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European Journal of Pediatrics

, Volume 178, Issue 7, pp 995–1003 | Cite as

Developmental and behavioral problems in preschool-aged primary ciliary dyskinesia patients

  • P. Zengin AkkusEmail author
  • M. Gharibzadeh Hizal
  • E. Ilter Bahadur
  • E.N. Ozmert
  • S. Eryilmaz Polat
  • G. Ozdemir
  • S. Karahan
  • E. Yalcin
  • D. Dogru Ersoz
  • N. Kiper
  • U. Ozcelik
Original Article

Abstract

Primary ciliary dyskinesia (PCD) causes a broad spectrum of disease. This study aims to explore the developmental, behavioral, and social-emotional aspects of preschool-aged children with PCD. Fourteen PCD, 17 cystic fibrosis (CF) patients and 15 healthy subjects were enrolled. Developmental features of the participants were evaluated with Ages and Stages Questionnaire. Parents of participants filled out the Child Behavior Checklist (CBCL). The number of children screened positive for developmental delay was statistically higher in the PCD group. Higher numbers of children with PCD were screened positive for developmental delay in communication and problem-solving domains. Delay in fine motor skill domain was more common in children with PCD and CF compared to healthy subjects. There was no difference among the three groups in terms of gross motor and personal-social development. None of the children in all three groups was shown to have social-emotional problems. In CBCL, patients with CF had higher internalizing problem scores. Externalizing and total problem scores did not differ between the three groups. However, among PCD patients, children with developmental delay on more than one domain had higher externalizing and total problem scores.

Conclusion: The current study revealed that positive screening for developmental delay is more common in preschool-aged PCD patients compared to patients with CF and healthy children.

What is Known:

Intelligence scores of school-aged PCD patients are similar to healthy subjects despite their higher internalizing problem scores on Child Behavior Checklist (CBCL).

School-aged PCD patients exhibit higher hyperactivity and inattention findings.

What is New:

Positive screening for developmental delay in communication, problem-solving and fine motor skills is more common in preschool-aged PCD patients.

Preschool-aged PCD patients screened positive for developmental delay in more than one domain have higher externalizing and total problem scores on CBCL.

Keywords

Primary ciliary dyskinesia Developmental delay Behavioral problems Social-emotional problems 

Abbreviations

AAP

American Academy of Pediatrics

ASQ

Ages and Stages Questionnaire

ASQ:SE

Ages and Stages Questionnaire:social-emotional

ASQ-TR

Ages and Stages Questionnaire for Turkish children

CBCL

Child Behavior Checklist

CF

Cystic fibrosis

PSQ

Pediatric Sleep Questionnaire

PCD

Primary ciliary dyskinesia

SES

Socio-economic status

ASQ:SE-TR

Turkish version of the Ages and Stages Questionnaire:social-emotional

Notes

Authors’ contributions

Zengin Akkus P and Gharibzadeh Hizal M conceptualized and designed the study. They were responsible for all the assessments of patients. They drafted the initial manuscript, revised the manuscript, and approved the final manuscript.

Ilter Bahadur E, Esref S, and Ozdemir G were responsible for collecting data, they revised the manuscript and approved the final manuscript.

Karahan S carried out the statistical analyses, interpreted the statistical data, reviewed the manuscript, and approved the final manuscript.

Yalcin E, Dogru Ersoz D, and Kiper N interpreted the data, reviewed the manuscript, and approved the final manuscript.

Ozmert EN and Ozcelik U conceptualized and designed the study, supervised all the assessments of patients. They interpreted the statistical data, reviewed the manuscript, and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from parents of all participants included in the study.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The Ethics Committee of the Hacettepe University Faculty of Medicine approved the study design. This article does not contain any studies with animals performed by any of the authors.

