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Sex differences in patients with Tourette syndrome

Published online by Cambridge University Press:  16 February 2022

José Fidel Baizabal-Carvallo Open the ORCID record for José Fidel Baizabal-Carvallo [Opens in a new window]  and
Joseph Jankovic
José Fidel Baizabal-Carvallo*
Affiliation:
Parkinson’s Disease Center and Movement Disorders Clinic, Department of Neurology, Baylor College of Medicine, Houston, Texas, USA Department of Sciences and Engineering, University of Guanajuato, Guanajuato, México
Joseph Jankovic
Affiliation:
Parkinson’s Disease Center and Movement Disorders Clinic, Department of Neurology, Baylor College of Medicine, Houston, Texas, USA
*
* Author for correspondence: José Fidel Baizabal-Carvallo, MD, MSc Email: baizabaljf@hotmail.com
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Abstract

Background

Tourette syndrome (TS) is a neurodevelopmental disorder characterized by the presence of motor and phonic tics. It is at least three times more common in males compared with females; however, the clinical phenomenology between sexes has not been fully examined. We aimed to contrast the clinical features between males and females with TS and chronic tic disorder.

Methods

We studied 201 consecutive patients fulfilling the diagnostic criteria for TS, persistent (or chronic) motor and vocal tic disorder and provisional tic disorder that were considered within the TS spectrum disorder. We performed blinded evaluations of video-recordings and retrospectively reviewed the clinical charts of all patients.

Results

Age ranges between 4 and 65 years. Males represented 77.6% of patients in the cohort. Overall, no differences were observed in the frequency, distribution and complexity of tics between sexes, except for a higher frequency of attention-deficit/hyperactivity disorder (ADHD) (P = .003) among males. Patients younger than 18-years old, in addition to a higher frequency of ADHD (P = .026), males had a statistically higher frequency of complex motor tics (P = .049) and earlier age at onset (P = .072) than females in the multivariate regression analysis. However, these differences were lost in patients older than 18 years, due to increased complexity of tics in females with aging.

Conclusions

A sexual dimorphism was observed between patients with TS mainly before age of 18 years, suggesting an earlier onset of some types of tics and ADHD in males compared to females.

