PDF herunterladen
CC BY 4.0 · Arq Neuropsiquiatr 2025; 83(05): s00451809359
DOI: 10.1055/s-0045-1809359
Review Article

Could minor neurological dysfunction be a type of non-cerebral palsy motor impairment?

Ana Paula Hamad 
1   Universidade de São Paulo, Faculdade de Medicina de Ribeirão Preto, Departamento de Neurociências e Ciências do Comportamento, Ribeirão Preto SP, Brazil.
,
Carla Andrea Tanuri Cardoso Caldas 
1   Universidade de São Paulo, Faculdade de Medicina de Ribeirão Preto, Departamento de Neurociências e Ciências do Comportamento, Ribeirão Preto SP, Brazil.
,
Isabella Cristina Mendes de Sá e Silva 
1   Universidade de São Paulo, Faculdade de Medicina de Ribeirão Preto, Departamento de Neurociências e Ciências do Comportamento, Ribeirão Preto SP, Brazil.
,
Marina Estima Neiva Nunes 
1   Universidade de São Paulo, Faculdade de Medicina de Ribeirão Preto, Departamento de Neurociências e Ciências do Comportamento, Ribeirão Preto SP, Brazil.
› Institutsangaben
› Weitere Informationen
Auch verfügbar auf
  Lizenzen und Reprints

Abstract

Non-cerebral palsy motor impairments have been increasing over time, especially in preterm-born children, with a variety of labels, including, but not limited to, developmental coordination disorder and minor neurological dysfunction. They may not only negatively affect the child in their daily life activities, but are also associated with cognitive, emotional, and behavioral disorders, as well as decreased academic performance. Since there is a paucity of literature on non-cerebral palsy motor impairment, the main objective of the present study is to assess minor neurological dysfunction in the context of neurodevelopment. We reviewed the medical literature using the following search terms: preterm infants; follow-up; non-cerebral palsy motor impairment or disability; minor neurological dysfunction; developmental coordination disorder; neurological soft signs; and Touwen Neurological Examination. We compiled evidence-based data on minor neurological dysfunction critical domains, diagnosis, etiological factors and the influence of age and puberty in minor neurological signs. We also listed the cohort studies that used the Touwen Neurological Examination for premature or term-born follow-up, including those that suggest an association between minor neurological dysfunction and developmental coordination disorder as a motor impairment beyond cerebral palsy. Moreover, we found significant evidence of a correlation involving minor neurological dysfunction and cognitive, behavioral, and learning abilities, which, all in all, means that these children particularly deserve special attention regarding social, educational and healthcare resources. Furthermore, since motor activity seems to play an important role in the physical, mental, and neurological health of typical children, different approaches to education could have a positive impact on neurological development.

Keywords

Neurodevelopmental Disorders - Infant, Premature - Motor Skills Disorders - Psychomotor Disorders - Neurological Examination - Cognitive Dysfunction

Authors' Contributions

Conceptualization: APAH; Investigation: MENN; Supervision: APAH; Writing - original draft: APAH, CC, IMSS; Writing - review & editing; APAH, CC, IMSS, MENN.


Data Availability Statement

The contents underlying the research text are included in the manuscript.


Editor-in-Chief: Hélio A. G. Teive 0000-0003-2305-1073.


Associate Editor: Ana Carolina Coan 0000-0002-2888-929X.




Publikationsverlauf

Eingereicht: 05. September 2024

Angenommen: 11. März 2025

Artikel online veröffentlicht:
01. Juni 2025

© 2025. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution 4.0 International License, permitting copying and reproduction so long as the original work is given appropriate credit (https://creativecommons.org/licenses/by/4.0/)

Thieme Revinter Publicações Ltda.
Rua Rego Freitas, 175, loja 1, República, São Paulo, SP, CEP 01220-010, Brazil

Bibliographical Record
Ana Paula Hamad, Carla Andrea Tanuri Cardoso Caldas, Isabella Cristina Mendes de Sá e Silva, Marina Estima Neiva Nunes. Could minor neurological dysfunction be a type of non-cerebral palsy motor impairment?. Arq Neuropsiquiatr 2025; 83: s00451809359.
DOI: 10.1055/s-0045-1809359
 

