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Tic disorders in children and adolescents: does the clinical presentation differ in males and females? A report by the EMTICS group

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Abstract

Tic disorders have a strong male predominance, with a male-to-female ratio of 4:1 in Tourette syndrome (TS) and 2:1 in persistent tic disorders. In other neurodevelopmental conditions, such as autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD), the disparity in sex distribution has been partially related to differences in symptom presentation between males and females. In tic disorders, however, little research has been conducted on this topic, probably due to the limited access to large samples with a significant proportion of females. The aim of this study was to describe sex differences in the clinical presentation of tic disorders in children and adolescents in one of the largest pediatric samples with TS/persistent tic disorders (n = 709, 23.3% females) recruited as part of the European Multicenter Tics in Children Study (EMTICS). Validated measures assessed the severity of tics and comorbid psychiatric symptoms. Using mixed-effect models, we found that sex had a significant influence on the severity of tics, ADHD symptoms, ASD symptoms, and emotional problems. Males had more severe symptoms than females, except for emotional problems. We also observed a statistically significant interaction between sex and age on the severity of tics and compulsions, with females showing higher symptom severity with increasing age than males. These findings indicate that the clinical presentation of TS/persistent tic disorders varies with sex. Males seem to exhibit a more noticeable pattern of clinical symptoms at a younger age that may contribute to their earlier detection in comparison to females.

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Fig. 1

* statistical significant at 0.05 level. YGTSS Yale Global Tics Severity Scale, CY-BOCS Children’s Yale-Brown Obsessive Compulsive Scale, ADHD Attention/Deficit and Hyperactivity Disorder, SNAP-IV Swanson Nolan and Pelham-IV rating scale, ASD Autism Spectrum Disorder, ASSQ Autism Spectrum Screening Questionnaire, SDQ Strengths and Difficulties Questionnaire

