Neuroprotective therapies in the NICU in preterm infants: present and future (Neonatal Neurocritical Care Series).
Journal
Pediatric research
ISSN: 1530-0447
Titre abrégé: Pediatr Res
Pays: United States
ID NLM: 0100714
Informations de publication
Date de publication:
19 Dec 2023
19 Dec 2023
Historique:
received:
06
07
2023
accepted:
26
10
2023
revised:
19
10
2023
medline:
20
12
2023
pubmed:
20
12
2023
entrez:
19
12
2023
Statut:
aheadofprint
Résumé
The survival of preterm infants has steadily improved thanks to advances in perinatal and neonatal intensive clinical care. The focus is now on finding ways to improve morbidities, especially neurological outcomes. Although antenatal steroids and magnesium for preterm infants have become routine therapies, studies have mainly demonstrated short-term benefits for antenatal steroid therapy but limited evidence for impact on long-term neurodevelopmental outcomes. Further advances in neuroprotective and neurorestorative therapies, improved neuromonitoring modalities to optimize recruitment in trials, and improved biomarkers to assess the response to treatment are essential. Among the most promising agents, multipotential stem cells, immunomodulation, and anti-inflammatory therapies can improve neural outcomes in preclinical studies and are the subject of considerable ongoing research. In the meantime, bundles of care protecting and nurturing the brain in the neonatal intensive care unit and beyond should be widely implemented in an effort to limit injury and promote neuroplasticity. IMPACT: With improved survival of preterm infants due to improved antenatal and neonatal care, our focus must now be to improve long-term neurological and neurodevelopmental outcomes. This review details the multifactorial pathogenesis of preterm brain injury and neuroprotective strategies in use at present, including antenatal care, seizure management and non-pharmacological NICU care. We discuss treatment strategies that are being evaluated as potential interventions to improve the neurodevelopmental outcomes of infants born prematurely.
Identifiants
pubmed: 38114609
doi: 10.1038/s41390-023-02895-6
pii: 10.1038/s41390-023-02895-6
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Investigateurs
Sonia Lomeli Bonifacio
(SL)
Pia Wintermark
(P)
Hany Aly
(H)
Vann Chau
(V)
Hannah Glass
(H)
Monica Lemmon
(M)
Courtney Wusthoff
(C)
Gabrielle deVeber
(G)
Andrea Pardo
(A)
Melisa Carrasco
(M)
James Boardman
(J)
Dawn Gano
(D)
Eric Peeples
(E)
Informations de copyright
© 2023. The Author(s).
Références
Manuck, T. A. et al. Preterm neonatal morbidity and mortality by gestational age: a contemporary cohort. Am. J. Obstet. Gynecol. 215, 103.e101–103.e114 (2016).
doi: 10.1016/j.ajog.2016.01.004
Chawanpaiboon, S. et al. Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob. Health 7, e37–e46 (2019).
pubmed: 30389451
doi: 10.1016/S2214-109X(18)30451-0
Sarda, S. P., Sarri, G. & Siffel, C. Global prevalence of long-term neurodevelopmental impairment following extremely preterm birth: a systematic literature review. J. Int. Med. Res. 49, 3000605211028026 (2021).
pubmed: 34284680
doi: 10.1177/03000605211028026
Harrison, M. S. & Goldenberg, R. L. Global burden of prematurity. Semin. Fetal Neonatal Med. 21, 74–79 (2016).
pubmed: 26740166
doi: 10.1016/j.siny.2015.12.007
GBD 2017 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392, 1789–1858 (2018).
doi: 10.1016/S0140-6736(18)32279-7
Doyle, L. W., Spittle, A., Anderson, P. J. & Cheong, J. L. Y. School-aged neurodevelopmental outcomes for children born extremely preterm. Arch. Dis. Child 106, 834–838 (2021).
pubmed: 34035035
doi: 10.1136/archdischild-2021-321668
Linsell, L. et al. Cognitive trajectories from infancy to early adulthood following birth before 26 weeks of gestation: a prospective, population-based cohort study. Arch. Dis. Child 103, 363–370 (2018).
pubmed: 29146572
doi: 10.1136/archdischild-2017-313414
Perrone, S. et al. Personality, emotional and cognitive functions in young adults born preterm. Brain Dev. 42, 713–719 (2020).
pubmed: 32653254
doi: 10.1016/j.braindev.2020.06.014
Crump, C. An overview of adult health outcomes after preterm birth. Early Hum. Dev. 150, 105187 (2020).
pubmed: 32948365
pmcid: 7480736
doi: 10.1016/j.earlhumdev.2020.105187
Yates, N., Gunn, A. J., Bennet, L., Dhillon, S. K. & Davidson, J. O. Preventing brain injury in the preterm infant-current controversies and potential therapies. Int. J. Mol. Sci. 22, 1671 (2021).
pubmed: 33562339
pmcid: 7915709
doi: 10.3390/ijms22041671
Ophelders, D. et al. Preterm brain injury, antenatal triggers, and therapeutics: timing is key. Cells 9, 1871 (2020).
pubmed: 32785181
pmcid: 7464163
doi: 10.3390/cells9081871
Hagberg, H. et al. The role of inflammation in perinatal brain injury. Nat. Rev. Neurol. 11, 192–208 (2015).
pubmed: 25686754
pmcid: 4664161
doi: 10.1038/nrneurol.2015.13
Galinsky, R. et al. Complex interactions between hypoxia-ischemia and inflammation in preterm brain injury. Dev. Med. Child Neurol. 60, 126–133 (2018).
pubmed: 29194585
doi: 10.1111/dmcn.13629
Dean, J. M. et al. What brakes the preterm brain? An arresting story. Pediatr. Res. 75, 227–233 (2014).
pubmed: 24336432
doi: 10.1038/pr.2013.189
Kuban, K. C. et al. The breadth and type of systemic inflammation and the risk of adverse neurological outcomes in extremely low gestation newborns. Pediatr. Neurol. 52, 42–48 (2015).
pubmed: 25459361
doi: 10.1016/j.pediatrneurol.2014.10.005
Back, S. A. White Matter injury in the preterm infant: pathology and mechanisms. Acta Neuropathol. 134, 331–349 (2017).
pubmed: 28534077
pmcid: 5973818
doi: 10.1007/s00401-017-1718-6
Schneider, J. & Miller, S. P. Preterm Brain injury: white matter injury. Handb. Clin. Neurol. 162, 155–172 (2019).
pubmed: 31324309
doi: 10.1016/B978-0-444-64029-1.00007-2
Verney, C. et al. Microglial reaction in axonal crossroads is a hallmark of noncystic periventricular white matter injury in very preterm infants. J. Neuropathol. Exp. Neurol. 71, 251–264 (2012).
pubmed: 22318128
doi: 10.1097/NEN.0b013e3182496429
Kennedy, E., Poppe, T., Tottman, A. & Harding, J. Neurodevelopmental impairment is associated with altered white matter development in a cohort of school-aged children born very preterm. Neuroimage Clin. 31, 102730 (2021).
pubmed: 34174689
pmcid: 8246637
doi: 10.1016/j.nicl.2021.102730
Fleiss, B. & Gressens, P. Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsy? Lancet Neurol. 11, 556–566 (2012).
pubmed: 22608669
doi: 10.1016/S1474-4422(12)70058-3
Chakkarapani, A. A. et al. Therapies for neonatal encephalopathy: targeting the latent, secondary and tertiary phases of evolving brain injury. Semin. Fetal Neonatal Med. 26, 101256 (2021).
pubmed: 34154945
doi: 10.1016/j.siny.2021.101256
Fleiss, B., Murray, D. M., Bjorkman, S. T. & Wixey, J. A. Editorial: Pathomechanisms and treatments to protect the preterm, fetal growth restricted and neonatal encephalopathic brain. Front. Neurol. 12, 755617 (2021).
pubmed: 34566880
pmcid: 8458730
doi: 10.3389/fneur.2021.755617
Cheong, J. L., Spittle, A. J., Burnett, A. C., Anderson, P. J. & Doyle, L. W. Have outcomes following extremely preterm birth improved over time? Semin. Fetal Neonatal Med. 25, 101114 (2020).
pubmed: 32451304
doi: 10.1016/j.siny.2020.101114
Australian Cerebral Palsy Register. Report of the Australian Cerebral Palsy Register, Birth Years 1995–2016. https://cpregister.com/ (2023).
