risk, and genetic relationships of comorbid psychiatric disorders in Tourette syndrome. JAMA psychiatry. 2015;72:325–33. https://doi.org/10.1001/jamapsychiatry.2014.2650.CrossRefPubMedPubMedCentral

10.

Robertson MM, Cavanna AE. The Gilles de la Tourette syndrome: a principal component factor analytic study of a large pedigree. Psychiatr Genet. 2007;17:143–52. https://doi.org/10.1097/YPG.0b013e328015b937.CrossRefPubMed

11.

Huisman-van Dijk HM, van de Schoot R, Rijkeboer MM, et al. The relationship between tics, OC, ADHD and autism symptoms: a cross-disorder symptom analysis in Gilles de la Tourette syndrome patients and family-members. Psychiatry Res. 2016;237:138–46. https://doi.org/10.1016/j.psychres.2016.01.051.CrossRefPubMedPubMedCentral

12.

Eapen V, Snedden C, Črnčec R, et al. Tourette syndrome, co-morbidities and quality of life. ANZ J Psychiatry. 2016;50(82–93):12p. https://doi.org/10.1177/0004867415594429.

13.

Cukier HN, Dueker ND, Slifer SH, et al. Exome sequencing of extended families with autism reveals genes shared across neurodevelopmental and neuropsychiatric disorders. Mol Autism. 2014;5:1. https://doi.org/10.1186/2040-2392-5-1.CrossRefPubMedPubMedCentral

14.

Kern JK, Geier DA, King PG, et al. Shared brain connectivity issues, symptoms, and comorbidities in autism spectrum disorder, attention deficit/hyperactivity disorder, and Tourette syndrome. Brain Connect. 2015;5:321–35. https://doi.org/10.1089/brain.2014.0324.CrossRefPubMed

15.

Worbe Y. Neuroimaging signature of neuropsychiatric disorders. Curr Opin Neurol. 2015;28:358–64. https://doi.org/10.1097/WCO.0000000000000220.CrossRefPubMed

16.

Cominings DE, Himes JA, Comings BG. An epidemiologic study of Tourette’s syndrome in a single school district. J Clin Psychiatry. 1990;51:463–9.

17.

Apter A, Pauls DL, Bleich A, et al. An epidemiologic study of Gilles de la Tourette’s syndrome in Israel. Arch Gen Psychiatry. 1993;50:734–8.CrossRefPubMed

18.

Wang HS, Kuo MF. Tourette’s syndrome in Taiwan: an epidemiological study of tic disorders in an elementary school at Taipei County. Brain Dev. 2003. https://doi.org/10.1016/S0387-7604(03)90005-2.

19.

Kadesjö B, Gillberg C. Tourette’s disorder: epidemiology and comorbidity in primary school children. J Am Acad Child Adolesc Psychiatry. 2000;39:548–55. https://doi.org/10.1097/00004583-200005000-00007.CrossRefPubMed

20.

Khalifa N, von Knorring A-L. Psychopathology in a Swedish population of school children with tic disorders. J Am Acad Child Adolesc Psychiatry. 2006;45:1346–53. https://doi.org/10.1097/01.chi.0000251210.98749.83.CrossRefPubMed

21.

American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-IV-TR). 4th ed. St. Louis: American Psychiatric Association; 2000. https://doi.org/10.1176/appi.books.9780890420249.dsm-iv-tr.

22.

Polanczyk GV, Willcutt EG, Salum GA, et al. ADHD prevalence estimates across three decades: an updated systematic review and meta-regression analysis. Int J Epidemiol. 2014;43:434–42. https://doi.org/10.1093/ije/dyt261.CrossRefPubMedPubMedCentral

23.

Faraone SV, Sergeant J, Gillberg C, Biederman J. The worldwide prevalence of ADHD: is it an American condition? World Psychiatry. 2003;2:104–13. https://doi.org/10.1176/ajp.2007.164.6.942.PubMedPubMedCentral

24.

