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Turner syndrome: review of clinical, neuropsychiatric, and EEG status: an experience of tertiary center

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Abstract

We reviewed the clinical, neuropsychiatric, and EEG status of 53 turner syndrome (TS) females, aged 3–16 years, in Assiut university hospitals, Upper Egypt. The diagnosis and care of patients with TS in Egypt is still in the developing stage. Hence this study was undertaken to review the details of patients with TS with respect to the pattern of cognitive, psychiatric, and motor dysfunction. We aimed to provide a comprehensive data about the experience of our center comparable to previous studies, which have been published in this field. This will contribute to a better definition of the neuropsychiatric features that may be specific to TS that allows early and better detection and management of these cases. We found FSIQ and verbal IQ that seem to be at a nearly normal level and a decreased performance IQ. ADHD and autistic symptoms were found in 20.70 and 3.77 % of our cohort, respectively. The motor performance in TS was disturbed, with some neurological deficits present in 17 % (reduced muscle tone and reduced muscle power). In addition, females with TS in our study exhibit social and emotional problems, including anxiety (5.66 %) and depression (11.30 %). The EEG results revealed abnormalities in seven patients (13.20 %). One patient presenting with generalized tonic–clonic seizures showed generalized epileptiform activity, and six patients presenting with intellectual disabilities showed abnormal EEG background activity.

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Abbreviations

CARS:

Childhood Autism Rating Scale

CDI:

Children depression inventory

EEG:

Electroencephalogram

FSIQ:

Full Scale Intelligence Quotient

GTC:

Generalized tonic–clonic

isoXq:

Isochromosome X

TS:

Turner syndrome

rX:

Ring chromosome

VSD:

Ventricular septal defect

PIQ:

Performance intelligence quotient

VIQ:

Verbal intelligence quotient

References

  1. Davies W (2013) Using mouse models to investigate sex-linked genetic effects on brain, behavior and vulnerability to neuropsychiatric disorders. Brain Res Bull 92:12–20

    Article  PubMed  Google Scholar 

  2. Pinsker JE (2012) Clinical review: turner syndrome: updating the paradigm of clinical care. J Clin Endocrinol Metab 97(6):E994–E1003

    Article  CAS  PubMed  Google Scholar 

  3. Knickmeyer RC (2012) Turner syndrome: advances in understanding altered cognition, brain structure and function. Curr Opin Neurol 25(2):144–149

    Article  CAS  PubMed  Google Scholar 

  4. Uematsu A, Yorifuji T, Muroi J, Kawai M, Mamada M, Kaji M et al (2002) Parental origin of normal X chromosomes in Turner syndrome patients with various karyotypes: implications for the mechanism leading to generation of a 45, X karyotype. Am J Med Genet 111(2):134–139

    Article  PubMed  Google Scholar 

  5. Hamelin CE, Anglin G, Quigley CA, Deal CL (2006) Genomic imprinting in Turner syndrome: effects on response to growth hormones and on risk of sensorineural hearing loss. J Clin Endocrinol Metab 91(8):3002–3010

    Article  CAS  PubMed  Google Scholar 

  6. Bondy C, Hougen HY, Zhou J, Cheng CM (2012) Genomic imprinting and turner syndrome. Pediatr Endocrinol Rev 9(Suppl 2):728–732

    PubMed  Google Scholar 

  7. Bondy C, Matura LA, Wooten N, Troendle J, Zinn A, Bakalov VK (2007) The physical phenotype of girls and women with Turner syndrome is not X-imprinted. Hum Genet 121:469–474

    Article  PubMed  Google Scholar 

  8. Ko JM, Kim JM, Kim GH, Lee BH, Yoo HW (2010) Influence of parental origin of the X chromosome on physical phenotypes and GH responsiveness of patients with Turner syndrome. Clin Endocrinol 73(1):66–71

    CAS  Google Scholar 

  9. Lepage JF, Hong DS, Mazaika PK, Raman M, Sheau K, Marzelli MJ et al (2013) Genomic imprinting effects of the X chromosome on brain morphology. J Neurosci 33(19):8567–8574

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Davies W, Isles AR, Burgoyne PS, Wilkinson LS (2006) X-linked imprinting: effects on brain and behaviour. BioEssays 28:35–44