Cheong, J. L. Y. et al. Temporal trends in neurodevelopmental outcomes to 2 years after extremely preterm birth. JAMA Pediatr. 175, 1035–1042 (2021).
pubmed: 34279561
doi: 10.1001/jamapediatrics.2021.2052
Banker, B. Q. & Larroche, J. C. Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. Arch. Neurol. 7, 386–410 (1962).
pubmed: 13966380
doi: 10.1001/archneur.1962.04210050022004
Hamrick, S. E. et al. Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. J. Pediatr. 145, 593–599 (2004).
pubmed: 15520756
doi: 10.1016/j.jpeds.2004.05.042
Gano, D. et al. Diminished white matter injury over time in a cohort of premature newborns. J. Pediatr. 166, 39–43 (2015).
pubmed: 25311709
doi: 10.1016/j.jpeds.2014.09.009
Wassink, G. et al. A working model for hypothermic neuroprotection. J. Physiol. 596, 5641–5654 (2018).
pubmed: 29660115
pmcid: 6265568
doi: 10.1113/JP274928
Lear, B. A. et al. Tertiary cystic white matter injury as a potential phenomenon after hypoxia-ischaemia in preterm f sheep. Brain Commun. 3, fcab024 (2021).
pubmed: 33937767
pmcid: 8072523
doi: 10.1093/braincomms/fcab024
Pierrat, V. et al. Ultrasound diagnosis and neurodevelopmental outcome of localised and extensive cystic periventricular leucomalacia. Arch. Dis. Child Fetal Neonatal Ed. 84, F151–F156 (2001).
pubmed: 11320039
pmcid: 1721251
doi: 10.1136/fn.84.3.F151
Sarkar, S. et al. Outcome of preterm infants with transient cystic periventricular leukomalacia on serial cranial imaging up to term equivalent age. J. Pediatr. 195, 59–65.e53 (2018).
pubmed: 29398046
pmcid: 6407628
doi: 10.1016/j.jpeds.2017.12.010
Lear, B. A. et al. Is late prevention of cerebral palsy in extremely preterm infants plausible? Dev. Neurosci. 44, 177–185 (2021).
Vinukonda, G. et al. Effect of prenatal glucocorticoids on cerebral vasculature of the developing brain. Stroke 41, 1766–1773 (2010).
pubmed: 20616316
pmcid: 2920046
doi: 10.1161/STROKEAHA.110.588400
Carson, R., Monaghan-Nichols, A. P., DeFranco, D. B. & Rudine, A. C. Effects of antenatal glucocorticoids on the developing brain. Steroids 114, 25–32 (2016).
pubmed: 27343976
pmcid: 5052110
doi: 10.1016/j.steroids.2016.05.012
Stock, S. J., Thomson, A. J. & Papworth, S. Antenatal corticosteroids to reduce neonatal morbidity and mortality: Green-top Guideline No. 74. BJOG 129, e35–e60 (2022).
pubmed: 35172391
doi: 10.1111/1471-0528.17027
Committee on Obstetric Practice. Committee Opinion No. 713: Antenatal corticosteroid therapy for fetal maturation. Obstet. Gynecol. 130, e102–e109 (2017).
doi: 10.1097/AOG.0000000000002237
World Health Organization. WHO Recommendations on Antenatal Corticosteroids for Improving Preterm Birth Outcomes (World Health Organization, 2022).
Cahill, A. G., Kaimal, A. J., Kuller, J. A. & Turrentine, M. A. Use of antenatal corticosteroids at 22 weeks of gestation. American College of Obstetricians and Gynecologists, Society for Maternal-Fetal Medicine Accessed 14/12/23 https://www.bing.com/ck/a?!&&p=30a56bad003914b7JmltdHM9MTcwMjUxMjAwMCZpZ3VpZD0wZWIzY2VlOC1jNWQ0LTZmM2ItM2ZhYi1kZWI5YzQ3ZjZlMmEmaW5zaWQ9NTE3OQ&ptn=3&ver=2&hsh=3&fclid=0eb3cee8-c5d4-6f3b-3fab-deb9c47f6e2a&psq=antenatal+steroids+at+22+weeks+COG&u=a1aHR0cHM6Ly93d3cuYWNvZy5vcmcvY2xpbmljYWwvY2xpbmljYWwtZ3VpZGFuY2UvcHJhY3RpY2UtYWR2aXNvcnkvYXJ0aWNsZXMvMjAyMS8wOS91c2Utb2YtYW50ZW5hdGFsLWNvcnRpY29zdGVyb2lkcy1hdC0yMi13ZWVrcy1vZi1nZXN0YXRpb24&ntb=1 (2022).
McGoldrick, E., Stewart, F., Parker, R. & Dalziel, S. R. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst. Rev. 12, Cd004454 (2020).
pubmed: 33368142
Gyamfi-Bannerman, C. et al. Antenatal betamethasone for women at risk for late preterm delivery. N. Engl. J. Med. 374, 1311–1320 (2016).
pubmed: 26842679
pmcid: 4823164
doi: 10.1056/NEJMoa1516783
Räikkönen, K., Gissler, M. & Kajantie, E. Associations between maternal antenatal corticosteroid treatment and mental and behavioral disorders in children. JAMA 323, 1924–1933 (2020).
pubmed: 32427304
doi: 10.1001/jama.2020.3937
Räikkönen, K., Gissler, M., Tapiainen, T. & Kajantie, E. Associations between maternal antenatal corticosteroid treatment and psychological developmental and neurosensory disorders in children. JAMA Netw. Open 5, e2228518 (2022).
pubmed: 36001315
pmcid: 9403777
doi: 10.1001/jamanetworkopen.2022.28518
Doyle, L. W., Cheong, J. L., Hay, S., Manley, B. J. & Halliday, H. L. Late (≥7 days) systemic postnatal corticosteroids for prevention of bronchopulmonary dysplasia in preterm infants. Cochrane Database Syst. Rev. 11, Cd001145 (2021).
pubmed: 34758507
Ramaswamy, V. V. et al. Assessment of postnatal corticosteroids for the prevention of bronchopulmonary dysplasia in preterm neonates: a systematic review and network meta-analysis. JAMA Pediatr. 175, e206826 (2021).
pubmed: 33720274
pmcid: 7961472
doi: 10.1001/jamapediatrics.2020.6826
Doyle, L. W. & Anderson, P. J. Long-term outcomes of bronchopulmonary dysplasia. Semin. Fetal Neonatal Med. 14, 391–395 (2009).
pubmed: 19766550
doi: 10.1016/j.siny.2009.08.004
Rademaker, K. J., Groenendaal, F., van Bel, F., de Vries, L. S. & Uiterwaal, C. S. The DART study of low-dose dexamethasone therapy. Pediatrics 120, 689–690 (2007).
pubmed: 17766548
doi: 10.1542/peds.2007-1646
Doyle, L. W., Davis, P. G., Morley, C. J., McPhee, A. & Carlin, J. B. Outcome at 2 years of age of infants from the DART study: a multicenter, international, randomized, controlled trial of low-dose dexamethasone. Pediatrics 119, 716–721 (2007).
pubmed: 17403842
doi: 10.1542/peds.2006-2806
Koome, M. E. et al. Antenatal dexamethasone after asphyxia increases neural injury in preterm fetal sheep. PLoS ONE 8, e77480 (2013).
pubmed: 24204840
pmcid: 3799621
doi: 10.1371/journal.pone.0077480
Lear, C. A. et al. The effects of dexamethasone on post-asphyxial cerebral oxygenation in the preterm fetal sheep. J. Physiol. 592, 5493–5505 (2014).
pubmed: 25384775
pmcid: 4270508
doi: 10.1113/jphysiol.2014.281253
Doyle, L. W., Crowther, C. A., Middleton, P., Marret, S. & Rouse, D. Magnesium sulphate for women at risk of preterm birth for neuroprotection of the fetus. Cochrane Database Syst. Rev. 18, Cd004661 (2009).
