Impact of Cerebellar Injury on Neurodevelopmental Outcomes in Preterm Infants With Cerebral Palsy

Objective We aimed to analyze brain imaging findings and neurodevelopmental outcomes of preterm infants diagnosed with cerebral palsy. Design Brain magnetic resonance imaging of preterm infants born between 23 and 32 wks’ gestation and diagnosed with cerebral palsy at 2 yrs of corrected age were evaluated. Brain lesions were categorized as periventricular leukomalacia, intraventricular hemorrhage, and cerebellar hemorrhage and graded by the severity. Neurodevelopmental outcomes were assessed using the Bayley Scales of Infant and Toddler Development, Third Edition, at 18–24 mos corrected age, and the Korean Ages and Stages Questionnaire at 18 and 24 mos of corrected age. Results Cerebral palsy was found in 38 children (6.1%) among 618 survivors. Cerebellar injury of high-grade cerebellar hemorrhage and/or atrophy accounted for 25%. Among patients with supratentorial lesions, those having cerebellar injury showed significantly lower scores on each Korean Ages and Stages Questionnaire domain except gross motor than patients without cerebellar injury. They also revealed a high proportion of patients below the cutoff value of Korean Ages and Stages Questionnaire in language, fine motor, and problem-solving domains (P < 0.05) and lower Bayley Scales of Infant and Toddler Development, Third Edition, language composite scores (P = 0.038). Conclusions Poor neurodevelopmental outcomes other than motor function were associated with cerebellar injury. Evaluation of the cerebellum may help predict functional outcomes of patients with cerebral palsy.

[1]  I. Krägeloh-Mann,et al.  Neuroimaging Patterns and Function in Cerebral Palsy—Application of an MRI Classification , 2021, Frontiers in Neurology.

[2]  E. Sellier,et al.  Cerebral palsy in twins and higher multiple births: a Europe‐Australia population‐based study , 2021, Developmental medicine and child neurology.

[3]  P. Ellen Grant,et al.  Infant FreeSurfer: An automated segmentation and surface extraction pipeline for T1-weighted neuroimaging data of infants 0–2 years , 2020, NeuroImage.

[4]  S. Lydersen,et al.  Comorbidities in cerebral palsy: a patient registry study , 2020, Developmental medicine and child neurology.

[5]  L. D. de Vries,et al.  The CHOPIn Study: a Multicenter Study on Cerebellar Hemorrhage and Outcome in Preterm Infants , 2019, The Cerebellum.

[6]  Y. Chang,et al.  Neonatal Outcomes of Very Low Birth Weight Infants in Korean Neonatal Network from 2013 to 2016 , 2019, Journal of Korean medical science.

[7]  E. Kim,et al.  National Registry Data from Korean Neonatal Network: Two-Year Outcomes of Korean Very Low Birth Weight Infants Born in 2013–2014 , 2018, Journal of Korean medical science.

[8]  J. Shin,et al.  Incidence of Cerebral Palsy in Korea and the Effect of Socioeconomic Status: A Population-Based Nationwide Study , 2018, Yonsei medical journal.

[9]  K. Himmelmann,et al.  The panorama of cerebral palsy in Sweden part XII shows that patterns changed in the birth years 2007–2010 , 2018, Acta paediatrica.

[10]  U. Ådén,et al.  Cerebral Palsy in Extremely Preterm Infants , 2018, Pediatrics.

[11]  Jeroen Dudink,et al.  Impacts on prenatal development of the human cerebellum: a systematic review , 2017, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[12]  A. Starowicz-Filip,et al.  The role of the cerebellum in the regulation of language functions. , 2017, Psychiatria polska.

[13]  C. Vias,et al.  Cerebellar Contributions to Language in Typical and Atypical Development: A Review , 2017, Developmental neuropsychology.

[14]  Shirley Greenbaum,et al.  Cerebral Palsy—Trends in Epidemiology and Recent Development in Prenatal Mechanisms of Disease, Treatment, and Prevention , 2017, Front. Pediatr..

[15]  I. Krägeloh-Mann,et al.  MRI classification system (MRICS) for children with cerebral palsy: development, reliability, and recommendations , 2017, Developmental medicine and child neurology.

[16]  S. Sitaraman,et al.  Clinical Spectrum, Comorbidities, and Risk Factor Profile of Cerebral Palsy Children: A Prospective Study , 2017, Journal of pediatric neurosciences.

