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Journal of Neural Transmission

, Volume 125, Issue 7, pp 1077–1085 | Cite as

A study of sensory dysregulation in children with tic disorders

  • Hana Weisman
  • Shula Parush
  • Alan Apter
  • Silvana Fennig
  • Noa Benaroya-Milshtein
  • Tamar Steinberg
Psychiatry and Preclinical Psychiatric Studies - Original Article

Abstract

Disrupted somatosensory processing characterized by over- or under- responsiveness to environmental stimuli plays an important, yet often overlooked, role in typical development and is aberrant in various neurodevelopmental disorders. These dysfunctional somatosensory processes have been conceptualized as an entity termed somatosensory dysregulation (SMD). Since Tourette syndrome (TS) is a prototypical example of developmental psychopathological disorder, we hypothesised that SMD would be a feature found in children suffering from the disorder. Ninety-two subjects representing consecutive admissions to a tertiary paediatric Tourette syndrome clinic were admitted to the study. Comorbid conditions included ADHD, depression, anxiety disorder, and OCD. For purposes of the study, patients completed a battery of self-, caregiver-, and clinician-rated psychological instruments measuring TS core symptoms and comorbidities and quality of life. Sensory modulation was measured by self-report and by objective measures such as stimulation with Von Frey filaments. Almost 50% of the cohort had no SMD. Of the remainder, 14 (15%) had suspected SMD and 32 (34.8%) had SMD. SMD was significantly more common and severe when there were comorbidities. The presence of SMD was associated with more severe impairments in quality of life and less participation in daily activities. The SMD, as measured by subjective measures but not by objective, is probably more associated with central processing rather than peripheral perception.

Keywords

Tic disorders Tourette syndrome Sensory motor dysfunction Children Sensory processing 

Abbreviations

ADHD

Attention deficit disorder

CDI

Children’s depression inventory

CY-BOCS

Children yale brown obsessive compulsive scale

FPT

Fabric prickliness test

PICO-Q

Participation in childhood occupations questionnaire

OCD

Obsessive–compulsive disorder

QoL

Quality of life (questionnaire)