Crowther, C. A. et al. Assessing the neuroprotective benefits for babies of antenatal magnesium sulphate: an individual participant data meta-analysis. PLoS Med. 14, e1002398 (2017).
pubmed: 28976987
pmcid: 5627896
doi: 10.1371/journal.pmed.1002398
Wolf, H. T. et al. Magnesium sulphate for fetal neuroprotection at imminent risk for preterm delivery: a systematic review with meta-analysis and trial sequential analysis. BJOG 127, 1180–1188 (2020).
pubmed: 32237069
doi: 10.1111/1471-0528.16238
Rattray, B. N. et al. Antenatal magnesium sulfate and spontaneous intestinal perforation in infants less than 25 weeks gestation. J. Perinatol. 34, 819–822 (2014).
pubmed: 24901451
doi: 10.1038/jp.2014.106
Kamyar, M., Clark, E. A., Yoder, B. A., Varner, M. W. & Manuck, T. A. Antenatal magnesium sulfate, necrotizing enterocolitis, and death among neonates < 28 weeks gestation. AJP Rep. 6, e148–e154 (2016).
pubmed: 27054046
pmcid: 4816636
doi: 10.1055/s-0036-1581059
Sung, S. I. et al. Increased risk of meconium-related ileus in extremely premature infants exposed to antenatal magnesium sulfate. Neonatology 119, 68–76 (2022).
pubmed: 35016173
doi: 10.1159/000520452
Prasath, A., Aronoff, N., Chandrasekharan, P. & Diggikar, S. Antenatal magnesium sulfate and adverse gastrointestinal outcomes in preterm infants-a systematic review and meta-analysis. J. Perinatol. 43, 1087–1100 (2023).
pubmed: 37391507
doi: 10.1038/s41372-023-01710-8
Macones, G. A. MgSO
pubmed: 19482111
doi: 10.1016/j.ajog.2009.04.036
Crowther, C. A. et al. Prenatal intravenous magnesium at 30–34 weeks’ gestation and neurodevelopmental outcomes in offspring: the MAGENTA randomized clinical trial. JAMA 330, 603–614 (2023).
pubmed: 37581672
doi: 10.1001/jama.2023.12357
Doyle, L. W., Anderson, P. J., Haslam, R., Lee, K. J. & Crowther, C. School-age outcomes of very preterm infants after antenatal treatment with magnesium sulfate vs placebo. JAMA 312, 1105–1113 (2014).
pubmed: 25226476
doi: 10.1001/jama.2014.11189
Chollat, C. et al. School-age outcomes following a randomized controlled trial of magnesium sulfate for neuroprotection of preterm infants. J. Pediatr. 165, 398–400.e393 (2014).
pubmed: 24837863
doi: 10.1016/j.jpeds.2014.04.007
Galinsky, R. et al. A systematic review of magnesium sulfate for perinatal neuroprotection: what have we learnt from the past decade? Front. Neurol. 11, 449 (2020).
pubmed: 32536903
pmcid: 7267212
doi: 10.3389/fneur.2020.00449
Koning, G. et al. Magnesium induces preconditioning of the neonatal brain via profound mitochondrial protection. J. Cereb. Blood Flow Metab. 39, 1038–1055 (2019).
pubmed: 29206066
doi: 10.1177/0271678X17746132
Lingam, I. et al. Short-term effects of early initiation of magnesium infusion combined with cooling after hypoxia-ischemia in term piglets. Pediatr. Res. 86, 699–708 (2019).
pubmed: 31357208
doi: 10.1038/s41390-019-0511-8
Galinsky, R. et al. Magnesium sulphate reduces tertiary gliosis but does not improve eeg recovery or white or grey matter cell survival after asphyxia in preterm fetal sheep. J. Physiol. 601, 1999–2016 (2023).
pubmed: 36999348
doi: 10.1113/JP284381
Gunn, A. J., Gunn, T. R., de Haan, H. H., Williams, C. E. & Gluckman, P. D. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal lambs. J. Clin. Invest. 99, 248–256 (1997).
pubmed: 9005993
pmcid: 507792
doi: 10.1172/JCI119153
Jacobs, S. E. et al. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst. Rev. 2013, Cd003311 (2013).
pubmed: 23440789
pmcid: 7003568
Shankaran, S. et al. Childhood outcomes after hypothermia for neonatal encephalopathy. N. Engl. J. Med. 366, 2085–2092 (2012).
pubmed: 22646631
pmcid: 3459579
doi: 10.1056/NEJMoa1112066
Azzopardi, D. et al. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N. Engl. J. Med. 371, 140–149 (2014).
pubmed: 25006720
doi: 10.1056/NEJMoa1315788
Gunn, A. J. & Bennet, L. Brain cooling for preterm infants. Clin. Perinatol. 35, 735–748 (2008).
pubmed: 19026337
doi: 10.1016/j.clp.2008.07.012
Smit, E., Liu, X., Jary, S., Cowan, F. & Thoresen, M. Cooling neonates who do not fulfil the standard cooling criteria—short- and long-term outcomes. Acta Paediatr. 104, 138–145 (2015).
pubmed: 25164710
doi: 10.1111/apa.12784
Rao, R. et al. Safety and short-term outcomes of therapeutic hypothermia in preterm neonates 34–35 weeks gestational age with hypoxic-ischemic encephalopathy. J. Pediatr. 183, 37–42 (2017).
pubmed: 27979578
doi: 10.1016/j.jpeds.2016.11.019
Herrera, T. I. et al. Outcomes of preterm infants treated with hypothermia for hypoxic-ischemic encephalopathy. Early Hum. Dev. 125, 1–7 (2018).
pubmed: 30144709
doi: 10.1016/j.earlhumdev.2018.08.003
Barrett, R. D. et al. Destruction and reconstruction: hypoxia and the developing brain. Birth Defects Res. C Embryo Today 81, 163–176 (2007).
pubmed: 17963273
doi: 10.1002/bdrc.20095
Bennet, L. et al. The effect of cerebral hypothermia on white and grey matter injury induced by severe hypoxia in preterm fetal sheep. J. Physiol. 578, 491–506 (2007).
pubmed: 17095565
doi: 10.1113/jphysiol.2006.119602
Wassink, G. et al. Hypothermic neuroprotection is associated with recovery of spectral edge frequency after asphyxia in preterm fetal sheep. Stroke 46, 585–587 (2015).
pubmed: 25586829
doi: 10.1161/STROKEAHA.114.008484
Kuban, K. C. et al. Circulating inflammatory-associated proteins in the first month of life and cognitive impairment at age 10 years in children born extremely preterm. J. Pediatr. 180, 116–123.e111 (2017).
