Enriched environments and motor outcomes in cerebral palsy: systematic review and meta-analysis.
Abstract
BACKGROUND AND OBJECTIVES: Neuroplasticity evidence from animals favors an early enriched environment for promoting optimal brain injury recovery. In infants, systematic reviews show environmental enrichment (EE) improves cognitive outcomes but the effect on motor skills is less understood. The objective of this review was to appraise the effectiveness evidence about EE for improving the motor outcomes of infants at high risk of cerebral palsy (CP). METHODS: A systematic review was conducted. Cochrane Central Register of Controlled Trials (PubMed), Cumulative Index to Nursing and Allied Health Literature, Education Resource Information Center, SocINDEX, and PsycINFO databases were searched for literature meeting inclusion criteria: randomized controlled trials; high risk of /diagnosis of CP; >25% participants ≤2 years; parent or infant interventions postdischarge; and motor outcomes reported. Data were extracted using the Cochrane protocol regarding participants, intervention characteristics, and outcomes. Methodological quality was assessed using risk of bias assessment and GRADE. RESULTS: A total of 226 studies were identified. After removing duplicates and unrelated studies, 16 full-text articles were reviewed, of which 7 studies met inclusion criteria. The risk of bias varied between studies with the more recent studies demonstrating the lowest risk. Enrichment interventions varied in type and focus, making comparisons difficult. A meta-analysis was conducted of studies that compared enrichment to standard care (n = 5), and totaled 150 infants. A small positive effect for enrichment was found; standardized mean difference 0.39 (95% confidence interval 0.05-0.72; I(2) = 3%; P = .02) CONCLUSIONS: EE looks promising for CP, and therefore high-quality studies with well-defined EE strategies are urgently required.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The age association is consistent with early intervention because younger children may have more brain plasticity and adaptability.
“This was consistent with the idea of early intervention as younger children may have more brain plasticity and adaptability to improve their motor function than children at older ages.71,72”
From Effectiveness of Virtual Reality in Children With Cerebral Palsy: A Systematic Review and Meta-Analysis of Randomized Controlled Trials (2018) · cites this paper as [71]
Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series
(2008) · doi:10.1002/9780470712184 · Cited by 25,048 · see citing works
GRADE: an emerging consensus on rating quality of evidence and strength of recommendations
Guyatt, G. H., Oxman, A. D., Vist, G. E., Kunz, R., Falck-Ytter, Y., Alonso-Coello, P., & Schünemann, H. J. (2008) · BMJ · doi:10.1136/bmj.39489.470347.ad · Cited by 23,305 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2009.06.005 · Cited by 19,575 · see citing works
Palisano, R. J., Rosenbaum, P., Walter, S. D., Russell, D., Wood, E. P., & Galuppi, B. E. (1997) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.1997.tb07414.x · Cited by 6,728 · see citing works
From Neurons to Neighborhoods: The Science of Early Childhood Development
(2000) · doi:10.17226/9824 · Cited by 4,484 · see citing works
Bayley Scales of Infant Development
(2007) · Sage eBooks · doi:10.4135/9781412952644.n48 · Cited by 4,242 · see citing works
Neural consequences of enviromental enrichment
van Praag, H., Kempermann, G., & Gage, F. H. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044558 · Cited by 2,468 · see citing works
Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771 · see citing works
Bayley Scales of Infant Development
Lennon, E. M., Gardner, J. M., Karmel, B. Z., & Flory, M. J. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.23376-2 · Cited by 1,310 · see citing works
Spittle, A. J., Orton, J., Anderson, P. J., Boyd, R. N., & Doyle, L. W. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005495.pub4 · Cited by 1,072 · see citing works
Prognosis for Gross Motor Function in Cerebral Palsy
Rosenbaum, P., Walter, S. D., Hanna, S., Palisano, R. J., Russell, D. J., Raina, P. S., Wood, E. P., Bartlett, D. J., & Galuppi, B. E. (2002) · JAMA · doi:10.1001/jama.288.11.1357 · Cited by 1,051 · see citing works
Early experience alters brain function and structure