SCARED

Screen for child anxiety related emotional disorders

SMD

Sensory modulation dysfunction

SOR

Sensory over-reactivity

SSP

Short sensory profile

TS

Tourette syndrome

YGTSS

Yale global tic severity scale

Notes

Funding

No funding was received for this work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahn RR, Miller LJ, Milberger S, McIntosh DN (2004) Prevalence of parents’ perceptions of sensory processing disorders among kindergarten children. Am J Occup Ther 58(3):287–293CrossRefPubMedGoogle Scholar
  2. Arendt-Nielsen L, Yarnitsky D (2009) Experimental and clinical applications of quantitative sensory testing applied to skin, muscles and viscera. J Pain 10(6):556–572.  https://doi.org/10.1016/j.jpain.2009.02.002 CrossRefPubMedGoogle Scholar
  3. Ayres AJ (1972) Sensory integration and learning disorders. Western Psychological Services, Los AngelesGoogle Scholar
  4. Baranek GT, Roberts JE, David FJ, Sideris J, Mirrett PL, Hatton DD, Bailey DB Jr (2008) Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome. Phys Occup Ther Pediatr 28(1):79–98CrossRefPubMedGoogle Scholar
  5. Bar-Shalita T, Goldstand S, Hahn-Markowitz J, Parush S (2005) Typical children’s responsivity patterns of the tactile and vestibular systems. Am J Occup Ther 59(2):148–156CrossRefPubMedGoogle Scholar
  6. Bar-Shalita T, Vatine JJ, Seltzer Z, Parush S (2009a) Psychophysical correlates in children with sensory modulation disorder (SMD). Physiol Behav 98(5):631–639.  https://doi.org/10.1016/j.physbeh.2009.09.020 CrossRefPubMedGoogle Scholar
  7. Bar-Shalita T, Yochman A, Shapiro-Rihtman T, Vatine JJ, Parush S (2009b) The participation in childhood occupations questionnaire (PICO-Q): a pilot study. Phys Occup Ther Pediatr 29(3):295–310.  https://doi.org/10.1080/01942630903028440 CrossRefPubMedGoogle Scholar
  8. Baumgartner U, Magerl W, Klein T, Hopf HC, Treede RD (2002) Neurogenic hyperalgesia versus painful hypoalgesia: two distinct mechanisms of neuropathic pain. Pain 96(1–2):141–151CrossRefPubMedGoogle Scholar
  9. Belluscio BA, Jin L, Watters V, Lee TH, Hallett M (2011) Sensory sensitivity to external stimuli in Tourette syndrome patients. Mov Disord 26(14):2538–2543.  https://doi.org/10.1002/mds.23977 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Ben-Sasson A, Carter AS, Briggs-Gowan MJ (2009) Sensory over-responsivity in elementary school: prevalence and social-emotional correlates. J Abnorm Child Psychol 37(5):705–716.  https://doi.org/10.1007/s10802-008-9295-8 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Birmaher B, Khetarpal S, Brent D, Cully M, Balach L, Kaufman J, Neer SM (1997) The screen for child anxiety related emotional disorders (SCARED): scale construction and psychometric characteristics. J Am Acad Child Adolesc Psychiatry 36(4):545–553.  https://doi.org/10.1097/00004583-199704000-00018 CrossRefPubMedGoogle Scholar
  12. Birmaher B, Brent DA, Chiappetta L, Bridge J, Monga S, Baugher M (1999) Psychometric properties of the Screen for child anxiety related emotional disorders (SCARED): a replication study. J Am Acad Child Adolesc Psychiatry 38(10):1230–1236.  https://doi.org/10.1097/00004583-199910000-00011 CrossRefPubMedGoogle Scholar
  13. Carter AS, Ben-Sasson A, Briggs-Gowan MJ (2011) Sensory over-responsivity, psychopathology, and family impairment in school-aged children. J Am Acad Child Adolesc Psychiatry 50(12):1210–1219.  https://doi.org/10.1016/j.jaac.2011.09.010 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cervero F, Meyer RA, Campbell JN (1994) A psychophysical study of secondary hyperalgesia: evidence for increased pain to input from nociceptors. Pain 58(1):21–28CrossRefPubMedGoogle Scholar
  15. Cohn E, Miller LJ, Tickle-Degnen L (2000) Parental hopes for therapy outcomes: children with sensory modulation disorders. Am J Occup Ther 54(1):36–43CrossRefPubMedGoogle Scholar
  16. Conners CK (1997) Conners rating scales–revised: technical manual. Multi Health Systems North Tonawanda, New YorkGoogle Scholar
  17. Ganos Christos, Garrido Alicia, Navalpotro-Gómez Irene, Ricciardi Lucia, Martino Davide, Edwards Mark J, Tsakiris Manos, Haggard Patrick, Bhatia Kailash P (2015) Premonitory urge to tic in Tourette’s is associated with interoceptive awareness. Mov Disord 30(9):1198–1202CrossRefPubMedGoogle Scholar
  18. Garnsworthy RK, Gully RL, Kenins P, Mayfield RJ, Westerman RA (1988) Identification of the physical stimulus and the neural basis of fabric-evoked prickle. J Neurophysiol 59(4):1083–1097CrossRefPubMedGoogle Scholar