pubmed: 27788929
doi: 10.1016/j.jpeds.2016.09.054
Falck, M. et al. Hypothermic neuronal rescue from infection-sensitised hypoxic-ischaemic brain injury is pathogen dependent. Dev. Neurosci. 39, 238–247 (2017).
pubmed: 28407632
doi: 10.1159/000455838
Smith, M. J. et al. Neural stem cell treatment for perinatal brain injury: a systematic review and meta-analysis of preclinical studies. Stem Cells Transl. Med. 10, 1621–1636 (2021).
pubmed: 34542242
pmcid: 8641092
doi: 10.1002/sctm.21-0243
Penny, T. R. et al. Multiple doses of umbilical cord blood cells improve long-term brain injury in the neonatal rat. Brain Res. 1746, 147001 (2020).
pubmed: 32585139
doi: 10.1016/j.brainres.2020.147001
van Velthoven, C. T., Kavelaars, A., van Bel, F. & Heijnen, C. J. Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligodendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function. J. Neurosci. 30, 9603–9611 (2010).
pubmed: 20631189
pmcid: 6632441
doi: 10.1523/JNEUROSCI.1835-10.2010
Zhu, L. H. et al. Improvement of human umbilical cord mesenchymal stem cell transplantation on glial cell and behavioral function in a neonatal model of periventricular white matter damage. Brain Res. 1563, 13–21 (2014).
pubmed: 24680746
doi: 10.1016/j.brainres.2014.03.030
Davidson, J. O. et al. Window of opportunity for human amnion epithelial stem cells to attenuate astrogliosis after umbilical cord occlusion in preterm fetal sheep. Stem Cells Transl. Med. 10, 427–440 (2021).
pubmed: 33103374
doi: 10.1002/sctm.20-0314
van den Heuij, L. G. et al. Delayed intranasal infusion of human amnion epithelial cells improves white matter maturation after asphyxia in preterm fetal sheep. J. Cereb. Blood Flow Metab. 39, 223–239 (2019).
pubmed: 28895475
doi: 10.1177/0271678X17729954
Yawno, T. et al. Human amnion epithelial cells protect against white matter brain injury after repeated endotoxin exposure in the preterm ovine fetus. Cell Transpl. 26, 541–553 (2017).
doi: 10.3727/096368916X693572
Passera, S. et al. Therapeutic potential of stem cells for preterm infant brain damage: can we move from the heterogeneity of preclinical and clinical studies to established therapeutics? Biochem. Pharm. 186, 114461 (2021).
pubmed: 33571501
doi: 10.1016/j.bcp.2021.114461
Malhotra, A., Novak, I., Miller, S. L. & Jenkin, G. Autologous transplantation of umbilical cord blood-derived cells in extreme preterm infants: protocol for a safety and feasibility study. BMJ Open 10, e036065 (2020).
pubmed: 32398336
pmcid: 7223148
doi: 10.1136/bmjopen-2019-036065
Bennet, L. et al. Chronic inflammation and impaired development of the preterm brain. J. Reprod. Immunol. 125, 45–55 (2018).
pubmed: 29253793
doi: 10.1016/j.jri.2017.11.003
Huppi, P. S. et al. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107, 455–460 (2001).
pubmed: 11230582
doi: 10.1542/peds.107.3.455
Miller, S. L., Supramaniam, V. G., Jenkin, G., Walker, D. W. & Wallace, E. M. Cardiovascular responses to maternal betamethasone administration in the intrauterine growth-restricted ovine fetus. Am. J. Obstet. Gynecol. 201, 613 e611–613.e618 (2009).
doi: 10.1016/j.ajog.2009.07.028
Ment, L. R. et al. Longitudinal brain volume changes in preterm and term control subjects during late childhood and adolescence. Pediatrics 123, 503–511 (2009).
pubmed: 19171615
doi: 10.1542/peds.2008-0025
Ghotra, S., Vincer, M., Allen, V. M. & Khan, N. A population-based study of cystic white matter injury on ultrasound in very preterm infants born over two decades in Nova Scotia, Canada. J. Perinatol. 39, 269–277 (2019).
pubmed: 30552376
doi: 10.1038/s41372-018-0294-5
Northington, F. J. et al. Necrostatin decreases oxidative damage, inflammation, and injury after neonatal HI. J. Cereb. Blood Flow Metab. 31, 178–189 (2011).
pubmed: 20571523
doi: 10.1038/jcbfm.2010.72
Buser, J. R. et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 71, 93–109 (2012).
pubmed: 22275256
pmcid: 3270934
doi: 10.1002/ana.22627
Lear, C. A. et al. Tumour necrosis factor blockade after asphyxia in foetal sheep ameliorates cystic white matter injury. Brain 146, 1453–1466 (2023).
pubmed: 36087304
doi: 10.1093/brain/awac331
Green, E. A. et al. Anakinra Pilot—a clinical trial to demonstrate safety, feasibility and pharmacokinetics of interleukin 1 receptor antagonist in preterm infants. Front. Immunol. 13, 1022104 (2022).
pubmed: 36389766
pmcid: 9647081
doi: 10.3389/fimmu.2022.1022104
Wang, L., Zhang, Z., Wang, Y., Zhang, R. & Chopp, M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35, 1732–1737 (2004).
pubmed: 15178821
doi: 10.1161/01.STR.0000132196.49028.a4
Wallach, I. et al. Erythropoietin-receptor gene regulation in neuronal cells. Pediatr. Res. 65, 619–624 (2009).
pubmed: 19218878
doi: 10.1203/PDR.0b013e31819ea3b8
Sugawa, M., Sakurai, Y., Ishikawa-Ieda, Y., Suzuki, H. & Asou, H. Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci. Res. 44, 391–403 (2002).
pubmed: 12445627
doi: 10.1016/S0168-0102(02)00161-X
Nagai, A. et al. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J. Neuropathol. Exp. Neurol. 60, 386–392 (2001).
pubmed: 11305874
doi: 10.1093/jnen/60.4.386
Chong, Z. Z., Kang, J. Q. & Maiese, K. Erythropoietin fosters both intrinsic and extrinsic neuronal protection through modulation of microglia, Akt1, Bad, and caspase-mediated pathways. Br. J. Pharm. 138, 1107–1118 (2003).
doi: 10.1038/sj.bjp.0705161
Digicaylioglu, M. & Lipton, S. A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-κB signalling cascades. Nature 412, 641–647 (2001).
pubmed: 11493922
doi: 10.1038/35088074
Sun, Y., Calvert, J. W. & Zhang, J. H. Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke 36, 1672–1678 (2005).
pubmed: 16040592
doi: 10.1161/01.STR.0000173406.04891.8c
Juul, S. E. et al. Microarray analysis of high-dose recombinant erythropoietin treatment of unilateral brain injury in neonatal mouse hippocampus. Pediatr. Res. 65, 485–492 (2009).
pubmed: 19190543
doi: 10.1203/PDR.0b013e31819d90c8
Kumral, A. et al. Protective effects of erythropoietin against ethanol-induced apoptotic neurodegenaration and oxidative stress in the developing C57bl/6 mouse brain. Brain Res. Dev. Brain Res. 160, 146–156 (2005).
pubmed: 16236368
doi: 10.1016/j.devbrainres.2005.08.006
Chattopadhyay, A., Choudhury, T. D., Bandyopadhyay, D. & Datta, A. G. Protective effect of erythropoietin on the oxidative damage of erythrocyte membrane by hydroxyl radical. Biochem. Pharm. 59, 419–425 (2000).