Als, H., Duffy, F. H., McAnulty, G. B., Rivkin, M. J., Vajapeyam, S., Mulkern, R. V., Warfield, S. K., Huppi, P. S., Butler, S. C., Conneman, N., et al. (2004) · Pediatrics · doi:10.1542/peds.113.4.846 · Cited by 890 · see citing works
Biernaskie, J. A., & Corbett, D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05272.2001 · Cited by 608 · see citing works
Taub, E., Ramey, S. L., DeLuca, S., & Echols, K. (2004) · PEDIATRICS · doi:10.1542/peds.113.2.305 · Cited by 460 · see citing works
A systematic review of the effects of early intervention on motor development
Blauw-Hospers, C. H., & Hadders‐Algra, M. (2005) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162205000824 · Cited by 350 · see citing works
Will, B. E., Galani, R., Kelche, C. R., & Rosenzweig, M. R. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.03.001 · Cited by 349 · see citing works
Enrich the environment to empower the brain
Sale, A., Berardi, N., & Maffei, L. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2008.12.004 · Cited by 341 · see citing works
Bradley, R. H., Whiteside, L., Mundfrom, D. J., Casey, P. H., Kelleher, K. J., & Pope, S. K. (1994) · Child Development · doi:10.1111/j.1467-8624.1994.tb00755.x · Cited by 338 · see citing works
The caregiving context in institution-reared and family-reared infants and toddlers in Romania
Smyke, A. T., Koga, S. F., Johnson, D. E., Fox, N. A., Marshall, P. J., Nelson, C. A., Zeanah, C. H., & the BEIP Core Group (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01694.x · Cited by 319 · see citing works
McIntyre, S., Morgan, C., Walker, K., & Novak, I. (2011) · Developmental Disabilities Research Reviews · doi:10.1002/ddrr.1106 · Cited by 304 · see citing works
Effects of neurodevelopmental treatment (NDT) for cerebral palsy: an AACPDM evidence report
Butler, C., PhD, J. D., Adams, R., Chambers, H., Abel, M., Damiano, D., Edgar, T., Msall, M., Samson‐Fang, L., Stott, N. S., et al. (2001) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162201001414 · Cited by 297 · see citing works
The Reliability and Validity of the Quality of Upper Extremity Skills Test
DeMatteo, C. A., Law, M., Russell, D. J., Pollock, N., Rosenbaum, P., & Walter, S. D. (1993) · Physical & Occupational Therapy In Pediatrics · doi:10.1080/j006v13n02_01 · Cited by 287 · see citing works
Clinical disorders of brain plasticity
Johnston, M. V. (2003) · Brain and Development · doi:10.1016/s0387-7604(03)00102-5 · Cited by 275 · see citing works
The Effects of Physical Therapy on Cerebral Palsy
Palmer, F. B. S. C., Shapiro, B. K., Wachtel, R. C., Allen, M. C., Hiller, J. E., Harryman, S. E., Mosher, B. S., Meinert, C. L., & Capute, A. J. (1988) · New England Journal of Medicine · doi:10.1056/nejm198803313181302 · Cited by 270 · see citing works
Massage Accelerates Brain Development and the Maturation of Visual Function
Guzzetta, A., Baldini, S., Bancale, A., Baroncelli, L., Ciucci, F., Ghirri, P., Putignano, E., Sale, A., Viegi, A., Berardi, N., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5548-08.2009 · Cited by 244 · see citing works
ORTON, J., Spittle, A. J., Doyle, L. W., Anderson, P. J., & Boyd, R. N. (2009) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2009.03414.x · Cited by 240 · see citing works
Efficacy of Interventions to Improve Motor Development in Young Children: A Systematic Review
Riethmuller, A., Jones, R. A., & Okely, A. D. (2009) · PEDIATRICS · doi:10.1542/peds.2009-0333 · Cited by 230 · see citing works
Law, M., Darrah, J., Pollock, N., WILSON, B., Russell, D. J., Walter, S. D., Rosenbaum, P., & Galuppi, B. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.03962.x · Cited by 229 · see citing works
Bradley, R. H., Whiteside, L., Mundfrom, D. J., et al. (1994) · Child Development · doi:10.2307/1131388 · Cited by 195 · see citing works
Spittle, A. J., Boyd, R. N., Inder, T. E., & Doyle, L. W. (2009) · PEDIATRICS · doi:10.1542/peds.2008-0590 · Cited by 186 · see citing works
Ketelaar, M., Vermeer, A., & Helders, P. J. M. (1998) · Clinical Rehabilitation · doi:10.1191/026921598673571117 · Cited by 174 · see citing works
COMMITTEE ON INTEGRATING THE SCIENCE OF EARLY CHILDHOOD DEVELOPMENT
Shonkoff, J. P., & Phillips, D. A. (2000) · Cited by 170 · see citing works
The predictive validity of general movements – A systematic review
Burger, M., & Louw, Q. A. (2008) · European Journal of Paediatric Neurology · doi:10.1016/j.ejpn.2008.09.004 · Cited by 169 · see citing works
Löwing, K., Bexelius, A., & Carlberg, E. B. (2009) · Disability and Rehabilitation · doi:10.1080/09638280902822278 · Cited by 143 · see citing works
