Postnatal Nutrition to Improve Brain Development in the Preterm Infant: A Systematic Review From Bench to Bedside

Lisa M Hortensius, Ruurd M van Elburg, Cora H Nijboer, Manon J N L Benders, Caroline G M de Theije, Lisa M Hortensius, Ruurd M van Elburg, Cora H Nijboer, Manon J N L Benders, Caroline G M de Theije

Abstract

Background: Preterm infants are at high risk for Encephalopathy of Prematurity and successive adverse neurodevelopmental outcome. Adequate nutrition is crucial for healthy brain development. Maternal breast milk is first choice of post-natal enteral nutrition for preterm infants. However, breast milk contains insufficient nutrient quantities to meet the greater nutritional needs of preterm infants, meaning that supplementation is recommended. Aim: To provide an overview of current literature on potential nutritional interventions for improvement of neurodevelopmental outcome in preterm infants, by taking a bench to bedside approach from pre-clinical models of neonatal brain injury to randomized controlled clinical trials (RCTs) in preterm infants. Methods: Separate clinical and pre-clinical searches were performed in Medline and Embase for English written papers published between 08/2008 and 08/2018 that studied a single nutritional component. Papers were included if one of the following components was studied: lipids, carbohydrates, proteins, vitamins, minerals, probiotics, prebiotics, oligosaccharides, fatty acids, or amino acids, with brain injury, brain development or neurodevelopmental outcome as outcome measure in preterm infants (gestational age <32 weeks and/or birth weight <1,500 g) or in animal models of neonatal brain injury. Results: In total, 2,671 pre-clinical studies and 852 RCTs were screened, of which 24 pre-clinical and 22 RCTs were included in this review. In these trials supplementation with amino acids and protein, lipids, probiotics (only clinical), prebiotics (only clinical), vitamins, and minerals was studied. All included pre-clinical studies show positive effect of supplementation on brain injury and/or neurodevelopment. Although some nutrients, such as glutamine, show promising short term outcome in clinical studies, no evident long term effect of any supplemented nutrient was found. Main limitations were inclusion of studies no older than 10 years at time of search and studies that focused on single nutritional components only. Conclusion: Even though many pre-clinical trials demonstrate promising effects of different nutritional interventions on reducing brain injury and/or improving neurodevelopmental outcome, these positive effects have so far not evidently been demonstrated in RCTs. More clinically relevant animal models and long term follow up after clinical trials are needed to move novel nutritional therapies from bench to bedside of preterm infants.

Keywords: animal models; brain injury; clinical; neurodevelopment; nutrition; pre-clinical; preterm infants.

Figures

Figure 1
Figure 1
Flowchart of pre-clinical search process.
Figure 2
Figure 2
Flowchart of clinical search process.
Figure 3
Figure 3
Risk of bias of individual pre-clinical studies.
Figure 4
Figure 4
Risk of bias across pre-clinical studies.
Figure 5
Figure 5
Risk of bias of individual clinical studies.
Figure 6
Figure 6
Risk of bias across clinical studies.