pubmed: 10644050
doi: 10.1016/S0006-2952(99)00277-4
Gorio, A. et al. Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc. Natl Acad. Sci. USA 99, 9450–9455 (2002).
pubmed: 12082184
pmcid: 123161
doi: 10.1073/pnas.142287899
Villa, P. et al. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J. Exp. Med. 198, 971–975 (2003).
pubmed: 12975460
pmcid: 2194205
doi: 10.1084/jem.20021067
Sirén, A. L. et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc. Natl Acad. Sci. USA 98, 4044–4049 (2001).
pubmed: 11259643
pmcid: 31176
doi: 10.1073/pnas.051606598
Bian, X. X., Yuan, X. S. & Qi, C. P. Effect of recombinant human erythropoietin on serum S100b protein and interleukin-6 levels after traumatic brain injury in the rat. Neurol. Med. Chir. 50, 361–366 (2010).
doi: 10.2176/nmc.50.361
Yatsiv, I. et al. Erythropoietin is neuroprotective, improves functional recovery, and reduces neuronal apoptosis and inflammation in a rodent model of experimental closed head injury. FASEB J. 19, 1701–1703 (2005).
pubmed: 16099948
doi: 10.1096/fj.05-3907fje
Zacharias, R. et al. Dose-dependent effects of erythropoietin in propofol anesthetized neonatal rats. Brain Res. 1343, 14–19 (2010).
pubmed: 20452333
doi: 10.1016/j.brainres.2010.04.081
Kumral, A. et al. Erythropoietin increases glutathione peroxidase enzyme activity and decreases lipid peroxidation levels in hypoxic-ischemic brain injury in neonatal rats. Biol. Neonate 87, 15–18 (2005).
pubmed: 15334031
doi: 10.1159/000080490
Gonzalez, F. F. et al. Erythropoietin increases neurogenesis and oligodendrogliosis of subventricular zone precursor cells after neonatal stroke. Stroke 44, 753–758 (2013).
pubmed: 23391775
pmcid: 3689426
doi: 10.1161/STROKEAHA.111.000104
Kellert, B. A., McPherson, R. J. & Juul, S. E. A comparison of high-dose recombinant erythropoietin treatment regimens in brain-injured neonatal rats. Pediatr. Res. 61, 451–455 (2007).
pubmed: 17515870
doi: 10.1203/pdr.0b013e3180332cec
Gonzalez, F. F. et al. Erythropoietin sustains cognitive function and brain volume after neonatal stroke. Dev. Neurosci. 31, 403–411 (2009).
pubmed: 19672069
pmcid: 2820334
doi: 10.1159/000232558
Gonzalez, F. F. et al. Erythropoietin enhances long-term neuroprotection and neurogenesis in neonatal stroke. Dev. Neurosci. 29, 321–330 (2007).
pubmed: 17762200
doi: 10.1159/000105473
Demers, E. J., McPherson, R. J. & Juul, S. E. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr. Res. 58, 297–301 (2005).
pubmed: 16055937
doi: 10.1203/01.PDR.0000169971.64558.5A
McPherson, R. J., Demers, E. J. & Juul, S. E. Safety of high-dose recombinant erythropoietin in a neonatal rat model. Neonatology 91, 36–43 (2007).
pubmed: 17344650
doi: 10.1159/000096969
Iwai, M. et al. Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 41, 1032–1037 (2010).
pubmed: 20360553
pmcid: 2919308
doi: 10.1161/STROKEAHA.109.570325
Wassink, G. et al. Partial white and grey matter protection with prolonged infusion of recombinant human erythropoietin after asphyxia in preterm fetal sheep. J. Cereb. Blood Flow Metab. 37, 1080–1094 (2017).
pubmed: 27207167
doi: 10.1177/0271678X16650455
Dhillon, S. K. et al. Adverse neural effects of delayed, intermittent treatment with rEPO after asphyxia in preterm fetal sheep. J. Physiol. 599, 3593–3609 (2021).
pubmed: 34032286
doi: 10.1113/JP281269
Ohls, R. K. et al. Neurodevelopmental outcome and growth at 18 to 22 months’ corrected age in extremely low birth weight infants treated with early erythropoietin and iron. Pediatrics 114, 1287–1291 (2004).
pubmed: 15520109
doi: 10.1542/peds.2003-1129-L
Ohls, R. K. et al. Cognitive outcomes of preterm infants randomized to darbepoetin, erythropoietin, or placebo. Pediatrics 133, 1023–1030 (2014).
pubmed: 24819566
pmcid: 4531269
doi: 10.1542/peds.2013-4307
Natalucci, G. et al. Effect of early prophylactic high-dose recombinant human erythropoietin in very preterm infants on neurodevelopmental outcome at 2 years: a randomized clinical trial. JAMA 315, 2079–2085 (2016).
pubmed: 27187300
doi: 10.1001/jama.2016.5504
Song, J. et al. Recombinant human erythropoietin improves neurological outcomes in very preterm infants. Ann. Neurol. 80, 24–34 (2016).
pubmed: 27130143
pmcid: 5084793
doi: 10.1002/ana.24677
Juul, S. E. et al. A randomized trial of erythropoietin for neuroprotection in preterm infants. N. Engl. J. Med. 382, 233–243 (2020).
pubmed: 31940698
pmcid: 7060076
doi: 10.1056/NEJMoa1907423
Fischer, H. S., Reibel, N. J., Bührer, C. & Dame, C. Prophylactic early erythropoietin for neuroprotection in preterm infants: a meta-analysis. Pediatrics 139, e20164317 (2017).
Wood, T. R. et al. Early biomarkers of hypoxia and inflammation and two-year neurodevelopmental outcomes in the preterm erythropoietin neuroprotection (PENUT) trial. EBioMedicine 72, 103605 (2021).
pubmed: 34619638
pmcid: 8498235
doi: 10.1016/j.ebiom.2021.103605
Robertson, N. J. et al. Which neuroprotective agents are ready for bench to bedside translation in the newborn infant? J. Pediatr. 160, 544–552.e544 (2012).
pubmed: 22325255
pmcid: 4048707
doi: 10.1016/j.jpeds.2011.12.052
Drury, P. P. et al. Partial neural protection with prophylactic low-dose melatonin after asphyxia in preterm fetal sheep. J. Cereb. Blood Flow Metab. 34, 126–135 (2014).
pubmed: 24103904
doi: 10.1038/jcbfm.2013.174
Yawno, T. et al. The beneficial effects of melatonin administration following hypoxia-ischemia in preterm fetal sheep. Front. Cell Neurosci. 11, 296 (2017).
pubmed: 29018332
pmcid: 5615225
doi: 10.3389/fncel.2017.00296
Robertson, N. J. et al. High-dose melatonin and ethanol excipient combined with therapeutic hypothermia in a newborn piglet asphyxia model. Sci. Rep. 10, 3898 (2020).
pubmed: 32127612
pmcid: 7054316
doi: 10.1038/s41598-020-60858-x
Robertson, N. J. et al. Melatonin as an adjunct to therapeutic hypothermia in a piglet model of neonatal encephalopathy: a translational study. Neurobiol. Dis. 121, 240–251 (2019).
pubmed: 30300675
doi: 10.1016/j.nbd.2018.10.004
Ethanol in liquid preparations intended for children. Pediatrics 73, 405–407 (1984).