Quality of General Movements Is Related to White Matter Pathology in Very Preterm Infants
Spittle, A. J., Brown, N. C., Doyle, L. W., Boyd, R. N., Hunt, R. W., Bear, M. J., & Inder, T. E. (2008) · PEDIATRICS · doi:10.1542/peds.2007-1924 · Cited by 138 · see citing works
Enhanced Handling and Positioning in Early Infancy Advances Development Throughout the First Year
Lobo, M. A., & Galloway, J. C. (2012) · Child Development · doi:10.1111/j.1467-8624.2012.01772.x · Cited by 125 · see citing works
Modified constraint-induced therapy for children with hemiplegic cerebral palsy: a randomized trial
Wallen, M. A., Ziviani, J. M., Naylor, O., Evans, R., Novak, I., & Herbert, R. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.04086.x · Cited by 116 · see citing works
Bakermans‐Kranenburg, M. J., van IJzendoorn, M. H., & Juffer, F. (2008) · Monographs of the Society for Research in Child Development · doi:10.1111/j.1540-5834.2008.00498.x · Cited by 116 · see citing works
Influence of supine sleep positioning on early motor milestone acquisition
Majnemer, A., & Barr, R. G. (2005) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162205000733 · Cited by 115 · see citing works
Heathcock, J., Lobo, M. A., & Galloway, J. C. (2007) · Physical Therapy · doi:10.2522/ptj.20070145 · Cited by 105 · see citing works
Physical Therapy as a Determinant of Change in the Cerebral Palsied Infant
Scherzer, A. L., Miké, V., & Ilson, J. B. (1976) · PEDIATRICS · doi:10.1542/peds.58.1.47 · Cited by 104 · see citing works
Effect of Music by Mozart on Energy Expenditure in Growing Preterm Infants
Lubetzky, R., Mimouni, F. B., Dollberg, S., Reifen, R. M., Ashbel, G., & Mandel, D. (2009) · PEDIATRICS · doi:10.1542/peds.2009-0990 · Cited by 104 · see citing works
Blauw-Hospers, C. H., DEGRAAFPETERS, V., Dirks, T., Bos, A. F., & Hadders‐Algra, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.010 · Cited by 100 · see citing works
Pediatric Physical Therapy in Infancy: From Nightmare to Dream? A Two-Arm Randomized Trial
Blauw-Hospers, C. H., Dirks, T., Hulshof, L. J., Bos, A. F., & Hadders‐Algra, M. (2011) · Physical Therapy · doi:10.2522/ptj.20100205 · Cited by 99 · see citing works
Preventive Interventions for Preterm Children
Guralnick, M. J. (2012) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e31824eaa3c · Cited by 92 · see citing works
Dirks, T., Blauw-Hospers, C. H., Hulshof, L. J., & Hadders‐Algra, M. (2011) · Physical Therapy · doi:10.2522/ptj.20100207 · Cited by 88 · see citing works
Effect of an early intervention programme on low birthweight infants with cerebral injuries
Ohgi, S., Fukuda, M., Akiyama, T., & Gima, H. (2004) · Journal of Paediatrics and Child Health · doi:10.1111/j.1440-1754.2004.00512.x · Cited by 84 · see citing works
Infant motor development and equipment use in the home
Abbott, A., & Bartlett, D. J. (2001) · Child Care Health and Development · doi:10.1046/j.1365-2214.2001.00186.x · Cited by 70 · see citing works
Early Intensive Postural and Movement Training Advances Head Control in Very Young Infants
Lee, H.-M., & Galloway, J. C. (2012) · Physical Therapy · doi:10.2522/ptj.20110196 · Cited by 66 · see citing works
Spittle, A. J., Ferretti, C., Anderson, P. J., Orton, J., Eeles, A. L., Bates, L., Boyd, R. N., Inder, T. E., & Doyle, L. W. (2009) · BMC Pediatrics · doi:10.1186/1471-2431-9-73 · Cited by 60 · see citing works
Nelson, M. N., White‐Traut, R. C., Vasan, U., Silvestri, J. M., Comiskey, E., Meleedy‐Rey, P., Littau, S., Gu, G., & Patel, M. (2001) · Journal of Child Neurology · doi:10.1177/088307380101600706 · Cited by 57 · see citing works
DISTILLING THE EVIDENCE ON DEVELOPMENTAL CARE
Symington, A., & Pinelli, J. M. (2002) · Advances in Neonatal Care · doi:10.1053/adnc.2002.34546 · Cited by 51 · see citing works
The Relationship Between the Home Environment and Early Motor Development
Abbott, A., & Bartlett, D. J. (1999) · Physical & Occupational Therapy In Pediatrics · doi:10.1080/j006v19n01_04 · Cited by 41 · see citing works
Intervention for infants with brain injury: Results of a randomized controlled study
Badr, L. K., Garg, M., & Kamath, M. (2005) · Infant Behavior and Development · doi:10.1016/j.infbeh.2005.08.003 · Cited by 40 · see citing works
Animal Research on Effects of Experience on Brain and Behavior
Rosenzweig, M. R. (2002) · Infants & Young Children · doi:10.1097/00001163-200210000-00003 · Cited by 5 · see citing works