  19. Gouze KR, Hopkins J, LeBailly SA, Lavigne JV (2009) Re-examining the epidemiology of sensory regulation dysfunction and comorbid psychopathology. J Abnorm Child Psychol 37(8):1077–1087.  https://doi.org/10.1007/s10802-009-9333-1 CrossRefPubMedGoogle Scholar
  20. Hansson P, Backonja M, Bouhassira D (2007) Usefulness and limitations of quantitative sensory testing: clinical and research application in neuropathic pain states. Pain 129(3):256–259.  https://doi.org/10.1016/j.pain.2007.03.030 CrossRefPubMedGoogle Scholar
  21. Hicks CL, von Baeyer CL, Spafford PA, van Korlaar I, Goodenough B (2001) The faces pain scale-revised: toward a common metric in pediatric pain measurement. Pain 93(2):173–183CrossRefPubMedGoogle Scholar
  22. Houghton DC, Capriotti MR, Conelea CA, Woods DW (2014) Sensory phenomena in Tourette syndrome: their role in symptom formation and treatment. Curr Dev Disord Rep 1(4):245–251.  https://doi.org/10.1007/s40474-014-0026-2 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kong M, Pritchard M, Dean L, Talley M, Torbert R, Maha J (2017) A community-based sensory training program leads to improved experience at a local zoo for children with sensory challenges. Front Pediatr 5:193.  https://doi.org/10.3389/fped.2017.00193 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kovacs M (1981) Rating scales to assess depression in school-aged children. Acta Paedopsychiatr 46(5–6):305–315PubMedGoogle Scholar
  25. Kovacs M, Beck AT (1977) An empirical clinical approach towards a definition of childhood depression. In: Schultebrant JG, Raskin A (eds) Depression in children. Raven Press, New York, pp l–l25Google Scholar
  26. Kreitler S, Kreitler M (2006) Multidimensional quality of life: a new measure of quality of life in adults. Soc Indic Res 76(1):5–33CrossRefGoogle Scholar
  27. Landgren M, Pettersson R, Kjellman B, Gillberg C (1996) ADHD, DAMP and other neurodevelopmental/psychiatric disorders in 6-year-old children: epidemiology and co-morbidity. Dev Med Child Neurol 38(10):891–906CrossRefPubMedGoogle Scholar
  28. Leckman JF, Cohen DJ (1998) Tourette’s syndrome: tics, obsessions, compulsions—developmental psychopathology and clinical care. Wiley, New YorkGoogle Scholar
  29. Leckman JF, Riddle MA, Hardin MT, Ort SI, Swartz KL, Stevenson J, Cohen DJ (1989) The yale global tic severity scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry 28(4):566–573.  https://doi.org/10.1097/00004583-198907000-00015 CrossRefPubMedGoogle Scholar
  30. Leckman JF, Walker DE, Cohen DJ (1993) Premonitory urges in Tourette’s syndrome. Am J Psychiatry 150(1):98–102.  https://doi.org/10.1176/ajp.150.1.98 CrossRefPubMedGoogle Scholar
  31. Leckman JF, Walker DE, Goodman WK, Pauls DL, Cohen DJ (1994) “Just right” perceptions associated with compulsive behavior in Tourette’s syndrome. Am J Psychiatry 151(5):675–680.  https://doi.org/10.1176/ajp.151.5.675 CrossRefPubMedGoogle Scholar
  32. Leckman JF, Pauls DL, Zhang H, Rosario-Campos MC, Katsovich L, Kidd KK, Pakstis AJ, Alsobrook JP, Robertson MM, McMahon WM, Walkup JT, van de Wetering BJ, King RA, Cohen DJ (2003) Obsessive-compulsive symptom dimensions in affected sibling pairs diagnosed with Gilles de la Tourette syndrome. Am J Med Genet B Neuropsychiatr Genet 116B(1):60–68.  https://doi.org/10.1002/ajmg.b.10001 CrossRefPubMedGoogle Scholar
  33. Mangeot SD, Miller LJ, McIntosh DN, McGrath-Clarke J, Simon J, Hagerman RJ, Goldson E (2001) Sensory modulation dysfunction in children with attention-deficit-hyperactivity disorder. Dev Med Child Neurol 43(6):399–406CrossRefPubMedGoogle Scholar
  34. McIntosh DN, Miller LJ, Shyu V (1999a) Development and validation of the short sensory profile. In: Dunn W (ed) Sensory profile user’s manual. Psychological Corporation, San Antonio, pp 59–73Google Scholar
  35. McIntosh DN, Miller LJ, Shyu V, Hagerman RJ (1999b) Sensory-modulation disruption, electrodermal responses, and functional behaviors. Dev Med Child Neurol 41(9):608–615CrossRefPubMedGoogle Scholar
  36. Miller LJ, Lane SJ (2000) Toward a consensus in terminology in sensory integration theory and practice: part 1: sensory integration patterns of function and dysfunction. Sens Integr Spec Interest Sect Q 23(1):1–4Google Scholar
  37. Miller LJ, Reisman JE, McIntosh DN, Simon J (2001) An ecological model of sensory modulation: performance of children with fragile X syndrome, autistic disorder, attention-deficit/hyperactivity disorder, and sensory modulation dysfunction. Understanding the nature of sensory inte- gration with diverse populations. Therapy Skill Builders, San Antonio, pp 57–85Google Scholar