Keywords

TicsTourette syndromesexfemaleattention-deficit/hyperactivity disorder
Type
Original Research
Information
CNS Spectrums , Volume 28 , Issue 2 , April 2023 , pp. 205 - 211
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Jankovic, J. Tourette’s syndrome. N Engl J Med. 2001;345(16):1184–1192.CrossRefGoogle ScholarPubMed
Centers for Disease Control and Prevention (CDC). Prevalence of diagnosed Tourette syndrome in persons aged 6–17 years—United States, 2007. Morb Mortal Wkly Rep (MMWR). 2009;58(21):581–585.Google Scholar
Scahill, L, Specht, M, Page, C. The prevalence of tic disorders and clinical characteristics in children. J Obsessive Compuls Relat Disord. 2014;3(4):394–400.CrossRefGoogle ScholarPubMed
Scharf, JM, Miller, LL, Gauvin, CA, Alabiso, J, Mathews, CA, Ben-Shlomo, Y. Population prevalence of Tourette syndrome: a systematic review and meta-analysis. Mov Disord. 2015;30(2):221–228.CrossRefGoogle ScholarPubMed
Groth, C. Tourette syndrome in a longitudinal perspective. Clinical course of tics and comorbidities, coexisting psychopathologies, phenotypes and predictors. Dan Med J. 2018;65(4):B5465.Google Scholar
Garcia-Delgar, B, Servera, M, Coffey, BJ, et al. Tic disorders in children and adolescents: does the clinical presentation differ in males and females? A report by the EMTICS group. Eur Child Adolesc Psychiatry. 2021. doi:10.1007/s00787-021-01751-4.Google ScholarPubMed
Robertson, MM, Eapen, V, Singer, HS, et al. Gilles de la Tourette syndrome. Nat Rev Dis Primers. 2017;3:16097.10.1038/nrdp.2016.97CrossRefGoogle ScholarPubMed
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(4):325–333.10.1001/jamapsychiatry.2014.2650CrossRefGoogle ScholarPubMed
Santangelo, SL, Pauls, DL, Goldstein, JM, Faraone, SV, Tsuang, MT, Leckman, JF. Tourette’s syndrome: what are the influences of gender and comorbid obsessive–compulsive disorder? J Am Acad Child Adolesc Psychiatry. 1994;33(6):795–804.10.1097/00004583-199407000-00004CrossRefGoogle ScholarPubMed
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(8):451–457.10.1007/s00787-012-0278-5CrossRefGoogle ScholarPubMed
Wanderer, S, Roessner, V, Freeman, R, Bock, N, Rothenberger, A, Becker, A. Relationship of obsessive–compulsive disorder to age-related comorbidity in children and adolescents with Tourette syndrome. J Dev Behav Pediatr. 2012;33(2):124–133.CrossRefGoogle ScholarPubMed
Huisman-van Dijk, HM, Matthijssen, SJMA, Stockmann, RTS, Fritz, AV, Cath, DC. Effects of comorbidity on Tourette’s tic severity and quality of life. Acta Neurol Scand. 2019;140(6):390–398.CrossRefGoogle ScholarPubMed
Meoni, S, Macerollo, A, Moro, E. Sex differences in movement disorders. Nat Rev Neurol. 2020;16(2):84–96.CrossRefGoogle ScholarPubMed
Baizabal-Carvallo, JF, Jankovic, J. Gender differences in functional movement disorders. Mov Disord Clin Pract. 2019;7(2):182–187.10.1002/mdc3.12864CrossRefGoogle ScholarPubMed
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 5th ed. Arlington, VA: American Psychiatric Association; 2013.Google Scholar
Kim, S, Greene, DJ, Bihun, EC, et al. Provisional tic disorder is not so transient. Sci Rep. 2019;9(1):3951.CrossRefGoogle Scholar
Claudio-Campos, K, Stevens, D, Koo, SW, et al. Is persistent motor or vocal tic disorder a milder form of Tourette syndrome? Mov Disord. 2021;36(8):1899–1910.CrossRefGoogle ScholarPubMed
Jankovic, J, Kurlan, R. Tourette syndrome: evolving concepts. Mov Disord. 2011;26(6):1149–1156.CrossRefGoogle ScholarPubMed
Goetz, CG, Pappert, EJ, Louis, ED, Raman, R, Leurgans, S. Advantages of a modified scoring method for the rush video-based tic rating scale. Mov Disord. 1999;14(3):502–506.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Sambrani, T, Jakubovski, E, Müller-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;10:415.10.3389/fnins.2016.00415CrossRefGoogle ScholarPubMed
Lichter, DG, Finnegan, SG. Influence of gender on Tourette syndrome beyond adolescence. Eur Psychiatry. 2015;30(2):334–340.CrossRefGoogle ScholarPubMed
Openneer, TJC, Huyser, C, Martino, D, et al.. Clinical precursors of tics: an EMTICS study. J Child Psychol Psychiatry. 2021. doi:10.1111/jcpp.13472.Google ScholarPubMed
Franklin, ME, Harrison, JP, Benavides, KL. Obsessive–compulsive and tic-related disorders. Child Adolesc Psychiatr Clin N Am. 2012;21(3):555–571.10.1016/j.chc.2012.05.008CrossRefGoogle ScholarPubMed
Martino, D, Cavanna, AE, Robertson, MM, Orth, M. Prevalence and phenomenology of eye tics in Gilles de la Tourette syndrome. J Neurol. 2012;259(10):2137–2140.CrossRefGoogle ScholarPubMed