NDT in the United States Changes in Theory Advance Clinical Practice
Howle, J. M. (2007) · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Novak, I., Morgan, C., Fahey, M. C., Finch‐Edmondson, M., Galea, C., Hines, A., Langdon, K., McNamara, M., Paton, M. C. B., Popat, H. P., et al. (2020) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-020-1022-z · Cited by 1,208 · see citing works
Spittle, A. J., Orton, J., Anderson, P. J., Boyd, R. N., & Doyle, L. W. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005495.pub4 · Cited by 1,072 · see citing works
Environmental enrichment, new neurons and the neurobiology of individuality
Kempermann, G. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0120-x · Cited by 479 · see citing works
Pierce, K., Gazestani, V. H., Bacon, E., Barnes, C. C., Cha, D., Nalabolu, S., Lopez, L., Moore, A., Pence-Stophaeros, S., & Courchesne, E. (2019) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2019.0624 · Cited by 333 · see citing works
Emerging connections between cerebellar development, behaviour and complex brain disorders
Sathyanesan, A., Zhou, J., Scafidi, J., Heck, D. H., Sillitoe, R. V., & Gallo, V. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0152-2 · Cited by 322 · see citing works
Evidence-Based Diagnosis, Health Care, and Rehabilitation for Children With Cerebral Palsy
Novak, I. (2014) · Journal of Child Neurology · doi:10.1177/0883073814535503 · Cited by 264 · see citing works
Chen, Y., Fanchiang, H. D., & Howard, A. (2018) · Physical Therapy · doi:10.1093/ptj/pzx107 · Cited by 257 · see citing works
Early intervention in neurodevelopmental disorders: underlying neural mechanisms
Cioni, G., Inguaggiato, E., & Sgandurra, G. (2016) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13050 · Cited by 214 · see citing works
Spittle, A. J., & Treyvaud, K. (2016) · Seminars in Perinatology · doi:10.1053/j.semperi.2016.09.006 · Cited by 193 · see citing works
Early environment and long-term outcomes of preterm infants
Cheong, J. L. Y., Burnett, A., Treyvaud, K., & Spittle, A. J. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02121-w · Cited by 195 · see citing works
Early identification and intervention in cerebral palsy
Herskind, A., Greisen, G. O., & Nielsen, J. B. (2014) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.12531 · Cited by 159 · see citing works
Effect of early intervention in infants at very high risk of cerebral palsy: a systematic review
Hadders‐Algra, M., Boxum, A. G., Hielkema, T., & Hamer, E. G. (2016) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13331 · Cited by 154 · see citing works
Development (of Walking): 15 Suggestions
Adolph, K. E., Hoch, J. E., & Cole, W. G. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.05.010 · Cited by 146 · see citing works
Optimising motor learning in infants at high risk of cerebral palsy: a pilot study
Morgan, C., Novak, I., Dale, R. C., & Badawi, N. A. (2015) · BMC Pediatrics · doi:10.1186/s12887-015-0347-2 · Cited by 138 · see citing works
Khurana, S. G., Kane, A. E., Brown, S. E., Tarver, T., & Dusing, S. C. (2020) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.14485 · Cited by 131 · see citing works
Whittingham, K., Sanders, M. R., McKinlay, L., & Boyd, R. N. (2016) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsv118 · Cited by 113 · see citing works
Virtual Reality in Neurorehabilitation: An Umbrella Review of Meta-Analyses
Voinescu, A., Sui, J., & Fraser, D. S. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10071478 · Cited by 117 · see citing works
Lucas, B. R., Elliott, E. J., Coggan, S. E., Pinto, R. Z., Jirikowic, T., McCoy, S. W., & Latimer, J. (2016) · BMC Pediatrics · doi:10.1186/s12887-016-0731-6 · Cited by 121 · see citing works
Interventions to Reduce Behavioral Problems in Children With Cerebral Palsy: An RCT
Whittingham, K., Sanders, M., McKinlay, L., & Boyd, R. N. (2014) · Pediatrics · doi:10.1542/peds.2013-3620 · Cited by 105 · see citing works
Hubermann, L., Boychuck, Z., Shevell, M. I., & Majnemer, A. (2015) · Journal of Child Neurology · doi:10.1177/0883073815596610 · Cited by 103 · see citing works
Damiano, D. L., & Longo, E. (2021) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.14855 · Cited by 99 · see citing works
Dusing, S. C., Tripathi, T., Marcinowski, E. C., Thacker, L. R., Brown, L., & Hendricks‐Muñoz, K. D. (2018) · BMC Pediatrics · doi:10.1186/s12887-018-1011-4 · Cited by 98 · see citing works