Shapiro AK, Shapiro E, Wayne HL. The symptomatology and diagnosis of Gilles de la Tourette’s syndrome. J Am Acad Child Psychiatry. 1973;12:702–23.CrossRefPubMed

25.

Freeman RD. Tic disorders and ADHD: answers from a world-wide clinical dataset on Tourette syndrome. Eur Child Adolesc Psychiatry. 2007;16:15–23. https://doi.org/10.1007/s00787-007-1003-7.CrossRefPubMed

26.

Sambrani T, Jakubovski E, Muller-Vahl KR. New insights into clinical characteristics of Gilles de la Tourette syndrome: findings in 1032 patients from a single German center. Front Neurosci. 2016;10:415. https://doi.org/10.3389/fnins.2016.00415.CrossRefPubMedPubMedCentral

27.

Debes NM, Hjalgrim H, Skov L. Clinical aspects of Tourette syndrome. Ugeskr Laeger. 2008;170:2701–3.PubMed

28.

Specht MW, Woods DW, Piacentini J, et al. Clinical characteristics of children and adolescents with a primary tic disorder. J Dev Phys Disabil. 2011;23:15–31. https://doi.org/10.1007/s10882-010-9223-z.CrossRefPubMedPubMedCentral

29.

Lebowitz ER, Motlagh MG, Katsovich L, et al. Tourette syndrome in youth with and without obsessive compulsive disorder and attention deficit hyperactivity disorder. Eur Child Adolesc Psychiatry. 2012;21:451–7. https://doi.org/10.1007/s00787-012-0278-5.CrossRefPubMedPubMedCentral

30.

Byler DL, Chan L, Lehman E, et al. Tourette syndrome: a general pediatrician’s 35-year experience at a single center with follow-up in adulthood. Clin Pediatr (Phila). 2015;54:138–44. https://doi.org/10.1177/0009922814550396.CrossRef

31.

Altarac M, Saroha E. Lifetime prevalence of learning disability among US children. Pediatrics. 2007;119(Suppl):S77–83. https://doi.org/10.1542/peds.2006-2089L.CrossRefPubMed

32.

Comings DE, Comings BG. Tourette’s syndrome and attention deficit disorder with hyperactivity. Arch Gen Psychiatry. 1987;44:1023–6.CrossRefPubMed

33.

Teive HA, Germiniani FM, Della Coletta MV, Werneck LC. Tics and Tourette syndrome: clinical evaluation of 44 cases. Arq Neuropsiquiatr. 2001;59:725–8.CrossRefPubMed

34.

Yeates KO, Bornstein RA. Neuropsychological correlates of learning disability subtypes in children with Tourette’s syndrome. J Int Neuropsychol Soc. 1996;2:375–82.CrossRefPubMed

35.

Burd L, Freeman RD, Klug MG, Kerbeshian J. Tourette syndrome and learning disabilities. BMC Pediatr. 2005;5:34. https://doi.org/10.1186/1471-2431-5-34.CrossRefPubMedPubMedCentral

36.

Freeman RD, Fast DK, Burd L, et al. An international perspective on Tourette syndrome: selected findings from 3,500 individuals in 22 countries. Dev Med Child Neurol. 2000;42:436–47.CrossRefPubMed

37.

Elsabbagh M, Divan G, Koh YJ, et al. Global prevalence of autism and other pervasive developmental disorders. Autism Res. 2012;5:160–79. https://doi.org/10.1002/aur.239.CrossRefPubMedPubMedCentral

38.

Burd L, Fisher WW, Kerbeshian J, Arnold ME. Is development of Tourette disorder a marker for improvement in patients with autism and other pervasive developmental disorders? J Am Acad Child Adolesc Psychiatry. 1987;26:162–5. https://doi.org/10.1097/00004583-198703000-00006.CrossRefPubMed

39.

Comings DE, Comings BG. Clinical and genetic relationships between autism-pervasive developmental disorder and Tourette syndrome: a study of 19 cases. Am J Med Genet. 1991;39:180–91.CrossRefPubMed

40.