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Acknowledgements

The authors are deeply grateful to all children and their parents who willingly participated to make this research possible. This research was supported by the Deutsche Forschungsgemeinschaft (DFG): projects 1692/3-1, 4-1, SFB 936, and FOR 2698 (project numbers 396914663, 396577296, 396474989) (Münchau). We thank all colleagues at the various study centers who contributed to data collection: Julie E. Bruun, Judy Grejsen, Christine L. Ommundsen, Mette Rubæk (Capital Region Psychiatry, Copenhagen, Denmark); Benjamin Bodmer, Stephanie Enghardt (TUD Dresden, Germany); Stefanie Bokemeyer, Christiane Driedger-Garbe, Cornelia Reichert (MHH Hannover, Germany); Jenny Schmalfeld (Lübeck University, Germany); Victoria L. Turner, Martin L. Woods (Evelina London Children’s Hospital, United Kingdom); Franciska Gergye, Margit Kovacs, Reka Vidomusz (Vadaskert Budapest, Hungary); Silvana Fennig, Ella Gev, Matan Nahon, Danny Horesh, Chen Regev, Tomer Simcha, (Tel Aviv, Petah-Tikva, Israel); Els van den Ban, Sebastian F.T.M. de Bruijn, Nicole Driessen, Andreas Lamerz, Marieke Messchendorp, Judith J.G. Rath, Nadine Schalk, Deborah Sival, Noor Tromp, Frank Visscher and the Stichting Gilles de la Tourettes (UMCG Groningen, Netherlands); Maria Teresa Cáceres, Fátima Carrillo, Pilar Gómez-Garre, Laura Vargas, Ángela Periañez Vasco (Hospital Virgen del Rocío, Seville, Spain); Giuseppe Gagliardi (ASL Bari, Italy); Paolo Roazzi, Marco Tallon (ISS Rome, Italy); Maria Gariup, Marina Redondo (Hospital Clinic Barcelona, Spain); and all who may not have been mentioned. EMTICS group authorship/appendix: EMTICS group members are Alan Apter1, Valentina Baglioni2, Juliane Ball3, Noa Benaroya-Milshtein1, Emese Bognar4,5, Bianka Burger6,7, Judith Buse8, Francesco Cardona2, Marta Correa Vela9, Nanette M. Debes10, Andrea Dietrich11, Maria Cristina Ferro12, Carolin Fremer13, Blanca Garcia-Delgar14, Mariangela Gulisano12, Annelieke Hagen15,16, Julie Hagstrøm17, Tammy J. Hedderly18, Isobel Heyman19, Pieter J. Hoekstra11, Chaim Huyser15,16, Marcos Madruga-Garrido20, Anna Marotta21, Davide Martino22, Pablo Mir9, Astrid Morer14,23,24, Norbert Müller6,7, Kirsten Müller-Vahl13, Alexander Münchau25, Peter Nagy4,26, Valeria Neri2, Thaïra J.C. Openneer11, Alessandra Pellico12, Kerstin J. Plessen17,27, Cesare Porcelli21, Renata Rizzo12, Veit Roessner8, Daphna Ruhrman1, Jaana M.L. Schnell6, Paola Rosaria Silvestri2, Liselotte Skov10, Tamar Steinberg1, Friederike Tagwerker Gloor3, Zsanett Tarnok4, Susanne Walitza3, Elif Weidinger 6. 1Child and Adolescent Psychiatry Department, Schneider Children's Medical Center of Israel, affiliated to Sackler Faculty of Medicine, Tel Aviv University, Petah-Tikva, Israel. 2University La Sapienza of Rome, Department of Human Neurosciences, Rome, Italy. 3Clinic of Child and Adolescent Psychiatry and Psychotherapy, University of Zurich, Zurich, Switzerland. 4Vadaskert Child and Adolescent Psychiatric Hospital, Budapest, Hungary. 5Semmelweis University, Bókay Children's Clinic, Budapest, Hungary. 6Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany. 7Marion von Tessin Memory-Zentrum gGmbH, Munich, Germany. 8Department of Child and Adolescent Psychiatry, Medical Faculty Carl Gustav Carus, TU Dresden, Dresden, Germany. 9Unidad de Trastornos del Movimiento, Servicio de Neurología y Neurofisiología Clinica. Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocio/CSIC/Universidad de Sevilla, Seville, Spain. 10Paediatric Department, Herlev University Hospital, Herlev, Denmark. 11University of Groningen, University Medical Center Groningen, Department of Child and Adolescent Psychiatry, Groningen, The Netherlands. 12Child Neuropsychiatry Section, Department of Clinical and Experimental Medicine, School of Medicine, Catania University, Catania, Italy. 13Clinic of Psychiatry, Socialpsychiatry and Psychotherapy, Hannover Medical School, Hannover, Germany. 14Department of Child and Adolescent Psychiatry and Psychology, Institute of Neurosciences, Hospital Clinic Universitari, Barcelona, Spain. 15De Bascule, Academic Center for Child and Adolescent Psychiatry, Amsterdam, The Netherlands. 16Academic Medical Center, Department of Child and Adolescent Psychiatry, Amsterdam, The Netherlands. 17Child and Adolescent Mental Health Center, Mental Health Services, Capital Region of Denmark and University of Copenhagen, Copenhagen, Denmark. 18Evelina London Children’s Hospital GSTT, Kings Health Partners AHSC, London, UK. 19 Great Ormond Street Hospital for Children, and UCL Institute of Child Health, London, UK. 20Sección de Neuropediatría, Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla, Seville, Spain. 21Azienda Sanitaria Locale di Bari, Mental Health Department, Child and Adolescent Service of Bari Metropolitan Area, Bari, Italy. 22Department of Clinical Neurosciences, University of Calgary, Calgary, Canada. 23Institut d'Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain. 24Centro de Investigacion en Red de Salud Mental (CIBERSAM), Instituto Carlos III, Spain. 25Institute of Systems Motor Science, University of Lübeck, Lübeck, Germany. 26Bethesda Children's Hospital, Budapest, Hungary. 27Division of Child and Adolescent Psychiatry, Department of Psychiatry, Lausanne University Hospital, Lausanne, Switzerland

Funding

This project has received funding from the European Union's Seventh Framework Program for Research, technological development and demonstration under grant agreement no 278367.