    Article  CAS  PubMed  Google Scholar 

  11. Davies W, Isles AR, Smith R, Karunadasa D, Burrmann D, Humby T et al (2005) Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nat Genet 37:625–629

    Article  CAS  PubMed  Google Scholar 

  12. Wilkinson LS, Davies W, Isles AR (2007) Genomic imprinting effects on brain development and function. Nat Rev Neurosci 8:832–843

    Article  CAS  PubMed  Google Scholar 

  13. Skuse DH, James RS, Bishop DVM, Coppin B, Dalton P, Aamodt-Lepper G et al (1997) Evidence from turner’s syndrome of an imprinted X-linked locus affecting cognitive function. Nature 387:705–708

    Article  CAS  PubMed  Google Scholar 

  14. Wechsler D (2002) Wechsler preschool and primary scale of intelligence—third Edition. The Psychological Corporation, San Antonio

    Google Scholar 

  15. Wechsler D (2004) The Wechsler intelligence scale for children—fourth edition. Pearson Assessment, London

    Google Scholar 

  16. Hong D, Kent JS, Kesler S (2009) Cognitive profile of Turner syndrome. Dev Disabil Res Rev 15(4):270–278

    Article  PubMed Central  PubMed  Google Scholar 

  17. Cornoldi C, Marconi F, Vecchi T (2001) Visuospatial working memory in Turner’s syndrome. Brain Cogn 46:90–94

    Article  CAS  PubMed  Google Scholar 

  18. Kesler SR, Menon V, Reiss AL (2006) Neurofunctional differences associated with arithmetic processing in Turner syndrome. Cereb Cortex 16:849–856

    Article  PubMed Central  PubMed  Google Scholar 

  19. Simon TJ, Takarae Y, DeBoer T, McDonald-McGinn DM, Zackai EH, Ross JL (2008) Overlapping numerical cognition impairments in children with chromosome 22q11.2 deletion or Turner syndromes. Neuropsychologia 46:82–94

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Mazzocco MM, Baumgardner T, Freund LS, Reiss AL (1998) Social functioning among girls with Fragile X or Turner Syndrome and their sisters. J Autism Dev Disord 28:509–517

    Article  CAS  PubMed  Google Scholar 

  21. Bender BG, Linden MG, Robinson A (1993) Neuropsychological impairment in 42 adolescents with sex chromosome abnormalities. Am J Med Genet 48:169–173

    Article  CAS  PubMed  Google Scholar 

  22. Pennington BF, Heaton RK, Karzmark P, Pendleton MG, Lehman R, Shucard DW (1985) The neuropsychological phenotype in Turner’s syndrome. Cortex 21:391–404

    Article  CAS  PubMed  Google Scholar 

  23. Rovet J, Netley C (1982) Processing deficits in Turner’s syndrome. Dev Psychol 18:77–94

    Article  Google Scholar 

  24. Rovet JF, Szekely C, Hockenberry M (1994) Specific arithmetic calculation deficits in children with Turner’s syndrome. J Clin Exp Neuropsychol 16:820–839

    Article  CAS  PubMed  Google Scholar 

  25. Shucard DW, Shucard JL, Clopper RR, Schachter M (1992) Electrophysiological and neuropsychological indices of cognitive processing deficits in Turner’s syndrome. Dev Neuropsychol 8:299–323

    Article  Google Scholar 

  26. Ross JL, Stefanotos GA, Kushner H, Zinn A, Bondy C, Roeltgen D (2002) Persistent cognitive deficits in adult women with Turner Syndrome. Neurology 58:218–225

    Article  CAS  PubMed  Google Scholar 

  27. Christopoulos P, Deligeoroglou E, Laggari V, Christogiorgos S, Creatsas G (2008) Psychological and behavioural aspects of patients with Turner syndrome from childhood to adulthood: a review of the clinical literature. J Psychosom Obstet Gynecol 29(1):45–51

    Article  CAS  Google Scholar 

  28. Loscalzo ML, Van PL, Ho VB, Bakalov VK, Rosing DR, Malone CA et al (2005) Association between fetal lymphedema and congenital cardiovascular defects in Turner syndrome. Pediatrics 115:732–735