Orton, J., Doyle, L. W., Tripathi, T., Boyd, R. N., Anderson, P. J., & Spittle, A. J. (2024) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005495.pub5 · Cited by 98 · see citing works
Sgandurra, G., Lorentzen, J., Inguaggiato, E., Bartalena, L., Beani, E., Cecchi, F., Dario, P., Giampietri, M., Greisen, G. O., Herskind, A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173521 · Cited by 95 · see citing works
Morgan, C., Novak, I., Dale, R. C., Guzzetta, A., & Badawi, N. A. (2014) · BMC Neurology · doi:10.1186/s12883-014-0203-2 · Cited by 95 · see citing works
Chen, Y.-P., Lee, S.-Y., & Howard, A. M. (2014) · Pediatric Physical Therapy · doi:10.1097/pep.0000000000000046 · Cited by 86 · see citing works
High-risk follow-up: Early intervention and rehabilitation
Novak, I., & Morgan, C. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64029-1.00023-0 · Cited by 87 · see citing works
Early intervention programmes for infants at high risk of atypical neurodevelopmental outcome
Hutchon, B., Gibbs, D., Harniess, P., Jary, S., Crossley, S., Moffat, J., Basu, N., & Basu, A. P. (2019) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.14187 · Cited by 84 · see citing works
The role of enriched environment in neural development and repair
Han, Y., Yuan, M., Guo, Y., Shen, X.-Y., Gao, Z.-K., & Bi, X. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.890666 · Cited by 89 · see citing works
Inguaggiato, E., Sgandurra, G., & Cioni, G. (2017) · Neuropsychiatrie de l Enfance et de l Adolescence · doi:10.1016/j.neurenf.2017.03.009 · Cited by 78 · see citing works
Robotic Therapies for Children with Cerebral Palsy: A Systematic Review
Bayón, C., & Raya, R. (2016) · Translational Biomedicine · doi:10.21767/2172-0479.100044 · Cited by 77 · see citing works
Neurodevelopmental Therapy for Cerebral Palsy: A Meta-analysis
Velde, A. T., Morgan, C., Finch‐Edmondson, M., McNamara, L., McNamara, M., Paton, M. C. B., Stanton, E., Webb, A., Badawi, N. A., & Novak, I. (2022) · PEDIATRICS · doi:10.1542/peds.2021-055061 · Cited by 76 · see citing works
Activity-Based Therapies for Repair of the Corticospinal System Injured during Development
Friel, K. M., Williams, P. T. J. A., Serradj, N., Chakrabarty, S., & Martin, J. H. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00229 · Cited by 76 · see citing works
Byrne, R., Duncan, A. F., Pickar, T., Burkhardt, S., Boyd, R. N., Neel, M. L., & Maitre, N. L. (2019) · Child Care Health and Development · doi:10.1111/cch.12707 · Cited by 75 · see citing works
Downs, J. A., Rodger, J., Li, C., Tan, X., Hu, N., Wong, K., de Klerk, N. H., & Leonard, H. (2018) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-017-0752-8 · Cited by 70 · see citing works
Prescribing Physical, Occupational, and Speech Therapy Services for Children With Disabilities
Houtrow, A. J., Murphy, N., Kuo, D. Z., Apkon, S. D., Brei, T. J., Davidson, L. F., Davis, B. E., Ellerbeck, K. A., Hyman, S. L., Leppert, M. L. O., et al. (2019) · PEDIATRICS · doi:10.1542/peds.2019-0285 · Cited by 69 · see citing works
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
Festante, F., Antonelli, C., Chorna, O. D., Corsi, G., & Guzzetta, A. (2019) · Neural Plasticity · doi:10.1155/2019/5759694 · Cited by 62 · see citing works
Silveira, R. C., Mendes, E. W., Fuentefria, R. D. N., Valentini, N. C., & Procianoy, R. S. (2018) · BMC Pediatrics · doi:10.1186/s12887-018-1240-6 · Cited by 58 · see citing works
Mohandas, N., Bass-Stringer, S., Maksimovic, J., Crompton, K. E., Loke, Y. J., Walstab, J., Reid, S. M., Amor, D. J., Reddihough, D. S., & Craig, J. M. (2018) · Clinical Epigenetics · doi:10.1186/s13148-018-0457-4 · Cited by 56 · see citing works
Benfer, K. A., Novak, I., Morgan, C., Whittingham, K., Khan, N. Z., Ware, R. S., Bell, K. L., Bandaranayake, S., Salt, A., Ghosh, A. K., et al. (2018) · BMJ Open · doi:10.1136/bmjopen-2017-021186 · Cited by 52 · see citing works
Brain structural maturation and the foundations of cognitive behavioral development
Walhovd, K. B., Tamnes, C. K., & Fjell, A. M. (2014) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000074 · Cited by 50 · see citing works
Physical therapy in children with cerebral palsy in Brazil: a scoping review
Furtado, M. A. D. S., Ayupe, K. M. A., Christovão, I. S., de Sousa, R. R., Rosenbaum, P., Camargos, A. C. R., & Leite, H. R. (2021) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.15067 · Cited by 50 · see citing works