  • References

  • 1 Spittle AJ, Cameron K, Doyle LW, Cheong JL. Victorian Infant Collaborative Study Group. Motor Impairment Trends in Extremely Preterm Children: 1991-2005. Pediatrics 2018; 141 (04) e20173410
    CrossrefPubMedSuche in Google Scholar
  • 2 Nosko D, Broström L, Bolk J, Ådén U, Örtqvist M. Changes in prevalence of non-optimal neurological condition between 6.5 and 12 years in children born extremely preterm. Eur J Paediatr Neurol 2023; 45: 14-18
    CrossrefPubMedSuche in Google Scholar
  • 3 Williams J, Lee KJ, Anderson PJ. Prevalence of motor-skill impairment in preterm children who do not develop cerebral palsy: a systematic review. Dev Med Child Neurol 2010; 52 (03) 232-237
    CrossrefPubMedSuche in Google Scholar
  • 4 Tommiska V, Lano A, Kleemola P, Klenberg L, Lehtonen L, Löppönen T. et al; Finnish ELBW Cohort Study Group (FinELBW). Analysis of neurodevelopmental outcomes of preadolescents born with extremely low weight revealed impairments in multiple developmental domains despite absence of cognitive impairment. Health Sci Rep 2020; 3 (03) e180
    CrossrefPubMedSuche in Google Scholar
  • 5 Erdi-Krausz G, Rocha R, Brown A, Myneni A, Lennartsson F, Romsauerova A. et al. Neonatal hypoxic-ischaemic encephalopathy: Motor impairment beyond cerebral palsy. Eur J Paediatr Neurol 2021; 35: 74-81
    CrossrefPubMedSuche in Google Scholar
  • 6 Blank R, Barnett AL, Cairney J, Green D, Kirby A, Polatajko H. et al. International clinical practice recommendations on the definition, diagnosis, assessment, intervention, and psychosocial aspects of developmental coordination disorder. Dev Med Child Neurol 2019; 61 (03) 242-285
    CrossrefPubMedSuche in Google Scholar
  • 7 American Psychiatric Association; DSM-5 Task Force. Diagnostic and statistical manual of mental disorders: DSM-5. 5th ed. Washington, DC: American Psychiatric Publishing, Inc.; 2013. . 10.1176/appi.books.9780890425596
    Suche in Google Scholar
  • 8 Lefèvre AB. Exame neurológico evolutivo. São Paulo: Sarvier; 1972
    Suche in Google Scholar
  • 9 Touwen BCL. Examination of the child with minor neurological dysfunction. 2nd ed. London: Heinemann Medical; 1979
    Suche in Google Scholar
  • 10 Hadders-Algra M. Two distinct forms of minor neurological dysfunction: perspectives emerging from a review of data of the Groningen Perinatal Project. Dev Med Child Neurol 2002; 44 (08) 561-571
    CrossrefPubMedSuche in Google Scholar
  • 11 Hadders-Algra M. Developmental coordination disorder: is clumsy motor behavior caused by a lesion of the brain at early age?. Neural Plast 2003; 10 (1-2): 39-50
    CrossrefPubMedSuche in Google Scholar
  • 12 Hadders-Algra M, Heineman KR, Bos AF, Middelburg KJ. The assessment of minor neurological dysfunction in infancy using the Touwen Infant Neurological Examination: strengths and limitations. Dev Med Child Neurol 2010; 52 (01) 87-92
    CrossrefPubMedSuche in Google Scholar
  • 13 Peters LH, Maathuis CG, Hadders-Algra M. Limited motor performance and minor neurological dysfunction at school age. Acta Paediatr 2011; 100 (02) 271-278
    CrossrefPubMedSuche in Google Scholar
  • 14 Jongmans M, Mercuri E, de Vries L, Dubowitz L, Henderson SE. Minor neurological signs and perceptual-motor difficulties in prematurely born children. Arch Dis Child Fetal Neonatal Ed 1997; 76 (01) F9-F14
    CrossrefPubMedSuche in Google Scholar
  • 15 D'Agati E, Pitzianti M, Curatolo P, Pasini A. Scientific Evidence for the Evaluation of Neurological Soft Signs as Atypical Neurodevelopment Markers in Childhood Neuropsychiatric Disorders. J Psychiatr Pract 2018; 24 (04) 230-238
    CrossrefPubMedSuche in Google Scholar