Marriage K, Miles T, Stokes D, Davey M. Clinical and research implications of the co-occurrence of Asperger’s and Tourette syndromes. ANZ J Psychiatry. 1993;27:666–72. https://doi.org/10.3109/00048679309075829.

41.

Sverd J, Montero G, Gurevich N. Brief report: cases for an association between Tourette syndrome, autistic disorder, and schizophrenia-like disorder. J Autism Dev Disord. 1993;23:407–13. https://doi.org/10.1007/BF01046229.CrossRefPubMed

42.

Kano YO. Tourette’s disorder coupled with infantile autism: a prospective study of two boys. Jpn J Psychiatry Neurol. 1988;42:49–57.PubMed

43.

Baron-Cohen S, Scahill VL, Izaguirre D, et al. The prevalence of Gilles de la Tourette syndrome in children and adolescents with autism: a large scale study. Psychol Med. 1999;29:1151–9.CrossRefPubMed

44.

Canitano R, Vivanti G. Tics and Tourette syndrome in autism spectrum disorders. Autism. 2007;11:19–28. https://doi.org/10.1177/1362361307070992.CrossRefPubMed

45.

Burd L, Li Q, Kerbeshian J, et al. Tourette syndrome and comorbid pervasive developmental disorders. J Child Neurol. 2009;24:170–5. https://doi.org/10.1177/0883073808322666.CrossRefPubMed

46.

Darrow SM, Grados M, Sandor P, et al. Autism spectrum symptoms in a Tourette’s disorder sample. J Am Acad Child Adolesc Psychiatry. 2017;56(610–617):e1. https://doi.org/10.1016/j.jaac.2017.05.002.

47.

Clarke RA, Lee S, Eapen V. Pathogenetic model for Tourette syndrome delineates overlap with related neurodevelopmental disorders including autism. Transl Psychiatry. 2012;2:e158. https://doi.org/10.1038/tp.2012.75.CrossRefPubMedPubMedCentral

48.

Willcutt EG, Pennington BF, Duncan L, et al. Understanding the complex etiologies of developmental disorders: behavioral and molecular genetic approaches. J Dev Behav Pediatr. 2010;31:533–44. https://doi.org/10.1097/DBP.0b013e3181ef42a1.CrossRefPubMedPubMedCentral

49.

Gillberg C. The ESSENCE in child psychiatry: early symptomatic syndromes eliciting neurodevelopmental clinical examinations. Res Dev Disabil. 2010;31:1543–51. https://doi.org/10.1016/j.ridd.2010.06.002.CrossRefPubMed

50.

Cohen DJ, Paul R, Volkmar FR. Issues in the classification of pervasive and other developmental disorders: toward DSM-IV. J Am Acad Child Psychiatry. 1986;25:213–20. https://doi.org/10.1016/S0002-7138(09)60228-4.CrossRefPubMed

51.

Roessner V, Plessen KJ, Rothenberger A, et al. European clinical guidelines for Tourette syndrome and other tic disorders. Part II: pharmacological treatment. Eur Child Adolesc Psychiatry. 2011;20:173–96. https://doi.org/10.1007/s00787-011-0163-7.CrossRefPubMedPubMedCentral

52.

Hartmann A, Martino D, Murphy T. Gilles de la Tourette syndrome—a treatable condition? Rev Neurol (Paris). 2016;172:446–54. https://doi.org/10.1016/j.neurol.2016.07.004.CrossRef

53.

Verdellen C, van de Griendt J, Hartmann A, Murphy T. European clinical guidelines for Tourette syndrome and other tic disorders. Part III: behavioural and psychosocial interventions. Eur Child Adolesc Psychiatry. 2011;20:197–207. https://doi.org/10.1007/s00787-011-0167-3.CrossRefPubMed

54.

Chee KY, Sachdev P. The clinical features of Tourette’s disorder: an Australian study using a structured interview schedule. ANZ J Psychiatry. 1994;28:313–8. https://doi.org/10.1080/00048679409075645.