Sgandurra, G., Bartalena, L., Cecchi, F., Cioni, G., Giampietri, M., Greisen, G. O., Herskind, A., Inguaggiato, E., Lorentzen, J., Nielsen, J. B., et al. (2016) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2016.01.013 · Cited by 45 · see citing works
Treadmill interventions in children under six years of age at risk of neuromotor delay
Valentín-Gudiol, M., Mattern-Baxter, K., Farrés, M. G., Calafat, C. B., Hadders‐Algra, M., & Angulo-Barroso, R. M. (2017) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd009242.pub3 · Cited by 45 · see citing works
Finch‐Edmondson, M., Morgan, C., Hunt, R. W., & Novak, I. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00015 · Cited by 47 · see citing works
Dursun, N., Gokbel, T., Akarsu, M., & Dursun, E. (2016) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0000000000000627 · Cited by 43 · see citing works
Tesson, S., Butow, P. N., Marshall, K. H., Fonagy, P., & Kasparian, N. A. (2021) · Health Psychology Review · doi:10.1080/17437199.2021.1927136 · Cited by 43 · see citing works
Low birth weight, family income and paternal absence as risk factors in neuropsychomotor development
de Araújo, L. B., Mélo, T. R., & Israel, V. L. (2017) · Journal of Human Growth and Development · doi:10.7322/jhgd.124072 · Cited by 44 · see citing works
GEARing smart environments for pediatric motor rehabilitation
Kokkoni, E., Mavroudi, E., Zehfroosh, A., Galloway, J. C., Vidal, R., Heinz, J., & Tanner, H. (2020) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-020-0647-0 · Cited by 39 · see citing works
Estevez, K. J. N., Rondón-Ortiz, A. N., Nguyen, J., & Kentner, A. C. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.08.192 · Cited by 39 · see citing works
A Randomized Trial of Baby Triple P for Preterm Infants: Child Outcomes at 2 Years of Corrected Age
Colditz, P. B., Boyd, R. N., Winter, L., Pritchard, M. A., Gray, P. H., Whittingham, K., O'Callaghan, M. J., Jardine, L. A., O'Rourke, P. K., Marquart, L., et al. (2019) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2019.01.024 · Cited by 37 · see citing works
Perinatal arterial ischemic stroke
Martínez-Biarge, M., Ferriero, D. M., & Cowan, F. M. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64029-1.00011-4 · Cited by 36 · see citing works
Sgandurra, G., Bartalena, L., Cioni, G., Greisen, G. O., Herskind, A., Inguaggiato, E., Lorentzen, J., Nielsen, J. B., & Sicola, E. (2014) · BMC Pediatrics · doi:10.1186/1471-2431-14-268 · Cited by 35 · see citing works
Khalil, M. H. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1368411 · Cited by 33 · see citing works
Providing a Primary Care Medical Home for Children and Youth With Cerebral Palsy
Noritz, G. H., Davidson, L. F., Steingass, K. J., Noritz, G. H., Agrawal, R., Ellerbeck, K. A., Foster, J. E. A., Fremion, E., Frierson, S. L., Leppert, M. L. O., et al. (2022) · PEDIATRICS · doi:10.1542/peds.2022-060055 · Cited by 32 · see citing works
Early detection of general movements trajectories in very low birth weight infants
Porro, M., Fontana, C., Giannì, M. L., Pesenti, N., Boggini, T., Carli, A. D., Bon, G. D., Lucco, G., Mosca, F., Fumagalli, M., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-70003-3 · Cited by 32 · see citing works
Santos-Pinto, C. D. B., Soares, D. D. A., Ferrari, F. P., Ajalla, M. E. A., Venancio, F. A., da Rosa, T. S., & de Oliveira, E. F. (2020) · BMC Public Health · doi:10.1186/s12889-020-08880-6 · Cited by 31 · see citing works
Calder, S. D., Ward, R., Jones, M., Johnston, J., & Claessen, M. (2017) · Disability and Rehabilitation · doi:10.1080/09638288.2017.1353144 · Cited by 30 · see citing works
Polizzi, C., Perricone, G., Morales, M. R., & Burgio, S. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18168670 · Cited by 28 · see citing works
Sgandurra, G., Beani, E., Giampietri, M., Rizzi, R., & Cioni, G. (2018) · BMC Pediatrics · doi:10.1186/s12887-018-1264-y · Cited by 27 · see citing works
Tallon, M. M., Kendall, G. E., Priddis, L. E., Newall, F. H., & Young, J. (2017) · Journal of Pediatric Nursing · doi:10.1016/j.pedn.2017.06.009 · Cited by 27 · see citing works
Peyton, C., Sukal‐Moulton, T., Carroll, A. J., Anderson, E. L., Brozek, A., Davis, M. M., Horowitz, J., Jayaraman, A., O’Brien, M. K., Patrick, C., et al. (2022) · Frontiers in Pediatrics · doi:10.3389/fped.2021.787196 · Cited by 26 · see citing works
Woolfenden, S. R., Farrar, M. A., Eapen, V., Masi, A., Wakefield, C. E., Badawi, N. A., Novak, I., Nassar, N., Lingam, R., & Dale, R. C. (2022) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.15289 · Cited by 28 · see citing works