  • 16 Hadders-Algra M. Examination of the child with minor neurological dysfunction. 3rd ed. London: Mac Keith Press; 2010. . (Clinics in Developmental Medicine.)
    Suche in Google Scholar
  • 17 Hempel MS. The neurological examination technique for toddler-age. Groningen: : s.n.; 1993. . 232 p.
    Suche in Google Scholar
  • 18 Schendelaar P, Seggers J, Heineman MJ, Hadders-Algra M. Neurological condition assessed with the Hempel examination and cognition and behaviour at 4years. Early Hum Dev 2017; 112: 9-13
    CrossrefPubMedSuche in Google Scholar
  • 19 Werry JS, Aman MG. The reliability and diagnostic validity of the physical and neurological examination for soft signs (PANESS). J Autism Child Schizophr 1976; 6 (03) 253-262
    CrossrefPubMedSuche in Google Scholar
  • 20 Vitiello B, Ricciuti AJ, Stoff DM, Behar D, Denckla MB. Reliability of subtle (soft) neurological signs in children. J Am Acad Child Adolesc Psychiatry 1989; 28 (05) 749-753
    CrossrefPubMedSuche in Google Scholar
  • 21 Kikkert HK, de Jong C, Van den Heuvel ER, Hadders-Algra M. Minor neurological dysfunction and behaviour in 9-year-old children born at term: evidence for sex dimorphism. Dev Med Child Neurol 2013; 55 (11) 1023-1029
    CrossrefPubMedSuche in Google Scholar
  • 22 Peters LH, Maathuis KG, Kouw E, Hamming M, Hadders-Algra M. Test-retest, inter-assessor and intra-assessor reliability of the modified Touwen examination. Eur J Paediatr Neurol 2008; 12 (04) 328-333
    CrossrefPubMedSuche in Google Scholar
  • 23 Fily A, Truffert P, Ego A, Depoortere MH, Haquin C, Pierrat V. Neurological assessment at five years of age in infants born preterm. Acta Paediatr 2003; 92 (12) 1433-1437
    CrossrefSuche in Google Scholar
  • 24 Kakebeeke TH, Jongmans MJ, Dubowitz LM, Schoemaker MM, Henderson SE. Some aspects of the reliability of Touwen's examination of the child with minor neurological dysfunction. Dev Med Child Neurol 1993; 35 (12) 1097-1105
    CrossrefPubMedSuche in Google Scholar
  • 25 Davis NM, Ford GW, Anderson PJ, Doyle LW. Victorian Infant Collaborative Study Group. Developmental coordination disorder at 8 years of age in a regional cohort of extremely-low-birthweight or very preterm infants. Dev Med Child Neurol 2007; 49 (05) 325-330
    CrossrefPubMedSuche in Google Scholar
  • 26 Broström L, Vollmer B, Bolk J, Eklöf E, Ådén U. Minor neurological dysfunction and associations with motor function, general cognitive abilities, and behaviour in children born extremely preterm. Dev Med Child Neurol 2018; 60 (08) 826-832
    CrossrefPubMedSuche in Google Scholar
  • 27 Larroque B, Ancel PY, Marret S, Marchand L, André M, Arnaud C. et al; EPIPAGE Study group. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet 2008; 371 (9615) 813-820
    CrossrefPubMedSuche in Google Scholar
  • 28 Stirrups R. Mijna Hadders-Algra. Lancet Child Adolesc Health 2020; 4 (03) 181
    CrossrefPubMedSuche in Google Scholar
  • 29 Hadders-Algra M, Touwen BC, Olinga AA, Huisjes HJ. Minor neurological dysfunction and behavioural development. A report from the Groningen Perinatal Project. Early Hum Dev 1985; 11 (3-4): 221-229
    CrossrefPubMedSuche in Google Scholar
  • 30 Arnaud C, Daubisse-Marliac L, White-Koning M, Pierrat V, Larroque B, Grandjean H. et al. Prevalence and associated factors of minor neuromotor dysfunctions at age 5 years in prematurely born children: the EPIPAGE Study. Arch Pediatr Adolesc Med 2007; 161 (11) 1053-1061
    CrossrefPubMedSuche in Google Scholar
  • 31 Hadders-Algra M, Touwen BC. Minor neurological dysfunction is more closely related to learning difficulties than to behavioral problems. J Learn Disabil 1992; 25 (10) 649-657