DeMuro, R. L., Nafziger, A. N., Blask, D. E., Menhinick, A. M. & Bertino, J. S. Jr. The absolute bioavailability of oral melatonin. J. Clin. Pharm. 40, 781–784 (2000).
doi: 10.1177/00912700022009422
El-Gendy, F. M., El-Hawy, M. A. & Hassan, M. G. Beneficial effect of melatonin in the treatment of neonatal sepsis. J. Matern. Fetal Neonatal Med. 31, 2299–2303 (2018).
pubmed: 28612668
doi: 10.1080/14767058.2017.1342794
Gitto, E. et al. Correlation among cytokines, bronchopulmonary dysplasia and modality of ventilation in preterm newborns: improvement with melatonin treatment. J. Pineal Res. 39, 287–293 (2005).
pubmed: 16150110
doi: 10.1111/j.1600-079X.2005.00251.x
Marseglia, L. et al. Antioxidant effect of melatonin in preterm newborns. Oxid. Med. Cell Longev. 2021, 6308255 (2021).
pubmed: 34840669
pmcid: 8626170
doi: 10.1155/2021/6308255
Coviello, C. et al. Isoprostanes as biomarker for white matter injury in extremely preterm infants. Front. Pediatr. 8, 618622 (2020).
pubmed: 33585368
doi: 10.3389/fped.2020.618622
Häusler, S. et al. Melatonin as a therapy for preterm brain injury: what is the evidence? Antioxidants 12, 1630 (2023).
Australian New Zealand Clinical Trials Registry (ANZCTR). Cognitive Improvement at 2 Years Corrected Postnatal Age through Early Restoration of Circadian Rhythms in Very Preterm Infants Via Environmental Modification from Birth until Discharge Home: The CIRCA DIEM Study. https://www.anzctr.org.au/Trial/Registration/TrialReview.aspx?id=374490 (ANZCTR, 2018).
Schmidt, B. et al. Caffeine therapy for apnea of prematurity. N. Engl. J. Med. 354, 2112–2121 (2006).
pubmed: 16707748
doi: 10.1056/NEJMoa054065
Henderson‐Smart, D. J. & De Paoli, A. G. Methylxanthine treatment for apnoea in preterm infants. Cochrane Database Syst. Rev. 8, CD000140 (2010).
Bruschettini, M. et al. Caffeine dosing regimens in preterm infants with or at risk for apnea of prematurity. Cochrane Database Syst. Rev. 4, CD013873 (2023).
Schmidt, B. et al. Long-term effects of caffeine therapy for apnea of prematurity. N. Engl. J. Med. 357, 1893–1902 (2007).
pubmed: 17989382
doi: 10.1056/NEJMoa073679
Schmidt, B. et al. Survival without disability to age 5 years after neonatal caffeine therapy for apnea of prematurity. JAMA 307, 275–282 (2012).
pubmed: 22253394
doi: 10.1001/jama.2011.2024
Mürner-Lavanchy, I. M. et al. Neurobehavioral outcomes 11 years after neonatal caffeine therapy for apnea of prematurity. Pediatrics 141, e20174047 (2018).
Schmidt, B. et al. Academic performance, motor function, and behavior 11 years after neonatal caffeine citrate therapy for apnea of prematurity: an 11-year follow-up of the CAP randomized clinical trial. JAMA Pediatr. 171, 564–572 (2017).
pubmed: 28437520
doi: 10.1001/jamapediatrics.2017.0238
Parikka, V. et al. The effect of caffeine citrate on neural breathing pattern in preterm infants. Early Hum. Dev. 91, 565–568 (2015).
pubmed: 26217936
doi: 10.1016/j.earlhumdev.2015.06.007
Back, S. A. et al. Protective effects of caffeine on chronic hypoxia-induced perinatal white matter injury. Ann. Neurol. 60, 696–705 (2006).
pubmed: 17044013
doi: 10.1002/ana.21008
McLeod, R. M., Rosenkrantz, T. S., Fitch, R. H. & Koski, R. R. Sex differences in microglia activation in a rodent model of preterm hypoxic ischemic injury with caffeine treatment. Biomedicines 11, 185 (2023).
Alexander, M., Smith, A. L., Rosenkrantz, T. S. & Fitch, R. H. Therapeutic effect of caffeine treatment immediately following neonatal hypoxic-ischemic injury on spatial memory in male rats. Brain Sci. 3, 177–190 (2013).
pubmed: 24961313
pmcid: 4061822
doi: 10.3390/brainsci3010177
Kilicdag, H., Daglioglu, Y. K., Erdogan, S. & Zorludemir, S. Effects of caffeine on neuronal apoptosis in neonatal hypoxic-ischemic brain injury. J. Matern. Fetal Neonatal Med. 27, 1470–1475 (2014).
pubmed: 24392823
doi: 10.3109/14767058.2013.878694
Ronen, G. M., Penney, S. & Andrews, W. The epidemiology of clinical neonatal seizures in Newfoundland: a population-based study. J. Pediatr. 134, 71–75 (1999).
pubmed: 9880452
doi: 10.1016/S0022-3476(99)70374-4
Glass, H. C. et al. Seizures in preterm neonates: a multicenter observational cohort study. Pediatr. Neurol. 72, 19–24 (2017).
pubmed: 28558955
pmcid: 5863228
doi: 10.1016/j.pediatrneurol.2017.04.016
Ronen, G. M., Buckley, D., Penney, S. & Streiner, D. L. Long-term prognosis in children with neonatal seizures: a population-based study. Neurology 69, 1816–1822 (2007).
pubmed: 17984448
doi: 10.1212/01.wnl.0000279335.85797.2c
Zhou, K. Q. et al. Treating seizures after hypoxic-ischemic encephalopathy—current controversies and future directions. Int. J. Mol. Sci. 22, 7121 (2021).
Galinsky, R. et al. Magnesium sulfate reduces eeg activity but is not neuroprotective after asphyxia in preterm fetal sheep. J. Cereb. Blood Flow Metab. 37, 1362–1373 (2017).
pubmed: 27317658
doi: 10.1177/0271678X16655548
Bittigau, P. et al. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc. Natl Acad. Sci. USA 99, 15089–15094 (2002).
pubmed: 12417760
pmcid: 137548
doi: 10.1073/pnas.222550499
Forcelli, P. A., Janssen, M. J., Vicini, S. & Gale, K. Neonatal exposure to antiepileptic drugs disrupts striatal synaptic development. Ann. Neurol. 72, 363–372 (2012).
pubmed: 22581672
pmcid: 3421036
doi: 10.1002/ana.23600
Browne, J. V., Jaeger, C. B. & Kenner, C. Executive summary: standards, competencies, and recommended best practices for infant- and family-centered developmental care in the intensive care unit. J. Perinatol. 40, 5–10 (2020).
pubmed: 32859958
doi: 10.1038/s41372-020-0767-1
WHO Immediate KMC Study Group. Impact of continuous kangaroo mother care initiated immediately after birth (iKMC) on survival of newborns with birth weight between 1.0 to < 1.8 kg: study protocol for a randomized controlled trial. Trials 21, 280 (2020).
doi: 10.1186/s13063-020-4101-1
Cho, E. S. et al. The effects of kangaroo care in the neonatal intensive care unit on the physiological functions of preterm infants, maternal-infant attachment, and maternal stress. J. Pediatr. Nurs. 31, 430–438 (2016).
pubmed: 26975461
doi: 10.1016/j.pedn.2016.02.007
Gonya, J., Ray, W. C., Rumpf, R. W. & Brock, G. Investigating skin-to-skin care patterns with extremely preterm infants in the NICU and their effect on early cognitive and communication performance: a retrospective cohort study. BMJ Open 7, e012985 (2017).