References

  1. 1.
    Achenbach TM (1992) Manual for the child behavior checklist/2–3 and 1992 profile: profile for boys and girls. Auswertungsbögen. Department of Psychiatry, University of VermontGoogle Scholar
  2. 2.
    Achenbach TM, Rescorla LA (2000) Manual for the ASEBA preschool forms and profiles, vol 30. University of Vermont, Research center for children, youth, & families, BurlingtonGoogle Scholar
  3. 3.
    Afzelius BA (1976) A human syndrome caused by immotile cilia. Science (New York, NY) 193(4250):317–319CrossRefGoogle Scholar
  4. 4.
    Afzelius BA, Stenram U (2006) Prevalence and genetics of immotile-cilia syndrome and left-handedness. Int J Dev Biol 50(6):571–573.  https://doi.org/10.1387/ijdb.052132ba Google Scholar
  5. 5.
    Baker BL, McIntyre LL, Blacher J, Crnic K, Edelbrock C, Low C (2003) Pre-school children with and without developmental delay: behaviour problems and parenting stress over time. J Intellect Disabil Res 47(Pt 4-5):217–230CrossRefGoogle Scholar
  6. 6.
    Barbato A, Frischer T, Kuehni CE, Snijders D, Azevedo I, Baktai G, Bartoloni L, Eber E, Escribano A, Haarman E, Hesselmar B, Hogg C, Jorissen M, Lucas J, Nielsen KG, O'Callaghan C, Omran H, Pohunek P, Strippoli MP, Bush A (2009) Primary ciliary dyskinesia: a consensus statement on diagnostic and treatment approaches in children. Eur Respir J 34(6):1264–1276.  https://doi.org/10.1183/09031936.00176608 CrossRefGoogle Scholar
  7. 7.
    Behan L (2016) Primary ciliary dyskinesia: a biopsychosocial approach. PhD Thesis, University College CorkGoogle Scholar
  8. 8.
    Behan L, Rubbo B, Lucas JS, Dunn Galvin A (2017) The patient's experience of primary ciliary dyskinesia: a systematic review. Qual Life Res Int J Qual Life Asp Treat Care Rehab 26(9):2265–2285.  https://doi.org/10.1007/s11136-017-1564-y Google Scholar
  9. 9.
    Bell MF, Bayliss DM, Glauert R, Harrison A, Ohan JL (2016) Chronic illness and developmental vulnerability at school entry. Pediatrics 137(5):e20152475.  https://doi.org/10.1542/peds.2015-2475 CrossRefGoogle Scholar
  10. 10.
    Carotenuto M, Esposito M, Di Pasquale F, De Stefano S, Santamaria F (2013) Psychological, cognitive and maternal stress assessment in children with primary ciliary dyskinesia. World J Pediatr 9(4):312–317.  https://doi.org/10.1007/s12519-013-0441-1 CrossRefGoogle Scholar
  11. 11.
    Chervin RD, Hedger K, Dillon JE, Pituch KJ (2000) Pediatric sleep questionnaire (PSQ): validity and reliability of scales for sleep-disordered breathing, snoring, sleepiness, and behavioral problems. Sleep Med 1(1):21–32CrossRefGoogle Scholar
  12. 12.
    de Almeida Thomazinho P, de Miranda Chaves CR, Passaro CP, Meio MD (2011) Motor delay in cystic fibrosis infants: an observational study. Early Hum Dev 87(12):769–773.  https://doi.org/10.1016/j.earlhumdev.2011.05.012 CrossRefGoogle Scholar
  13. 13.
    De Brauwer PJ, Blaise P, Hermans G, Boniver V, Bartsch P, Rakic JM (2010) Retinitis pigmentosa and bronchiectasis: a case report on a rare association suggestive of a common underlying primary ciliary dyskinesia (PCD). Bull Soc Belge Ophtalmol (314):9–14Google Scholar
  14. 14.
    Dekker MC, Koot HM, van der Ende J, Verhulst FC (2002) Emotional and behavioral problems in children and adolescents with and without intellectual disability. J Child Psychol Psychiatry Allied Discip 43(8):1087–1098CrossRefGoogle Scholar
  15. 15.