    CrossrefPubMedSuche in Google Scholar
  • 32 Kikkert HK, De Jong C, Hadders-Algra M. Minor neurological dysfunction and IQ in 9-year-old children born at term. Dev Med Child Neurol 2011; 53 (04) e16-e25
    CrossrefPubMedSuche in Google Scholar
  • 33 Punt M, De Jong M, De Groot E, Hadders-Algra M. Minor neurological dysfunction in children with dyslexia. Dev Med Child Neurol 2010; 52 (12) 1127-1132
    CrossrefPubMedSuche in Google Scholar
  • 34 Hadders-Algra M, Huisjes HJ, Touwen BC. Perinatal risk factors and minor neurological dysfunction: significance for behaviour and school achievement at nine years. Dev Med Child Neurol 1988; 30 (04) 482-491
    CrossrefPubMedSuche in Google Scholar
  • 35 Soorani-Lunsing RJ, Hadders-Algra M, Olinga AA, Huisjes HJ, Touwen BC. Is minor neurological dysfunction at 12 years related to behaviour and cognition?. Dev Med Child Neurol 1993; 35 (04) 321-330
    CrossrefPubMedSuche in Google Scholar
  • 36 Lunsing RJ, Hadders-Algra M, Huisjes HJ, Touwen BC. Minor neurological dysfunction from birth to 12 years. I: Increase during late school-age. Dev Med Child Neurol 1992; 34 (05) 399-403
    CrossrefPubMedSuche in Google Scholar
  • 37 Lunsing RJ, Hadders-Algra M, Huisjes HJ, Touwen BC. Minor neurological dysfunction from birth to 12 years. II: Puberty is related to decreased dysfunction. Dev Med Child Neurol 1992; 34 (05) 404-409
    CrossrefPubMedSuche in Google Scholar
  • 38 Soorani-Lunsing RJ, Hadders-Algra M, Huisjes HJ, Touwen BC. Neurobehavioural relationships after the onset of puberty. Dev Med Child Neurol 1994; 36 (04) 334-343
    CrossrefPubMedSuche in Google Scholar
  • 39 Hadders-Algra M, Gramsbergen A. Discussion: significance and treatment of clumsiness in children. Neural Plast 2003; 10 (1-2): 165-178
    CrossrefPubMedSuche in Google Scholar
  • 40 Yildiz R, Yildiz A, Gucuyener K, Acar ASS, Elbasan B. Minor neurological dysfunction in preterm children and its association with school readiness. Int J Disabil Dev Educ 2020; 67 (02) 125-134 Available from: https://www.tandfonline.com/doi/full/10.1080/1034912X.2019.1614154
    CrossrefSuche in Google Scholar
  • 41 Van Hus JW, Potharst ES, Jeukens-Visser M, Kok JH, Van Wassenaer-Leemhuis AG. Motor impairment in very preterm-born children: links with other developmental deficits at 5 years of age. Dev Med Child Neurol 2014; 56 (06) 587-594
    CrossrefPubMedSuche in Google Scholar
  • 42 Kurpershoek T, Potharst-Sirag ES, Aarnoudse-Moens CS, Van Wassenaer-Leemhuis AG. Minor neurological dysfunction in five year old very preterm children is associated with lower processing speed. Early Hum Dev 2016; 103: 55-60
    CrossrefPubMedSuche in Google Scholar
  • 43 Mikkola K, Ritari N, Tommiska V, Salokorpi T, Lehtonen L, Tammela O. et al. Neurodevelopmental outcome at 5 years of age of a national cohort of extremely low birth weight infants who were born in 1996-1997. Pediatrics 2005; 116 (06) 1391-1400
    CrossrefPubMedSuche in Google Scholar
  • 44 Edwards J, Berube M, Erlandson K, Haug S, Johnstone H, Meagher M. et al. Developmental coordination disorder in school-aged children born very preterm and/or at very low birth weight: a systematic review. J Dev Behav Pediatr 2011; 32 (09) 678-687
    CrossrefPubMedSuche in Google Scholar
  • 45 Peters LHJ, Maathuis CGB, Hadders-Algra M. Neural correlates of developmental coordination disorder. Dev Med Child Neurol 2013; 55 (Suppl. 04) 59-64
    CrossrefPubMedSuche in Google Scholar
  • 46 Niutanen U, Lönnberg P, Wolford E, Metsäranta M, Lano A. Extremely preterm children and relationships of minor neurodevelopmental impairments at 6 years. Front Psychol 2022; 13: 996472