Mercer Moss, FJ, Baddeley, R, Canagarajah, N. Eye movements to natural images as a function of sex and personality. PLoS One. 2012;7(11):e47870.10.1371/journal.pone.0047870CrossRefGoogle ScholarPubMed
Schulte, L, Hawelka, S, Pletzer, BA. Eye-movements during number comparison: associations to sex and sex hormones. Physiol Behav. 2020;227:113161.10.1016/j.physbeh.2020.113161CrossRefGoogle ScholarPubMed
Wolff, N, Luehr, I, Sender, J, et al. A DTI study on the corpus callosum of treatment-naïve boys with “pure” Tourette syndrome. Psychiatry Res Neuroimaging. 2016;247:1–8.CrossRefGoogle Scholar
Jackson, SR, Loayza, J, Crighton, M, Sigurdsson, HP, Dyke, K, Jackson, GM. The role of the insula in the generation of motor tics and the experience of the premonitory urge-to-tic in Tourette syndrome. Cortex. 2020;126:119–133.CrossRefGoogle ScholarPubMed
Eliot, L, Ahmed, A, Khan, H, Patel, J Dump the “dimorphism”: comprehensive synthesis of human brain studies reveals few male-female differences beyond size. Neurosci Biobehav Rev. 2021;125:667–697.10.1016/j.neubiorev.2021.02.026CrossRefGoogle ScholarPubMed
Baumgardner, TL, Singer, HS, Denckla, MB, et al. Corpus callosum morphology in children with Tourette syndrome and attention deficit hyperactivity disorder. Neurology. 1996;47(2):477–482.10.1212/WNL.47.2.477CrossRefGoogle ScholarPubMed
Fahim, C, Yoon, U, Das, S, et al. Somatosensory-motor bodily representation cortical thinning in Tourette: effects of tic severity, age and gender. Cortex. 2010;46(6):750–760.10.1016/j.cortex.2009.06.008CrossRefGoogle ScholarPubMed
Mostofsky, SH, Wendlandt, J, Cutting, L, Denckla, MB, Singer, HS. Corpus callosum measurements in girls with Tourette syndrome. Neurology. 1999;53(6):1345–1347.CrossRefGoogle ScholarPubMed
Zimmerman, AM, Abrams, MT, Giuliano, JD, Denckla, MB, Singer, HS. Subcortical volumes in girls with Tourette syndrome: support for a gender effect. Neurology. 2000;54(12):2224–2229.CrossRefGoogle ScholarPubMed
Luders, E, Narr, KL, Hamilton, LS, et al. Decreased callosal thickness in attention-deficit/hyperactivity disorder. Biol Psychiatry. 2009;65(1):84–88.CrossRefGoogle ScholarPubMed
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(Pt 2):472–482.CrossRefGoogle ScholarPubMed
Cui, G, Ou, Y, Chen, Y, et al. Altered global brain functional connectivity in drug-naive patients with obsessive–compulsive disorder. Front Psychiatry. 2020;11:98.CrossRefGoogle ScholarPubMed
Andersen, SL, Teicher, MH. Sex differences in dopamine receptors and their relevance to ADHD. Neurosci Biobehav Rev. 2000;24(1):137–141.CrossRefGoogle ScholarPubMed
Jankovic, J, Gelineau-Kattner, R, Davidson, A. Tourette’s syndrome in adults. Mov Disord. 2010;25(13):2171–2175.10.1002/mds.23199CrossRefGoogle ScholarPubMed
Pinares-Garcia, P, Stratikopoulos, M, Zagato, A, Loke, H, Lee, J. Sex: a significant risk factor for neurodevelopmental and neurodegenerative disorders. Brain Sci. 2018;8(8):154.10.3390/brainsci8080154CrossRefGoogle ScholarPubMed
Andersen, SL, Rutstein, M, Benzo, JM, Hostetter, JC, Teicher, MH. Sex differences in dopamine receptor overproduction and elimination. Neuroreport. 1997;8(6):1495–1498.CrossRefGoogle ScholarPubMed
Weiss, M, Worling, D, Wasdell, M. A chart review study of the inattentive and combined types of ADHD. J Atten Disord. 2003;7(1):1–9.10.1177/108705470300700101CrossRefGoogle ScholarPubMed
Levy, F, Hay, DA, Bennett, KS, McStephen, M. Gender differences in ADHD subtype comorbidity. J Am Acad Child Adolesc Psychiatry. 2005;44(4):368–376.10.1097/01.chi.0000153232.64968.c1CrossRefGoogle ScholarPubMed
Hassan, N, Cavanna, AE. The prognosis of Tourette syndrome: implications for clinical practice. Funct Neurol. 2012;27(1):23–27.Google ScholarPubMed
Burd, L, Kerbeshian, PJ, Barth, A, Klug, MG, Avery, PK, Benz, B. Long-term follow-up of an epidemiologically defined cohort of patients with Tourette syndrome. J Child Neurol. 2001;16(6):431–437.CrossRefGoogle ScholarPubMed
Cavanna, AE, David, K, Orth, M, Robertson, MM. Predictors during childhood of future health-related quality of life in adults with Gilles de la Tourette syndrome. Eur J Paediatr Neurol. 2012;16(6):605–612.10.1016/j.ejpn.2012.02.004CrossRefGoogle ScholarPubMed
Garris, J, Quigg, M. The female Tourette patient: sex differences in Tourette disorder. Neurosci Biobehav Rev. 2021;129:261–268.CrossRefGoogle ScholarPubMed
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