  38. Miller LJ, Nielsen DM, Schoen SA (2012) Attention deficit hyperactivity disorder and sensory modulation disorder: a comparison of behavior and physiology. Res Dev Disabil 33(3):804–818.  https://doi.org/10.1016/j.ridd.2011.12.005 CrossRefPubMedGoogle Scholar
  39. Neil L, Green D, Pellicano E (2017) The psychometric properties of a new measure of sensory behaviors in autistic children. J Autism Dev Disord 47(4):1261–1268.  https://doi.org/10.1007/s10803-016-3018-8 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Parush S, Sohmer H, Steinberg A, Kaitz M (2007) Somatosensory function in boys with ADHD and tactile defensiveness. Physiol Behav 90(4):553–558.  https://doi.org/10.1016/j.physbeh.2006.11.004 CrossRefPubMedGoogle Scholar
  41. Patel N, Jankovic J, Hallett M (2014) Sensory aspects of movement disorders. Lancet Neurol 13(1):100–112.  https://doi.org/10.1016/S1474-4422(13)70213-8 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Puts NA, Harris AD, Crocetti D, Nettles C, Singer HS, Tommerdahl M, Edden RA, Mostofsky SH (2015) Reduced GABAergic inhibition and abnormal sensory symptoms in children with Tourette syndrome. J Neurophysiol 114(2):808–817.  https://doi.org/10.1152/jn.00060.2015jn.00060.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ruhrman D, Gev E, Benaroya-Milshtein N, Fennig S, Krispin O, Apter A, Steinberg T (2016) Non-motor aspects of tic disorders-new developments. Front Psychiatry 7:213.  https://doi.org/10.3389/fpsyt.2016.00213 PubMedGoogle Scholar
  44. Scahill L, Riddle MA, McSwiggin-Hardin M, Ort SI, King RA, Goodman WK, Cicchetti D, Leckman JF (1997) Children’s yale-brown obsessive compulsive scale: reliability and validity. J Am Acad Child Adolesc Psychiatry 36(6):844–852.  https://doi.org/10.1097/00004583-199706000-00023 CrossRefPubMedGoogle Scholar
  45. Schunke O, Grashorn W, Kahl U, Schottle D, Haggard P, Munchau A, Bingel U, Ganos C (2016) Quantitative sensory testing in adults with tourette syndrome. Parkinsonism Relat Disord 24:132–136.  https://doi.org/10.1016/j.parkreldis.2016.01.006 CrossRefPubMedGoogle Scholar
  46. Steinberg T, Shmuel Baruch S, Harush A, Dar R, Woods D, Piacentini J, Apter A (2010) Tic disorders and the premonitory urge. J Neural Transm (Vienna) 117(2):277–284.  https://doi.org/10.1007/s00702-009-0353-3 CrossRefGoogle Scholar
  47. Stewart SE, Ceranoglu TA, O’Hanley T, Geller DA (2005) Performance of clinician versus self-report measures to identify obsessive-compulsive disorder in children and adolescents. J Child Adolesc Psychopharmacol 15(6):956–963.  https://doi.org/10.1089/cap.2005.15.956 CrossRefPubMedGoogle Scholar
  48. Thibault A, Forget R, Lambert J (1994) Evaluation of cutaneous and proprioceptive sensation in children: a reliability study. Dev Med Child Neurol 36(9):796–812CrossRefPubMedGoogle Scholar
  49. Tomchek SD, Dunn W (2007) Sensory processing in children with and without autism: a comparative study using the short sensory profile. Am J Occup Ther 61(2):190–200CrossRefPubMedGoogle Scholar
  50. Verdugo R, Ochoa JL (1992) Quantitative somatosensory thermotest. A key method for functional evaluation of small calibre afferent channels. Brain 115(Pt3):893–913CrossRefPubMedGoogle Scholar
  51. Woods DW, Piacentini J, Himle MB, Chang S (2005) Premonitory urge for tics scale (PUTS): initial psychometric results and examination of the premonitory urge phenomenon in youths with Tic disorders. J Dev Behav Pediatr 26(6):397–403.  https://doi.org/10.1097/00004703-200512000-00001 CrossRefPubMedGoogle Scholar
  52. Yochman A, Alon-Beery O, Sribman A, Parush S (2013) Differential diagnosis of sensory modulation disorder (SMD) and attention deficit hyperactivity disorder (ADHD): participation, sensation, and attention. Front Hum Neurosci 7:862.  https://doi.org/10.3389/fnhum.2013.00862 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Hana Weisman
    • 1
    • 2
    • 3
    • 4
  • Shula Parush
    • 3
  • Alan Apter
    • 1
  • Silvana Fennig
    • 1
  • Noa Benaroya-Milshtein
    • 1
  • Tamar Steinberg
    • 1
  1. 1.The Matta and Harry Freund Neuropsychiatric Tourette ClinicSchneider Children’s Medical Center of IsraelPetach TikvaIsrael
  2. 2.Affiliated to Sackler Faculty of Medicine, Tel Aviv UniversityTel AvivIsrael
  3. 3.School of Occupational TherapyFaculty of Medicine of Hadassah and the Hebrew University of JerusalemJerusalemIsrael
  4. 4.The Medical Psychology ClinicSheba Medical CenterTel HashomerIsrael

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