    Article  PubMed  Google Scholar 

  29. Good CD, Lawrence K, Thomas NS, Price CJ, Ashburner J, Friston KJ et al (2003) Dosage-sensitive X-linked locus influences the development of amygdala and orbitofrontal cortex, and fear recognition in humans. Brain 126:2431–2446

    Article  PubMed  Google Scholar 

  30. Kesler SR, Blasey CM, Brown WE, Yankowitz J, Zeng CM, Bender BG et al (2003) Effects of X-monosomy and X-linked imprinting on superior temporal gyrus morphology in Turner syndrome. Biol Psychiatry 54:636–646

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Cutter WJ, Daly EM, Robertson DMW, Chitnis XA, van Amelsvoort TA, Simmons A et al (2006) Influence of X chromosome and hormones on human brain development: a magnetic resonance imaging and proton magnetic resonance spectroscopy study of Turner syndrome. Biol Psychiatry 59:273–283

    Article  CAS  PubMed  Google Scholar 

  32. Kesler SR, Garrett A, Bender B, Yankowitz J, Zeng SM, Reiss AL et al (2004) Amygdala and hippocampal volumes in Turner syndrome: a high-resolution MRI study of X-monosomy. Neuropsychologia 42:1971–1978

    Article  PubMed Central  PubMed  Google Scholar 

  33. Molko N, Cachia A, Riviere D, Mangin JF, Bruandet M, LeBihan D et al (2004) Brain anatomy in Turner syndrome: evidence for impaired social and spatial-numerical networks. Cereb Cortex 14:840–850

    Article  CAS  PubMed  Google Scholar 

  34. Haberecht MF, Menon V, Warsofsky IS, White CD, Dyer-Friedman J, Glover GH et al (2001) Functional neuroanatomy of visuo-spatial working memory in Turner syndrome. Hum Brain Mapp 14:96–107

    Article  CAS  PubMed  Google Scholar 

  35. Salbenblatt JA, Meyers DC, Bender BG, Linden MG, Robinson A (1989) Gross and fine motor development in 45, X and 47 XXX girls. Pediatrics 84:678–682

    CAS  PubMed  Google Scholar 

  36. Haverkamp F, Keuker T, Woelfle J, Kaiser G, Zerres K, Rietz C (2003) Familial factors and hearing impairment modulate the neuromotor phenotype in Turner syndrome. Eur J Pediatr 162:30–35

    Article  PubMed  Google Scholar 

  37. der Sanden Nijhuis-van MWG, Smits-Engelsman BCM, Eling PATM (2000) Motor performance in girls with Turner’s syndrome. Dev Med Child Neurol 42:685–690

    Article  Google Scholar 

  38. Ross JL, Kushner H, Roeltgen D (1996) Developmental changes in motor function in girls with Turner syndrome. Pediatr Neurol 15:317–322

    Article  CAS  PubMed  Google Scholar 

  39. Van Borsel J, Dhooge I, Verhoye K, Derde C (1999) Communication problems in Turner syndrome: a sample survey. J Commun Dis 32:435–446

    Article  Google Scholar 

  40. Mathisen B, Reilly S, Skuse D (1992) Oral motor dysfunction and feeding disorders of infants with Turner’s syndrome. Dev Med Child Neurol 34:141–149

    Article  CAS  PubMed  Google Scholar 

  41. Clark C, Klonoff H, Hayden M (1990) Regional cerebral glucose metabolism in Turner syndrome. Can J Neurol Sci 17:140–144

    CAS  PubMed  Google Scholar 

  42. Smits-Engelsman BCM, der Sanden Nijhuis-van MWG, Duysens J (2003) An exploratory study of the kinematics of girls with Turner syndrome in a visuo-motor task. Inf Child Dev 12(3):267–277

    Article  Google Scholar 

  43. McGlone J (1985) Can spatial deficits in Turner’s syndrome be explained by focal CNS dysfunction or a typical speech lateralization? J Clin Exp Neuropsychol 7:375–394

    Article  CAS  PubMed  Google Scholar 

  44. Reiss AL, Mazzocco MM, Greenlaw R, Freund LS, Ross JL (1995) Neurodevelopmental effects of X-monosomy: a volumetric imaging study. Ann Neurol 36:731–738