[17]  H. Arai,et al.  Cerebellar injury in preterm children with cerebral palsy after intraventricular hemorrhage: Prevalence and relationship to functional outcomes , 2015, Brain and Development.

[18]  Hiroyuki Kidokoro,et al.  Brain Injury and Altered Brain Growth in Preterm Infants: Predictors and Prognosis , 2014, Pediatrics.

[19]  K. Himmelmann,et al.  The panorama of cerebral palsy in Sweden. XI. Changing patterns in the birth‐year period 2003–2006 , 2014, Acta paediatrica.

[20]  K. Hustad,et al.  Speech and language development in 2-year-old children with cerebral palsy , 2014, Developmental neurorehabilitation.

[21]  Nicolas Guizard,et al.  Injury to the premature cerebellum: outcome is related to remote cortical development. , 2014, Cerebral cortex.

[22]  N. Jetté,et al.  An update on the prevalence of cerebral palsy: a systematic review and meta‐analysis , 2013, Developmental medicine and child neurology.

[23]  K. Haginoya,et al.  Brain magnetic resonance imaging and motor and intellectual functioning in 86 patients born at term with spastic diplegia , 2013, Developmental medicine and child neurology.

[24]  Steven P. Miller,et al.  Preterm Cerebellar Growth Impairment After Postnatal Exposure to Glucocorticoids , 2011, Science Translational Medicine.

[25]  B. Vohr,et al.  Expressive vocabulary of children with hearing loss in the first 2 years of life: impact of early intervention , 2011, Journal of Perinatology.

[26]  Colin Studholme,et al.  Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth. , 2011, The Journal of pediatrics.

[27]  G. Rosenbluth,et al.  Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. , 2011, The Journal of pediatrics.

[28]  J. Volpe.  Cerebellum of the Premature Infant: Rapidly Developing, Vulnerable, Clinically Important , 2009, Journal of child neurology.

[29]  F. Walther,et al.  Cerebellar injury in preterm infants: incidence and findings on US and MR images. , 2009, Radiology.

[30]  C. Van den Broeck,et al.  Prevalence, type, distribution, and severity of cerebral palsy in relation to gestational age: a meta‐analytic review , 2008, Developmental medicine and child neurology.

[31]  Catherine Limperopoulos,et al.  Does Cerebellar Injury in Premature Infants Contribute to the High Prevalence of Long-term Cognitive, Learning, and Behavioral Disability in Survivors? , 2007, Pediatrics.

[32]  J. Allsop,et al.  Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. , 2006, AJNR. American journal of neuroradiology.

[33]  Richard L Robertson,et al.  Impaired Trophic Interactions Between the Cerebellum and the Cerebrum Among Preterm Infants , 2005, Pediatrics.

[34]  D. Currie,et al.  Comparison of risk factors for cerebral palsy in twins and singletons. , 2005, Developmental medicine and child neurology.

[35]  J. Bodensteiner,et al.  Frequency and Nature of Cerebellar Injury in the Extremely Premature Survivor with Cerebral Palsy , 2005, Journal of child neurology.

[36]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[37]  H. Dolk,et al.  Multiple birth and cerebral palsy in Europe: a multicenter study , 2004, Acta obstetricia et gynecologica Scandinavica.

[38]  F. Cowan,et al.  MR imaging quantification of cerebellar growth following hypoxic-ischemic injury to the neonatal brain. , 2004, AJNR. American journal of neuroradiology.

[39]  T. Han,et al.  Risk Factors of Cerebral Palsy in Preterm Infants , 2002, American journal of physical medicine & rehabilitation.

[40]  G. Hägglund,et al.  Cerebral palsy in southern Sweden I. Prevalence and clinical features , 2001, Acta paediatrica.

[41]  M. Ditchfield,et al.  Magnetic resonance imaging findings in cerebral palsy , 2000, Journal of paediatrics and child health.

[42]  S. Fujimoto,et al.  Magnetic Resonance Imaging Children with Spastic Diplegia: Correlation with the Severity of their Motor and Mental Abnormality , 1991, Developmental medicine and child neurology.

[43]  L. Papile,et al.  Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. , 1978, The Journal of pediatrics.

[44]  W. Kułak,et al.  The cerebellum in children with spastic cerebral palsy: Volumetrics MRI study , 2011 .

[45]  L. Monte,et al.  [Bronchopulmonary dysplasia]. , 2005, Jornal de pediatria.

[46]  P. Grimaud.  [Cerebral palsy]. , 1972, Pediatrie.