Testing Seefeldt’s Proficiency Barrier: A Longitudinal Study
Garbeloto, F., Pacheco, M. M., Stodden, D. F., Tani, G., & Maia, J. A. R. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19127184 · Cited by 30 · see citing works
Tann, C. J., Kohli-Lynch, M., Nalugya, R., Sadoo, S., Martin, K., Lassman, R., Nanyunja, C., Musoke, M., Sewagaba, M., Nampijja, M., et al. (2021) · Infants & Young Children · doi:10.1097/iyc.0000000000000182 · Cited by 24 · see citing works
Apaydın, U., Yıldız, R., Yıldız, A., Acar, Ş. S., Gücüyener, K., & Elbasan, B. (2023) · Brain and Behavior · doi:10.1002/brb3.3199 · Cited by 24 · see citing works
CareToy: Stimulation and Assessment of Preterm Infant’s Activity Using a Novel Sensorized System
Rihar, A., Sgandurra, G., Beani, E., Cecchi, F., Pašič, J., Cioni, G., Dario, P., Mihelj, M., & Munih, M. (2016) · Annals of Biomedical Engineering · doi:10.1007/s10439-016-1669-4 · Cited by 24 · see citing works
Early Intervention Therapy Services for Infants With or at Risk for Cerebral Palsy
Gmmash, A., & Effgen, S. K. (2019) · Pediatric Physical Therapy · doi:10.1097/pep.0000000000000619 · Cited by 23 · see citing works
Whittingham, K., Sheffield, J., & Boyd, R. N. (2016) · BMJ Open · doi:10.1136/bmjopen-2016-012807 · Cited by 22 · see citing works
Liu, H.-Y., Guo, J., Zeng, C., Cao, Y., Ran, R., Wu, T., Yang, G., Zhao, D., Yang, P., Yu, X. B., et al. (2022) · Frontiers in Pediatrics · doi:10.3389/fped.2021.793561 · Cited by 22 · see citing works
Ferre, C. L., & Gordon, A. M. (2017) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13497 · Cited by 22 · see citing works
Daily Intervention for Young Children With Cerebral Palsy in GMFCS Level V
Heathcock, J., Baranet, K., Ferrante, R., & Hendershot, S. (2015) · Pediatric Physical Therapy · doi:10.1097/pep.0000000000000149 · Cited by 21 · see citing works
The Role of the Neurointensive Care Nursery for Neonatal Encephalopathy
Glass, H. C., & Rowitch, D. H. (2016) · Clinics in Perinatology · doi:10.1016/j.clp.2016.04.011 · Cited by 20 · see citing works
Beani, E., Menici, V., Cecchi, A., Cioni, M. L., Giampietri, M., Rizzi, R., Sgandurra, G., & Cioni, G. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.601137 · Cited by 19 · see citing works
Zhang, Y., Li, R., Miao, X., Cheng, L. J., & Lau, Y. (2021) · Gait & Posture · doi:10.1016/j.gaitpost.2021.10.046 · Cited by 18 · see citing works
Efficacy of Therapist Supported Interventions from the Neonatal Intensive Care Unit to Home
McCarty, D. B., Letzkus, L., Attridge, E., & Dusing, S. C. (2023) · Clinics in Perinatology · doi:10.1016/j.clp.2022.10.004 · Cited by 19 · see citing works
Ward, R., Reynolds, J. E., Bear, N., Elliott, C. M., & Valentine, J. P. (2016) · Disability and Rehabilitation · doi:10.3109/09638288.2016.1153162 · Cited by 19 · see citing works
Brandão, M. B., Frota, L. M. D. C. P., Miranda, J. L., Brasil, R. M. C., & Mancini, M. C. (2019) · Physical & Occupational Therapy In Pediatrics · doi:10.1080/01942638.2019.1600100 · Cited by 19 · see citing works
Qian, G., Cai, X., Xu, K., Tian, H., Meng, Q., Ossowski, Z. M., & Liang, J. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2022.1005485 · Cited by 20 · see citing works
The effects of acrobatic exercise on brain plasticity: a systematic review of animal studies
Gutierrez, R. M. S., Ricci, N. A., Gomes, Q. R. S., de Oliveira, D. L., & Pires, R. S. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1631-3 · Cited by 18 · see citing works
Eliasson, A., Holmström, L., Aarne, P., von Mentzer, C. N., Weiland, A.-L., Sjöstrand, L., Forssberg, H., Tedroff, K., & Löwing, K. (2016) · BMC Pediatrics · doi:10.1186/s12887-016-0711-x · Cited by 18 · see citing works
Cameron, K. L., Coulston, F., Kwong, A., Whittingham, K., Morgan, C., Boyd, R. N., Crowle, C., Sakakini, H., & Spittle, A. J. (2024) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.16190 · Cited by 17 · see citing works
Research Foundations for Evidence-Informed Early Childhood Intervention Performance Checklists
Dunst, C. J. (2017) · Education Sciences · doi:10.3390/educsci7040078 · Cited by 17 · see citing works
Provenzi, L., Grumi, S., Rinaldi, E., & Giusti, L. (2021) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2021.104048 · Cited by 19 · see citing works
Cecchi, F., Sgandurra, G., Mihelj, M., Mici, L., Zhang, J., Munih, M., Cioni, G., Laschi, C., & Dario, P. (2016) · IEEE Robotics & Automation Magazine · doi:10.1109/mra.2015.2506058 · Cited by 16 · see citing works