pubmed: 28320787
pmcid: 5372108
doi: 10.1136/bmjopen-2016-012985
Marvin, M. M., Gardner, F. C., Sarsfield, K. M., Travagli, R. A. & Doheny, K. K. Increased frequency of skin-to-skin contact is associated with enhanced vagal tone and improved health outcomes in preterm neonates. Am. J. Perinatol. 36, 505–510 (2019).
pubmed: 30193382
doi: 10.1055/s-0038-1669946
Georgieff, M. K., Ramel, S. E. & Cusick, S. E. Nutritional influences on brain development. Acta Paediatr. 107, 1310–1321 (2018).
pubmed: 29468731
pmcid: 6045434
doi: 10.1111/apa.14287
Ottolini, K. M., Andescavage, N., Keller, S. & Limperopoulos, C. Nutrition and the developing brain: the road to optimizing early neurodevelopment: a systematic review. Pediatr. Res. 87, 194–201 (2020).
pubmed: 31349359
doi: 10.1038/s41390-019-0508-3
McPherson, C. et al. Brain injury and development in preterm infants exposed to fentanyl. Ann. Pharmacother. 49, 1291–1297 (2015).
pubmed: 26369570
pmcid: 4644677
doi: 10.1177/1060028015606732
Giordano, V. et al. Effect of increased opiate exposure on three years neurodevelopmental outcome in extremely preterm infants. Early Hum. Dev. 123, 1–5 (2018).
pubmed: 29935388
doi: 10.1016/j.earlhumdev.2018.06.010
Zwicker, J. G. et al. Smaller cerebellar growth and poorer neurodevelopmental outcomes in very preterm infants exposed to neonatal morphine. J. Pediatr. 172, 81–87.e82 (2016).
pubmed: 26763312
pmcid: 5462546
doi: 10.1016/j.jpeds.2015.12.024
McPherson, C., Miller, S. P., El-Dib, M., Massaro, A. N. & Inder, T. E. The influence of pain, agitation, and their management on the immature brain. Pediatr. Res. 88, 168–175 (2020).
pubmed: 31896130
pmcid: 7223850
doi: 10.1038/s41390-019-0744-6
Duerden, E. G. et al. Association of early skin breaks and neonatal thalamic maturation: a modifiable risk? Neurology 95, e3420–e3427 (2020).
pubmed: 33087497
pmcid: 7836658
doi: 10.1212/WNL.0000000000010953
Brummelte, S. et al. Procedural pain and brain development in premature newborns. Ann. Neurol. 71, 385–396 (2012).
pubmed: 22374882
pmcid: 3760843
doi: 10.1002/ana.22267
Vinall, J. et al. Invasive procedures in preterm children: brain and cognitive development at school age. Pediatrics 133, 412–421 (2014).
pubmed: 24534406
pmcid: 3934331
doi: 10.1542/peds.2013-1863
Campbell-Yeo, M. et al. Sustained efficacy of kangaroo care for repeated painful procedures over neonatal intensive care unit hospitalization: a single-blind randomized controlled trial. Pain 160, 2580–2588 (2019).
pubmed: 31356452
doi: 10.1097/j.pain.0000000000001646
Harrison, D., Loughnan, P., Manias, E. & Johnston, L. Analgesics administered during minor painful procedures in a cohort of hospitalized infants: a prospective clinical audit. J. Pain 10, 715–722 (2009).
pubmed: 19398379
doi: 10.1016/j.jpain.2008.12.011
Bennet, L., Walker, D. W. & Horne, R. S. C. Waking up too early—the consequences of preterm birth on sleep development. J. Physiol. 596, 5687–5708 (2018).
pubmed: 29691876
pmcid: 6265542
doi: 10.1113/JP274950
van den Hoogen, A. et al. How to improve sleep in a neonatal intensive care unit: a systematic review. Early Hum. Dev. 113, 78–86 (2017).
pubmed: 28720290
doi: 10.1016/j.earlhumdev.2017.07.002
Erdei, C., Inder, T. E., Dodrill, P. & Woodward, L. J. The Growth and Development Unit. A proposed approach for enhancing infant neurodevelopment and family-centered care in the neonatal intensive care unit. J. Perinatol. 39, 1684–1687 (2019).
pubmed: 31582813
doi: 10.1038/s41372-019-0514-7
O’Brien, K. et al. Effectiveness of family integrated care in neonatal intensive care units on infant and parent outcomes: a multicentre, multinational, cluster-randomised controlled trial. Lancet Child Adolesc. Health 2, 245–254 (2018).
pubmed: 30169298
doi: 10.1016/S2352-4642(18)30039-7
Edwards, E. M. & Horbar, J. D. Following through: interventions to improve long-term outcomes of preterm infants. Semin. Perinatol. 45, 151414 (2021).
pubmed: 33853737
doi: 10.1016/j.semperi.2021.151414
Waddington, C., van Veenendaal, N. R., O’Brien, K. & Patel, N. Family integrated care: supporting parents as primary caregivers in the neonatal intensive care unit. Pediatr. Investig. 5, 148–154 (2021).
pubmed: 34179713
pmcid: 8212757
doi: 10.1002/ped4.12277
Volpe, J. J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 8, 110–124 (2009).
pubmed: 19081519
pmcid: 2707149
doi: 10.1016/S1474-4422(08)70294-1
Baier, R. J. Genetics of perinatal brain injury in the preterm infant. Front. Biosci. 11, 1371–1387 (2006).
pubmed: 16368523
doi: 10.2741/1890
Sparrow, S. et al. Epigenomic profiling of preterm infants reveals DNA methylation differences at sites associated with neural function. Transl. Psychiatry 6, e716 (2016).
pubmed: 26784970
pmcid: 5068883
doi: 10.1038/tp.2015.210
Blüml, S., Wisnowski, J. L., Nelson, M. D. Jr., Paquette, L. & Panigrahy, A. Metabolic maturation of white matter is altered in preterm infants. PLoS ONE 9, e85829 (2014).
pubmed: 24465731
pmcid: 3899075
doi: 10.1371/journal.pone.0085829
McCrea, H. J. & Ment, L. R. The diagnosis, management, and postnatal prevention of intraventricular hemorrhage in the preterm neonate. Clin. Perinatol. 35, 777–792 (2008).
pubmed: 19026340
pmcid: 2901530
doi: 10.1016/j.clp.2008.07.014
Kofke, W. A. Incrementally applied multifaceted therapeutic bundles in neuroprotection clinical trials…time for change. Neurocrit. Care 12, 438–444 (2010).
pubmed: 20146027
doi: 10.1007/s12028-010-9332-7
Helenius, K., Longford, N., Lehtonen, L., Modi, N. & Gale, C. Association of early postnatal transfer and birth outside a tertiary hospital with mortality and severe brain injury in extremely preterm infants: observational cohort study with propensity score matching. BMJ 367, l5678 (2019).
pubmed: 31619384
pmcid: 6812621
doi: 10.1136/bmj.l5678
Fabres, J., Carlo, W. A., Phillips, V., Howard, G. & Ambalavanan, N. Both extremes of arterial carbon dioxide pressure and the magnitude of fluctuations in arterial carbon dioxide pressure are associated with severe intraventricular hemorrhage in preterm infants. Pediatrics 119, 299–305 (2007).
pubmed: 17272619
doi: 10.1542/peds.2006-2434
Miller, S. S., Lee, H. C. & Gould, J. B. Hypothermia in very low birth weight infants: distribution, risk factors and outcomes. J. Perinatol. 31, S49–S56 (2011).
pubmed: 21448204
doi: 10.1038/jp.2010.177
Vesoulis, Z. A. et al. Blood pressure extremes and severe IVH in preterm infants. Pediatr. Res. 87, 69–73 (2020).