55.

Abwender DA, Como PG, Kurlan R, et al. School problems in Tourette’s syndrome. Arch Neurol. 1996;53:509–11.CrossRefPubMed

56.

Cardoso F, Veado CC, de Oliveira JT. A Brazilian cohort of patients with Tourette’s syndrome. J Neurol Neurosurg Psychiatry. 1996;60:209–12.CrossRefPubMedPubMedCentral

57.

Schuerholz LJ, Baumgardner TL, Singer HS, et al. Neuropsychological status of children with Tourette’s syndrome with and without attention deficit hyperactivity disorder. Neurology. 1996;46:958–65.CrossRefPubMed

58.

Wodrich DL, Benjamin E, Lachar D. Tourette’s syndrome and psychopathology in a child psychiatry setting. J Am Acad Child Adolesc Psychiatry. 1997;36:1618–24. https://doi.org/10.1016/S0890-8567(09)66574-6.PubMed

59.

Kano Y, Ohta M, Nagai Y. Clinical characteristics of Tourette syndrome. Psychiatry Clin Neurosci. 1998;52:51–7. https://doi.org/10.1111/j.1440-1819.1998.tb00972.x.CrossRefPubMed

60.

Saccomani L, Fabiana V, Manuela B, Giambattista R. Tourette syndrome and chronic tics in a sample of children and adolescents. Brain Dev. 2005;27:349–52. https://doi.org/10.1016/j.braindev.2004.09.007.CrossRefPubMed

61.

Termine C, Balottin U, Rossi G, et al. Psychopathology in children and adolescents with Tourette’s syndrome: a controlled study. Brain Dev. 2006;28:69–75. https://doi.org/10.1016/j.braindev.2005.04.006.CrossRefPubMed

62.

Janik P, Kalbarczyk A, Sitek M. Clinical analysis of Gilles de la Tourette syndrome based on 126 cases. Neurol Neurochir Pol. 2007;41:381–7.PubMed

63.

Roessner V, Becker A, Banaschewski T, et al. Developmental psychopathology of children and adolescents with Tourette syndrome—impact of ADHD. Eur Child Adolesc Psychiatry. 2007;16:24–35. https://doi.org/10.1007/s00787-007-1004-6.CrossRefPubMed

64.

Robertson MM, Althoff RR, Hafez A, Pauls DL. Principal components analysis of a large cohort with Tourette syndrome. Br J Psychiatry. 2008;193:31–6. https://doi.org/10.1192/bjp.bp.107.039909.CrossRefPubMed

65.

Ghanizadeh A, Mosallaei S. Psychiatric disorders and behavioral problems in children and adolescents with Tourette syndrome. Brain Dev. 2009;31:15–9. https://doi.org/10.1016/j.braindev.2008.03.010.CrossRefPubMed

66.

Gorman DA, Thompson N, Plessen KJ, et al. Psychosocial outcome and psychiatric comorbidity in older adolescents with Tourette syndrome: controlled study. Br J Psychiatry. 2010;197:36–44. https://doi.org/10.1192/bjp.bp.109.071050.CrossRefPubMedPubMedCentral

67.

Rizzo R, Gulisano M, Pellico A, et al. Tourette syndrome and comorbid conditions: a spectrum of different severities and complexities. J Child Neurol. 2014;29:1383–9. https://doi.org/10.1177/0883073814534317.CrossRefPubMed

Title: Tourette syndrome and other neurodevelopmental disorders: a comprehensive review
Authors: Elena Cravedi
Emmanuelle Deniau
Marianna Giannitelli
Jean Xavier
Andreas Hartmann
David Cohen
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Child and Adolescent Psychiatry and Mental Health / Issue 1/2017
Electronic ISSN: 1753-2000
DOI: https://doi.org/10.1186/s13034-017-0196-x

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Springer Medicine

Tourette syndrome and other neurodevelopmental disorders: a comprehensive review

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