Early Intervention for Children with Cerebral Palsy
Spittle, A. J., & Morgan, C. (2017) · Springer eBooks · doi:10.1007/978-3-319-67858-0_18 · Cited by 16 · see citing works
Effects of creative dance-based exercise on gait performance in adolescents with cerebral palsy
Joung, H. J., Park, J., Ahn, J., Park, M. S., & Lee, Y. (2020) · Journal of Exercise Rehabilitation · doi:10.12965/jer.2040384.192 · Cited by 16 · see citing works
Julien, L., Moreau-Pernet, G., Rochette, E., Lemaire, J., Pontier, B., Bourrand, S., Pereira, B., Chassain, C., Sontheimer, A., & Sarret, C. (2024) · Pediatric Research · doi:10.1038/s41390-024-03240-1 · Cited by 15 · see citing works
Hip problems in cerebral palsy
Yıldız, C., & Demirkale, İ. (2013) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000040 · Cited by 15 · see citing works
Deng, W., Anastasopoulos, S., deRegnier, R.-A. O., Pouppirt, N. R., Barlow, A. K., Patrick, C., O’Brien, M. K., Babula, S., Sukal‐Moulton, T., Peyton, C., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0291408 · Cited by 14 · see citing works
Han, Y., Shen, X.-Y., Gao, Z.-K., Han, P., & Bi, X. (2024) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2024.110912 · Cited by 14 · see citing works
Narrative Review of the Theoretical–Methodological Foundations of the TREINI Program
Loffi, R. G., Souto, D. O., Cruz, T. K. F., de Lima, A. F. B., Costa, F. R. M., Barreto, S. R., SANTANA, P. C. M., Nascimento, A. A. A. C., & Haase, V. G. (2024) · Children · doi:10.3390/children11101181 · Cited by 15 · see citing works
Durán-Carabali, L. E., Odorcyk, F. K., Sanches, E. F., de Mattos, M. M., Anschau, F., & Netto, C. A. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02730-9 · Cited by 14 · see citing works
Interventions for Motor Disorders in High-Risk Neonates
McNamara, L., Morgan, C., & Novak, I. (2023) · Clinics in Perinatology · doi:10.1016/j.clp.2022.11.002 · Cited by 13 · see citing works
Exergaming for dementia and mild cognitive impairment
Voinescu, A., Papaioannou, T., Petrini, K., & Fraser, D. S. (2024) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013853.pub2 · Cited by 13 · see citing works
Poggioli, M., Minichilli, F., Bononi, T., Meghi, P., André, P., Crecchi, A., Rossi, B., Carboncini, M. C., Ottolini, A., & Bonfiglio, L. (2016) · Neural Plasticity · doi:10.1155/2016/4323792 · Cited by 13 · see citing works
Saussez, G., Laethem, M. V., & Bleyenheuft, Y. (2018) · Journal of Child Neurology · doi:10.1177/0883073817753291 · Cited by 13 · see citing works
de Oliveira, G. R., & Vidal, M. F. (2020) · Clinical Case Reports · doi:10.1002/ccr3.2860 · Cited by 13 · see citing works
Decoding the aquatic motor behavior: description and reflection on the functional movement
Iucksch, D. D., de Araújo, L. B., Novakoski, K. R. M., Yamaguchi, B., Carneiro, C. F., Mélo, T. R., & Israel, V. L. (2020) · Acta Scientiarum Health Sciences · doi:10.4025/actascihealthsci.v42i1.47129 · Cited by 13 · see citing works
- Authors
- Morgan, C., Novak, I., & Badawi, N.
- Affiliations
- Cerebral Palsy Alliance (AU)
- The University of Sydney (AU)
- Venue
- PEDIATRICS
- Publisher
- American Academy of Pediatrics (AAP)
- Published
- 2013-09-01
- Volume
- 132
- Issue
- 3
- Pages
- e735-e746
- ISSN
- 0031-4005 (ISSN-L)
- 1098-4275
- OpenAlex
- W2059028608
- Cited by
- 207
- References
- 58
- Citations by year
- 2026: 14 · 2025: 15 · 2024: 23 · 2023: 15 · 2022: 22 · 2021: 21 · 2020: 15 · 2019: 19 · 2018: 12 · 2017: 15 · 2016: 19 · 2015: 6 · 2014: 9 · 2013: 1
- FWCI
- 1.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- PEDIATRICS (publishedVersion)
- PubMed (publishedVersion)
- ResearchOnline@ND (The University of Notre Dame) (submittedVersion)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Cerebral Palsy and Movement Disorders
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Infant Development and Preterm Care
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- environmental enrichment, cerebral palsy, motor outcome, neuroplasticity, motor development, early intervention, brain injury recovery
- MeSH terms
- Brain, Cerebral Palsy, Child, Preschool, Cognition Disorders, Education, Female, Humans, Infant, Male, Neuronal Plasticity, Psychomotor Disorders, Social Environment, Randomized Controlled Trials as Topic, Treatment Outcome, Physical Therapy Modalities, Mobility Limitation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review