pubmed: 31578033
doi: 10.1038/s41390-019-0585-3
Goswami, I. R., Abou Mehrem, A., Scott, J., Esser, M. J. & Mohammad, K. Metabolic acidosis rather than hypo/hypercapnia in the first 72 h of life associated with intraventricular hemorrhage in preterm neonates. J. Matern. Fetal Neonatal Med. 34, 3874–3882 (2021).
pubmed: 31852289
doi: 10.1080/14767058.2019.1701649
Malusky, S. & Donze, A. Neutral head positioning in premature infants for intraventricular hemorrhage prevention: an evidence-based review. Neonatal Netw. 30, 381–396 (2011).
pubmed: 22052118
doi: 10.1891/0730-0832.30.6.381
Anand, K. J. Clinical importance of pain and stress in preterm neonates. Biol. Neonate 73, 1–9 (1998).
pubmed: 9458936
doi: 10.1159/000013953
Lee, H. J. et al. Early sodium and fluid intake and severe intraventricular hemorrhage in extremely low birth weight infants. J. Korean Med. Sci. 30, 283–289 (2015).
pubmed: 25729251
pmcid: 4330483
doi: 10.3346/jkms.2015.30.3.283
Murthy, P. et al. Neuroprotection care bundle implementation to decrease acute brain injury in preterm infants. Pediatr. Neurol. 110, 42–48 (2020).
pubmed: 32473764
doi: 10.1016/j.pediatrneurol.2020.04.016
de Bijl-Marcus, K., Brouwer, A. J., De Vries, L. S., Groenendaal, F. & Wezel-Meijler, G. V. Neonatal care bundles are associated with a reduction in the incidence of intraventricular haemorrhage in preterm infants: a multicentre cohort study. Arch. Dis. Child Fetal Neonatal Ed. 105, 419–424 (2020).
pubmed: 31732682
doi: 10.1136/archdischild-2018-316692
McLendon, D. et al. Implementation of potentially better practices for the prevention of brain hemorrhage and ischemic brain injury in very low birth weight infants. Pediatrics 111, e497–e503 (2003).
pubmed: 12671170
doi: 10.1542/peds.111.SE1.e497
Benlamri, A. et al. Neuroprotection care bundle implementation is associated with improved long-term neurodevelopmental outcomes in extremely premature infants. J. Perinatol. 42, 1380–1384 (2022).
pubmed: 35831577
doi: 10.1038/s41372-022-01443-0
Mohammad, K. et al. Impact of quality improvement outreach education on the incidence of acute brain injury in transported neonates born premature. J. Perinatol. 42, 1368–1373 (2022).
pubmed: 35508716
doi: 10.1038/s41372-022-01409-2
Cramer, S. C. et al. Harnessing neuroplasticity for clinical applications. Brain 134, 1591–1609 (2011).
pubmed: 21482550
pmcid: 3102236
doi: 10.1093/brain/awr039
DeMaster, D. et al. Nurturing the preterm infant brain: leveraging neuroplasticity to improve neurobehavioral outcomes. Pediatr. Res. 85, 166–175 (2019).
pubmed: 30531968
doi: 10.1038/s41390-018-0203-9
Maguire, C. M. et al. Effects of individualized developmental care in a randomized trial of preterm infants <32 weeks. Pediatrics 124, 1021–1030 (2009).
pubmed: 19786441
doi: 10.1542/peds.2008-1881
Procianoy, R. S., Mendes, E. W. & Silveira, R. C. Massage therapy improves neurodevelopment outcome at two years corrected age for very low birth weight infants. Early Hum. Dev. 86, 7–11 (2010).
pubmed: 20022717
doi: 10.1016/j.earlhumdev.2009.12.001
Feldman, R., Rosenthal, Z. & Eidelman, A. I. Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biol. Psychiatry 75, 56–64 (2014).
pubmed: 24094511
doi: 10.1016/j.biopsych.2013.08.012
Braid, S. & Bernstein, J. Improved cognitive development in preterm infants with shared book reading. Neonatal Netw. 34, 10–17 (2015).
pubmed: 26803041
doi: 10.1891/0730-0832.34.1.10
Chorna, O. et al. Neuroprocessing mechanisms of music during fetal and neonatal development: a role in neuroplasticity and neurodevelopment. Neural Plast. 2019, 3972918 (2019).
pubmed: 31015828
pmcid: 6446122
doi: 10.1155/2019/3972918
Shellhaas, R. A., Burns, J. W., Barks, J. D. E., Hassan, F. & Chervin, R. D. Maternal voice and infant sleep in the neonatal intensive care unit. Pediatrics 144, e20190288 (2019).
Smith, S. W., Ortmann, A. J. & Clark, W. W. Noise in the neonatal intensive care unit: a new approach to examining acoustic events. Noise Health 20, 121–130 (2018).
pubmed: 30136672
pmcid: 6122266
Shellhaas, R. A. et al. Neonatal sleep-wake analyses predict 18-month neurodevelopmental outcomes. Sleep 40, zsx144 (2017).
Forcada-Guex, M., Pierrehumbert, B., Borghini, A., Moessinger, A. & Muller-Nix, C. Early dyadic patterns of mother-infant interactions and outcomes of prematurity at 18 months. Pediatrics 118, e107–e114 (2006).
pubmed: 16818525
doi: 10.1542/peds.2005-1145
Benavente-Fernández, I., Siddiqi, A. & Miller, S. P. Socioeconomic status and brain injury in children born preterm: modifying neurodevelopmental outcome. Pediatr. Res. 87, 391–398 (2020).
pubmed: 31666689
doi: 10.1038/s41390-019-0646-7
Bills, S. E., Johnston, J. D., Shi, D. & Bradshaw, J. [Formula: see text] Social-environmental moderators of neurodevelopmental outcomes in youth born preterm: a systematic review. Child Neuropsychol. 27, 351–370 (2021).
pubmed: 33342364
doi: 10.1080/09297049.2020.1861229
Linsell, L., Malouf, R., Morris, J., Kurinczuk, J. J. & Marlow, N. Prognostic factors for poor cognitive development in children born very preterm or with very low birth weight: a systematic review. JAMA Pediatr. 169, 1162–1172 (2015).
pubmed: 26457641
pmcid: 5122448
doi: 10.1001/jamapediatrics.2015.2175
Joseph, R. M. et al. Maternal social risk, gestational age at delivery, and cognitive outcomes among adolescents born extremely preterm. Paediatr. Perinat. Epidemiol. 36, 654–664 (2022).
pubmed: 36530363
pmcid: 9754639
doi: 10.1111/ppe.12893
Benavente-Fernández, I. et al. Association of socioeconomic status and brain injury with neurodevelopmental outcomes of very preterm children. JAMA Netw. Open 2, e192914 (2019).
pubmed: 31050776
pmcid: 6503490
doi: 10.1001/jamanetworkopen.2019.2914
Salazar, E. G. et al. County-level maternal vulnerability and preterm birth in the US. JAMA Netw. Open 6, e2315306 (2023).
pubmed: 37227724
pmcid: 10214038
doi: 10.1001/jamanetworkopen.2023.15306
Carter, J. G., Feinglass, J. M. & Yee, L. M. Perception of neighborhood safety and maternal and neonatal health outcomes. JAMA Netw. Open 6, e2317153 (2023).
pubmed: 37256625
pmcid: 10233411
doi: 10.1001/jamanetworkopen.2023.17153
Mckinnon, K. et al. Association of preterm birth and socioeconomic status with neonatal brain structure. JAMA Netw. Open 6, e2316067 (2023).
pubmed: 37256618
pmcid: 10233421
doi: 10.1001/jamanetworkopen.2023.16067