    CrossrefPubMedSuche in Google Scholar
  • 47 Schmitt BD. The minimal brain dysfunction myth. Am J Dis Child 1975; 129 (11) 1313-1318
    CrossrefPubMedSuche in Google Scholar
  • 48 Lange KW, Reichl S, Lange KM, Tucha L, Tucha O. The history of attention deficit hyperactivity disorder. Atten Defic Hyperact Disord 2010; 2 (04) 241-255
    CrossrefPubMedSuche in Google Scholar
  • 49 Goulardins JB, Rigoli D, Licari M, Piek JP, Hasue RH, Oosterlaan J, Oliveira JA. Attention deficit hyperactivity disorder and developmental coordination disorder: Two separate disorders or do they share a common etiology. Behav Brain Res 2015; 292: 484-492
    CrossrefPubMedSuche in Google Scholar
  • 50 Goulardins JB, Marques JC, Oliveira JAd. Attention Deficit Hyperactivity Disorder and Motor Impairment. Percept Mot Skills 2017; 124 (02) 425-440
    CrossrefPubMedSuche in Google Scholar
  • 51 Lou HC, Henriksen L, Bruhn P, Børner H, Nielsen JB. Striatal dysfunction in attention deficit and hyperkinetic disorder. Arch Neurol 1989; 46 (01) 48-52
    CrossrefPubMedSuche in Google Scholar
  • 52 Paulsen K, O'Donnell JP. Construct validation of children's behavior problem dimensions: relationship to activity level, impulsivity, and soft neurological signs. J Psychol 1979; 101 (2d Half): 273-278
    CrossrefPubMedSuche in Google Scholar
  • 53 Hertzig ME. Neurological ‘soft’ signs in low-birthweight children. Dev Med Child Neurol 1981; 23 (06) 778-791
    CrossrefPubMedSuche in Google Scholar
  • 54 Rutter M. Developmental neuropsychiatry: concepts, issues and prospects. J Clin Neuropsychol 1982; 4 (02) 91-115
    CrossrefPubMedSuche in Google Scholar
  • 55 Sato M, Aotani H, Hattori R, Funato M. Behavioral outcome including attention deficit hyperactivity disorder/hyperactivity disorder and minor neurological signs in perinatal high-risk newborns at 4-6 years of age with relation to risk factors. Pediatr Int 2004; 46 (03) 346-352
    CrossrefPubMedSuche in Google Scholar
  • 56 Pitzianti M, D'Agati E, Casarelli L, Pontis M, Kaunzinger I, Lange KW. et al. Neurological soft signs are associated with attentional dysfunction in children with attention deficit hyperactivity disorder. Cogn Neuropsychiatry 2016; 21 (06) 475-493
    CrossrefPubMedSuche in Google Scholar
  • 57 Kikkert HK, De Jong C, Hadders-Algra M. Minor neurological dysfunction and cognition in 9-year-olds born at term. Early Hum Dev 2013; 89 (05) 263-270
    CrossrefPubMedSuche in Google Scholar
  • 58 Fonseca Vd. Desenvolvimento psicomotor e aprendizagem. Porto Alegre: ArtMed; 2008
    Suche in Google Scholar
  • 59 Adolph KE, Hoch JE. Motor development: embodied, embedded, enculturated, and enabling. Annu Rev Psychol 2019; 70: 141-164
    CrossrefPubMedSuche in Google Scholar
  • 60 Strasburger VC. Council on Communications and Media. Children, adolescents, obesity, and the media. Pediatrics 2011; 128 (01) 201-208
    CrossrefPubMedSuche in Google Scholar
  • 61 Kirkorian HL, Pempek TA, Murphy LA, Schmidt ME, Anderson DR. The impact of background television on parent-child interaction. Child Dev 2009; 80 (05) 1350-1359
    CrossrefPubMedSuche in Google Scholar
  • 62 Brooks SJ, Parks SM, Stamoulis C. Widespread Positive Direct and Indirect Effects of Regular Physical Activity on the Developing Functional Connectome in Early Adolescence. Cereb Cortex 2021; 31 (10) 4840-4852
    CrossrefPubMedSuche in Google Scholar
  • 63 Diamond A, Ling DS. Conclusions about interventions, programs, and approaches for improving executive functions that appear justified and those that, despite much hype, do not. Dev Cogn Neurosci 2016; 18: 34-48
    CrossrefPubMedSuche in Google Scholar