    Article  Google Scholar 

  45. Brown WE, Kesler SR, Eliez S, Warsofsky IS, Haberecht M, Patwardhan A et al (2002) Brain development in Turner syndrome: a magnetic resonance imaging study. Psychiatry Res: Neuroimaging 116:187–196

    Article  PubMed Central  PubMed  Google Scholar 

  46. Tamm L, Menon V, Reiss AL (2003) Abnormal prefrontal cortex function during response inhibition in Turner syndrome: functional magnetic resonance imaging evidence. Biol Psychiatry 53:107–111

    Article  PubMed  Google Scholar 

  47. Vulliemoz S, Seeck M (2007) Bilateral temporal lobe epilepsy in a patient with Turner syndrome mosaicism. Seizure 16:261–265

    Article  CAS  PubMed  Google Scholar 

  48. Tombini M, Marciani MG, Romigi A, Izzi F, Speril F, Bozzao A et al (2003) Bilateral frontal polymicrogyria and epilepsy in a patient with Turner mosaicism: a case report. J Neurol Sci 213:83–86

    Article  CAS  PubMed  Google Scholar 

  49. Striano S, Striano P, Tortora F, Elefante A (2005) Intractable epilepsy in Turner syndrome associated with bilateral perisylvian hypoplasia: one case report. Clin Neurol Neurosurg 108:56–59

    Article  PubMed  Google Scholar 

  50. El Abd S, Patton MA, Turk J, Hoey H, Howlin P (1999) Social communicational and behavioral deficits associated with ring X turner syndrome. Am J Med Genet 88:510–516

    Article  PubMed  Google Scholar 

  51. Tsuboi T, Nielsen J (1985) Electroencephalographic examination of 64 Danish Turner girls. Acta Neurol Scand 72:590–601

    Article  CAS  PubMed  Google Scholar 

  52. Grosso S, Farnetani MA, Di Bartolo RM, Berardi R, Pucci L, Mostardini R et al (2004) Electroencephalographic and epileptiform patterns in X chromosome anomalies. J Clin Neurophysiol 21:249–253

    Article  PubMed  Google Scholar 

  53. Knickmeyer RC, Davenport M (2011) Turner syndrome and sexual differentiation of the brain: implications for understanding male-biased neurodevelopmental disorders. J Neurodev Disord 3(4):293–306

    Article  PubMed Central  PubMed  Google Scholar 

  54. Schmidt PJ, Cardoso GMP, Ross JL et al (2006) Shyness, social anxiety, and impaired self-esteem in Turner syndrome and premature ovarian failure. JAMA 295:1374–1376

    Article  CAS  PubMed  Google Scholar 

  55. Russell HF, Wallis D, Mazzocco MMM, Moshang T, Zackai E, Zinn AR et al (2006) Increased prevalence of ADHD in Turner syndrome with no evidence of imprinting effects. J Pediatr Psychol 31:945–955

    Article  PubMed  Google Scholar 

  56. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. DSM-IV, Washington, DC

    Google Scholar 

  57. Schopler E, Reichller R, Renner BR (1994) The childhood autism rating scale CARS. Western Psychological Services, Los Angeles, pp 90025–91251

    Google Scholar 

  58. Rellini E, Tortolani D, Trillo S, Carbone S, Montecchi S (2004) Childhood autism rating scale CARS, and autism behavior checklist ABC, correspondence and conflicts with DSM-IV criteria in diagnosis of autism. J Autism Dev Disord 34:703–708

    Article  CAS  PubMed  Google Scholar 

  59. Donnelly SL, Wolpert CM, Menold MM, Bass MP, Gilbert JR, Cuccaro ML et al (2000) Female with autistic disorder and monosomy X (Turner syndrome): parent-of-origin effect of the X chromosome. Am J Med Genet 96:312–316

    Article  CAS  PubMed  Google Scholar 

  60. Telvi L, Lebbar A, Del Pino O, Barbet JP, Chaussain JL (1999) 45, X/46, XY mosaicism: report of 27 cases. Pediatrics 104:304–308

    Article  CAS  PubMed  Google Scholar 

  61. Creswell C, Skuse D (1999) Autism in association with Turner syndrome: implications for male vulnerability to pervasive developmental disorders. Neurocase 5:511–518

    Article  Google Scholar 

  62. McCauley E, Feuillan P, Kushner H, Ross JL (2001) Psychosocial development in adolescents with Turner syndrome. J Dev Behav Pediatr 22(6):360–365