    Erol N, Simsek Z, Oner O, Munir K (2005) Behavioral and emotional problems among Turkish children at ages 2 to 3 years. J Am Acad Child Adolesc Psychiatry 44(1):80–87CrossRefGoogle Scholar
  16. 16.
    Ferkol TW, Leigh MW (2012) Ciliopathies: the central role of cilia in a spectrum of pediatric disorders. J Pediatr 160(3):366–371.  https://doi.org/10.1016/j.jpeds.2011.11.024 CrossRefGoogle Scholar
  17. 17.
    Gozal D, Kheirandish-Gozal L, Bhattacharjee R, Spruyt K (2010) Neurocognitive and endothelial dysfunction in children with obstructive sleep apnea. Pediatrics 126(5):e1161–e1167.  https://doi.org/10.1542/peds.2010-0688 CrossRefGoogle Scholar
  18. 18.
    Gruber W, Orenstein DM, Paul K, Huls G, Braumann KM (2010) Motor performance is better than normal in preschool children with cystic fibrosis. Pediatr Pulmonol 45(6):527–535.  https://doi.org/10.1002/ppul.21098 Google Scholar
  19. 19.
    Hildebrandt F, Benzing T, Katsanis N (2011) Ciliopathies. N Engl J Med 364(16):1533–1543.  https://doi.org/10.1056/NEJMra1010172 CrossRefGoogle Scholar
  20. 20.
    Hollingshead AB (1975) Four factor index for social status. Yale University Press, New HavenGoogle Scholar
  21. 21.
    Horani A, Ferkol TW (2016) Primary ciliary dyskinesia and associated sensory ciliopathies. Expert Rev Respir Med 10(5):569–576.  https://doi.org/10.1586/17476348.2016.1165612 CrossRefGoogle Scholar
  22. 22.
    Kapci EG, Kucuker S, Uslu RI (2010) How applicable are ages and stages questionnaires for use with Turkish children? Top Early Child Spec Educ 30(3):176–188.  https://doi.org/10.1177/0271121410373149 CrossRefGoogle Scholar
  23. 23.
    Knowles MR, Daniels LA, Davis SD, Zariwala MA, Leigh MW (2013) Primary ciliary dyskinesia. Recent advances in diagnostics, genetics, and characterization of clinical disease. Am J Respir Crit Care Med 188(8):913–922.  https://doi.org/10.1164/rccm.201301-0059CI CrossRefGoogle Scholar
  24. 24.
    Kucuker S, Kapci EG, Uslu RI (2011) Evaluation of the Turkish version of the “ages and stages questionnaires: social-emotional” in identifying children with social-emotional problems. Infants Young Child 24(2):207–220CrossRefGoogle Scholar
  25. 25.
    Media and Young Minds (2016) Pediatrics 138(5):e20162591.  https://doi.org/10.1542/peds.2016-2591 CrossRefGoogle Scholar
  26. 26.
    Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N (1998) Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95(6):829–837CrossRefGoogle Scholar
  27. 27.
    Pazour GJ, Dickert BL, Vucica Y, Seeley ES, Rosenbaum JL, Witman GB, Cole DG (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151(3):709–718CrossRefGoogle Scholar
  28. 28.
    Prulière-Escabasse V, Coste A, Chauvin P, Fauroux B, Tamalet A, Garabedian E-N, Escudier E, Roger G (2010) Otologic features in children with primary ciliary dyskinesia. Arch Otolaryngol Head Neck Surg 136(11):1121–1126CrossRefGoogle Scholar
  29. 29.
    Sagel SD, Davis SD, Campisi P, Dell SD (2011) Update of respiratory tract disease in children with primary ciliary dyskinesia. Proc Am Thorac Soc 8(5):438–443CrossRefGoogle Scholar
  30. 30.
    Sismanlar Eyuboglu T, Aslan AT, Ceylan A, Soysal AS, Budakoglu II, Ulukavak Ciftci T, Kokturk O (2018) Neurocognitive disorders and sleep in children with primary ciliary dyskinesia. Pediatr Pulmonol 53(10):1436–1441.  https://doi.org/10.1002/ppul.24133 CrossRefGoogle Scholar
  31. 31.