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Author notes

  1. Andrea Dietrich and Astrid Morer contributed equally.

Authors and Affiliations

  1. Department of Child and Adolescent Psychiatry and Psychology, Institute of Neurosciences, Hospital Clinic Universitari, c/ Villarroel 170, Section 11 Floor 3, 08036, Barcelona, Spain

    Blanca Garcia-Delgar, Luisa Lázaro & Astrid Morer

  2. Departments of Psychology and Research Institute on Health Sciences, University of the Balearic Islands, Palma, Spain

    Mateu Servera

  3. Division of Child and Adolescent Psychiatry, Department of Psychiatry and Behavioral Sciences, Leonard M. Miller School of Medicine, University of Miami, Miami, FL, USA

    Barbara J. Coffey

  4. University of Barcelona, Barcelona, Spain

    Luisa Lázaro & Astrid Morer

  5. Institut D’Investigacions Biomediques August Pi I Sunyer (IDIBAPS), Barcelona, Spain

    Luisa Lázaro & Astrid Morer

  6. Centro de Investigacion en Red de Salud Mental (CIBERSAM), Instituto Carlos III, Madrid, Spain

    Luisa Lázaro & Astrid Morer

  7. Department of Child and Adolescent Psychiatry, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

    Thaïra Openneer, Pieter J. Hoekstra & Andrea Dietrich

  8. Child and Adolescent Psychiatry Department, Schneider Children’s Medical Center of Israel, affiliated to Sackler Faculty of Medicine, Tel Aviv University, Petah-Tikva, Israel

    Noa Benaroya-Milshtein & Tami Steinberg

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  1. Blanca Garcia-Delgar
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Consortia

the EMTICS collaborative group

  • Alan Apter
  • , Valentina Baglioni
  • , Juliane Ball
  • , Noa Benaroya-Milshtein
  • , Emese Bognar
  • , Bianka Burger
  • , Judith Buse
  • , Francesco Cardona
  • , Marta Correa Vela
  • , Nanette M. Debes
  • , Andrea Dietrich
  • , Maria Cristina Ferro
  • , Carolin Fremer
  • , Blanca Garcia-Delgar
  • , Mariangela Gulisano
  • , Annelieke Hagen
  • , Julie Hagstrøm
  • , Tammy J. Hedderly
  • , Isobel Heyman
  • , Pieter J. Hoekstra
  • , Chaim Huyser
  • , Marcos Madruga-Garrido
  • , Anna Marotta
  • , Davide Martino
  • , Pablo Mir
  • , Astrid Morer
  • , Norbert Müller
  • , Kirsten Müller-Vahl
  • , Alexander Münchau
  • , Peter Nagy
  • , Valeria Neri
  • , Thaïra J. C. Openneer
  • , Alessandra Pellico
  • , Kerstin J. Plessen
  • , Cesare Porcelli
  • , Renata Rizzo
  • , Veit Roessner
  • , Daphna Ruhrman
  • , Jaana M. L. Schnell
  • , Paola Rosaria Silvestri
  • , Liselotte Skov
  • , Tamar Steinberg
  • , Friederike Tagwerker Gloor
  • , Zsanett Tarnok
  • , Susanne Walitza
  •  & Elif Weidinger

Corresponding author

Correspondence to Blanca Garcia-Delgar.

Ethics declarations

Conflict of interest

Coffey is on the Scientific Advisory Board of Abide Therapeutics and Teva/ Nuvelution, has received honoraria from the American Academy of Child and Adolescent Psychiatry, Partners Healthcare, Harvard Medical School, Teva, CME Outfitters, University of Cincinnati, University of Texas Medical Branch, and University of Florida, and has received research support from Teva/ Nuvelution, Inc., Neurocrine Biosciences, Emalex, the National Institute of Mental Health (Grant No. 5R01MH115959-02), and University of California San Francisco. Müller-Vahl received funding for research from the EU (FP7-PEOPLE-2012-ITN No. 316978), the German Research Society (DFG: GZ MU 1527/3–1), the German Ministry of Education and Research (BMBF: 01KG1421), the National Institute of Mental Health (NIMH), GW, Almirall, Abide Therapeutics, and Therapix Biosiences, and consultant’s honoraria from Abide Therapeutics, Fundacion Canna, and Therapix Biosiences. On behalf of all other authors, the corresponding author declares that the other authors have no conflict of interest.

Ethics approval and consent to participate

The EMTICS study was approved by the local research ethics committees of each participating center and in accordance with the 1964 Helsinki Declaration and its later amendments. Written informed consent was obtained from all parents or legal guardians, and children and adolescents were asked to sign informed assent forms when appropriate.

Additional information

List of authors present in the EMTICS collaborative group is in acknowledgment.

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Garcia-Delgar, B., Servera, M., Coffey, B.J. 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 31, 1539–1548 (2022). https://doi.org/10.1007/s00787-021-01751-4

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  • DOI: https://doi.org/10.1007/s00787-021-01751-4

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