    Article  CAS  PubMed  Google Scholar 

  63. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders (4th ed). Washington, DC

  64. Cohen P, Cohen J, Kasen S, Velez C, Hartmark C, Johnson J et al (1993) An epidemiological study of disorders in late childhood and adolescence I. Age- and gender-specific prevalence. J Child Psychol Psychiatry 34:851–867

    Article  CAS  PubMed  Google Scholar 

  65. Robinson L, Sclar D, Skaer T, Galin R (1999) National trends in the prevalence of attention deficit hyperactivity disorder and the prescribing of methylphenidate among school-age children. Clin Pediat 38:209–217

    Article  Google Scholar 

  66. Kirk J, Mazzocco MMM, Kover ST (2005) Assessing executive dysfunction in girls with fragile X or Turner syndrome using the contingency naming test. Dev Neuropsychol 28:755–777

    Article  PubMed  Google Scholar 

  67. Kovacs M, Beck A (1977) An empirical-clinical approach toward a definition of childhood depression. In: Schulterbrandt J, Raskin A (eds) Depression in childhood: diagnosis. Treatment and conceptual models. Department of Health, Education and Welfare, Washington, DC, pp 1–26

    Google Scholar 

  68. Castaneda A, McCandless BR, Palermo DS (1956) The children’s form of the manifest anxiety scale. Child Dev 27:317–326

    Article  Google Scholar 

  69. Van Pareren YK, Duivenvoorden HJ, Slijper FM, Koot HM, Drop SL, de Muinck Keizer-Schrama SM (2005) Psychosocial functioning after discontinuation of long-term growth hormone treatment in girls with Turner syndrome. Horm Res 63(5):238–244

    Article  PubMed  Google Scholar 

  70. Kilic BG, Ergur AT, Ocal G (2005) Depression, levels of anxiety and self-concept in girls with Turner’s syndrome. J Pediatr Endocrinol Metab 18(11):1111–1117

    PubMed  Google Scholar 

  71. Downey J, Ehrhardt AA, Gruen R, Bell JJ, Morishima A (1989) Psychopathology and social functioning in women with Turner syndrome. J Nerv Ment Dis 177(4):191–201

    Article  CAS  PubMed  Google Scholar 

  72. McCauley E, Kay T, Ito J, Treder R (1987) The Turner syndrome: cognitive deficits, affective discrimination, and behavior problems. Child Dev 58(2):464–473

    Article  CAS  PubMed  Google Scholar 

  73. Ross JL, Roeltgen D, Feuillan P, Kushner H, Cutler G Jr (2000) Use of estrogen in young girls with Turner syndrome: effects on memory. Neurology 54(1):164–170

    Article  CAS  PubMed  Google Scholar 

  74. Lagrou K, Froidecoeur C, Verlinde F, Craen M, De Schepper J, François I et al (2006) Psychosocial functioning, self-perception and body image and their auxologic correlates in growth hormone and oestrogen-treated young adult women with Turner syndrome. Horm Res 66(6):277–284

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pediatrics, Faculty of Medicine, Assiut University, Assiut, 71516, Egypt

    Khaled Saad & Yasser F. Abdel-Raheem

  2. Department of Neurology and Psychiatry, Assiut University, Assiut, 71516, Egypt

    Ahmed A. Abdelrahman & Reda Badry

  3. Department of Obstetrics and Gynecology, Assiut University, Assiut, 71516, Egypt

    Essam R. Othman

  4. Department of Clinical Pathology, Cytogenetic Unit, Assiut University, Assiut, 71516, Egypt

    Hisham A. K. Othman

  5. Department of Public Health, Assiut University, Assiut, 71516, Egypt

    Karema M. Sobhy

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  1. Khaled Saad
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  2. Ahmed A. Abdelrahman
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  3. Yasser F. Abdel-Raheem
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  4. Essam R. Othman
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Correspondence to Khaled Saad.

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Saad, K., Abdelrahman, A.A., Abdel-Raheem, Y.F. et al. Turner syndrome: review of clinical, neuropsychiatric, and EEG status: an experience of tertiary center. Acta Neurol Belg 114, 1–9 (2014). https://doi.org/10.1007/s13760-013-0264-9

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