    Small JW, Hix-Small H, Vargas-Baron E, Marks KP (2018) Comparative use of the ages and stages questionnaires in low- and middle-income countries. Dev Med Child Neurol 61:431–443.  https://doi.org/10.1111/dmcn.13938 CrossRefGoogle Scholar
  32. 32.
    Sommer JU, Schäfer K, Omran H, Olbrich H, Wallmeier J, Blum A, Hörmann K, Stuck BA (2011) ENT manifestations in patients with primary ciliary dyskinesia: prevalence and significance of otorhinolaryngologic co-morbidities. Eur Arch Otorhinolaryngol 268(3):383–388CrossRefGoogle Scholar
  33. 33.
    Squires JPL, Bricker D (1999) The ASQ user’s guide for the ages & stages questionnaires: a parent-completed, child-monitoring system, 2nd edn. Paul H. Brookes Publishing Co, BaltimoreGoogle Scholar
  34. 34.
    Squires J, Bricker D, Twombly E (2003) The ASQ: SE user’s guide. Paul H. Brooks Publishing Co, BaltimoreGoogle Scholar
  35. 35.
    Tarkar A, Loges NT, Slagle CE, Francis R, Dougherty GW, Tamayo JV, Shook B, Cantino M, Schwartz D, Jahnke C, Olbrich H, Werner C, Raidt J, Pennekamp P, Abouhamed M, Hjeij R, Köhler G, Griese M, Li Y, Lemke K, Klena N, Liu X, Gabriel G, Tobita K, Jaspers M, Morgan LC, Shapiro AJ, Letteboer SJ, Mans DA, Carson JL, Leigh MW, Wolf WE, Chen S, Lucas JS, Onoufriadis A, Plagnol V, Schmidts M, Boldt K, Roepman R, Zariwala MA, Lo CW, Mitchison HM, Knowles MR, Burdine RD, Loturco JJ, Omran H (2013) DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nat Genet 45(9):995–1003.  https://doi.org/10.1038/ng.2707 CrossRefGoogle Scholar
  36. 36.
    Thompson RJ Jr, Gustafson KE, Hamlett KW, Spock A (1992) Psychological adjustment of children with cystic fibrosis: the role of child cognitive processes and maternal adjustment. J Pediatr Psychol 17(6):741–755CrossRefGoogle Scholar
  37. 37.
    Tierney AL, Nelson CA 3rd (2009) Brain development and the role of experience in the early years. Zero Three 30(2):9–13Google Scholar
  38. 38.
    Ward C, Massie J, Glazner J, Sheehan J, Canterford L, Armstrong D, Jaffe A, Hiscock H (2009) Problem behaviours and parenting in preschool children with cystic fibrosis. Arch Dis Child 94(5):341–347.  https://doi.org/10.1136/adc.2008.150789 CrossRefGoogle Scholar
  39. 39.
    Wessels MW, den Hollander NS, Willems PJ (2003) Mild fetal cerebral ventriculomegaly as a prenatal sonographic marker for Kartagener syndrome. Prenat Diagn 23(3):239–242.  https://doi.org/10.1002/pd.551 CrossRefGoogle Scholar
  40. 40.
    Yuksel H, Sogut A, Yilmaz O, Kutluay E (2011) Reliability and validity of the Turkish version of the pediatric sleep questionnaire: a tool for prediction of sleep related breathing disorder. Tuberk Toraks 59(3):236–241CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • P. Zengin Akkus
    • 1
    Email author
  • M. Gharibzadeh Hizal
    • 2
  • E. Ilter Bahadur
    • 1
  • E.N. Ozmert
    • 1
  • S. Eryilmaz Polat
    • 2
  • G. Ozdemir
    • 1
  • S. Karahan
    • 3
  • E. Yalcin
    • 2
  • D. Dogru Ersoz
    • 2
  • N. Kiper
    • 2
  • U. Ozcelik
    • 2
  1. 1.Faculty of Medicine, Department of Pediatrics, Division of Developmental PediatricsHacettepe UniversityAnkaraTurkey
  2. 2.Faculty of Medicine, Department of Pediatrics, Department of Pediatric PulmonologyHacettepe UniversityAnkaraTurkey
  3. 3.Faculty of Medicine, Department of BiostatisticsHacettepe UniversityAnkaraTurkey

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