References

    1. Almaas A. N., Tamnes C. K., Nakstad B., Henriksen C., Grydeland H., Walhovd K. B., et al. . (2016). Diffusion tensor imaging and behavior in premature infants at 8 years of age, a randomized controlled trial with long-chain polyunsaturated fatty acids. Early Hum. Dev. 95, 41–46. 10.1016/j.earlhumdev.2016.01.021
    1. Almaas A. N., Tamnes C. K., Nakstad B., Henriksen C., Walhovd K. B., Fjell A. M., et al. . (2015). Long-chain polyunsaturated fatty acids and cognition in VLBW infants at 8 years: an RCT. Pediatrics 135, 972–980. 10.1542/peds.2014-4094
    1. Alshweki A., Muñuzuri A. P., Baña A. M., de Castro M. J., Andrade F., Aldamiz-Echevarría L., et al. . (2015). Effects of different arachidonic acid supplementation on psychomotor development in very preterm infants; a randomized controlled trial. Nutr. J. 14:101. 10.1186/s12937-015-0091-3
    1. American Academy of Pediatrics (2009). Committee on nutrition: nutritional needs of the preterm infant, in Pediatric Nutrition Handbook, 6th Edn. ed Kleinman R. (Elk Grove Village, IL: American Academy of Pediatrics; ), 83.
    1. Amin H. J., Soraisham A. S., Sauve R. S. (2009). Neurodevelopmental outcomes of premature infants treated with l-arginine for prevention of necrotising enterocolitis. J. Paediatr. Child. Health 45, 219–223. 10.1111/j.1440-1754.2008.01458.x
    1. Andersen A. D., Sangild P. T., Munch S. L., van der Beek E. M., Renes I. B., Ginneken C. v., et al. . (2016). Delayed growth, motor function and learning in preterm pigs during early postnatal life. Am. J. Physiol. Regul. Integr. Comp. Physiol. 310, R481–R492. 10.1152/ajpregu.00349.2015
    1. Arteaga O., Revuelta M., Urigüen L., Martínez-Millán L., Hilario E., Álvarez A. (2017). Docosahexaenoic acid reduces cerebral damage and ameliorates long-term cognitive impairments caused by neonatal hypoxia-ischemia in rats. Mol. Neurobiol. 54, 7137–7155. 10.1007/s12035-016-0221-8
    1. Balakrishnan M., Jennings A., Przystac L., Phornphutkul C., Tucker R., Vohr B., et al. . (2017). Growth and neurodevelopmental outcomes of early, high-dose parenteral amino acid intake in very low birth weight infants: a randomized controlled trial. JPEN J. Parenter. Enteral. Nutr. 42, 597–606. 10.1177/0148607117696330
    1. Bellagamba M. P., Carmenati E., D'Ascenzo R., Malatesta M., Spagnoli C., Biagetti C., et al. . (2016). One extra gram of protein to preterm infants from birth to 1800 g: a single-blinded randomized clinical trial. J. Pediatr. Gastroenterol. Nutr. 62, 879–884. 10.1097/MPG.0000000000000989
    1. Berman D. R., Liu Y. Q., Barks J., Mozurkewich E. (2010). Docosahexaenoic acid confers neuroprotection in a rat model of perinatal hypoxia-ischemia potentiated by Escherichia coli lipopolysaccharide-induced systemic inflammation. Am. J. Obstet. Gynecol. 202, 469 e461–466. 10.1016/j.ajog.2010.01.076
    1. Berman D. R., Mozurkewich E., Liu Y., Barks J. (2009). Docosahexaenoic acid pretreatment confers neuroprotection in a rat model of perinatal cerebral hypoxia-ischemia. Am. J. Obstet. Gynecol. 200, 305.e1–e6. 10.1016/j.ajog.2009.01.020
    1. Berman D. R., Mozurkewich E., Liu Y., Shangguan Y., Barks J. D., Silverstein F. S. (2013). Docosahexaenoic acid augments hypothermic neuroprotection in a neonatal rat asphyxia model. Neonatology 104, 71–78. 10.1159/000351011
    1. Bertelsen R. J., Jensen E. T., Ringel-Kulka T. (2016). Use of probiotics and prebiotics in infant feeding. Best Pract. Res. Clin. Gastroenterol. 30, 39–48. 10.1016/j.bpg.2016.01.001
    1. Blanco C. L., Gong A. K., Schoolfield J., Green B. K., Daniels W., Liechty E. A., et al. . (2012). Impact of early and high amino acid supplementation on ELBW infants at 2 years. J. Pediatr. Gastroenterol. Nutr. 54, 601–607. 10.1097/MPG.0b013e31824887a0
    1. Bouyssi-Kobar M., du Plessis A. J., McCarter R., Brossard-Racine M., Murnick J., Tinkleman L., et al. . (2016). Third trimester brain growth in preterm infants compared with in utero healthy fetuses. Pediatrics 138:e20161640. 10.1542/peds.2016-1640
    1. Boyce C., Watson M., Lazidis G., Reeve S., Dods K., Simmer K., et al. . (2016). Preterm human milk composition: a systematic literature review. Br. J. Nutr. 116, 1033–1045. 10.1017/S0007114516003007
    1. Brown J. V., Embleton N. D., Harding J. E., McGuire W. (2016). Multi-nutrient fortification of human milk for preterm infants. Cochrane Database Syst. Rev. 8:CD000343 10.1002/14651858.CD000343.pub3
    1. Buddington R. K., Chizhikov V. V., Iskusnykh I. Y., Sable H. J., Sable J. J., Holloway Z. R., et al. . (2018). A phosphatidylserine source of docosahexanoic acid improves neurodevelopment and survival of preterm pigs. Nutrients 10:637. 10.3390/nu10050637
    1. Burattini I., Bellagamba M. P., Spagnoli C., D'Ascenzo R., Mazzoni N., Peretti A., et al. . (2013). Targeting 2.5 versus 4 g/kg/day of amino acids for extremely low birth weight infants: a randomized clinical trial. J. Pediatr. 163, 1278–1282 e1271. 10.1016/j.jpeds.2013.06.075
    1. Chan S. H., Johnson M. J., Leaf A. A., Vollmer B. (2016). Nutrition and neurodevelopmental outcomes in preterm infants: a systematic review. Acta Paediatr. 105, 587–599. 10.1111/apa.13344
    1. Chou I. C., Kuo H. T., Chang J. S., Wu S. F., Chiu H. Y., Su B. H., et al. . (2010). Lack of effects of oral probiotics on growth and neurodevelopmental outcomes in preterm very low birth weight infants. J. Pediatr. 156, 393–396. 10.1016/j.jpeds.2009.09.051
    1. Coviello C., Keunen K., Kersbergen K. J., Groenendaal F., Leemans A., Peels B., et al. . (2018). Effects of early nutrition and growth on brain volumes, white matter microstructure, and neurodevelopmental outcome in preterm newborns. Pediatr. Res. 83, 102–110. 10.1038/pr.2017.227
    1. Dabydeen L., Thomas J. E., Aston T. J., Hartley H., Sinha S. K., Eyre J. A. (2008). High-energy and -protein diet increases brain and corticospinal tract growth in term and preterm infants after perinatal brain injury. Pediatrics 121, 148–156. 10.1542/peds.2007-1267
    1. de Kieviet J. F., Oosterlaan J., Vermeulen R. J., Pouwels P. J., Lafeber H. N., van Elburg R. M. (2012). Effects of glutamine on brain development in very preterm children at school age. Pediatrics 130, e1121–e1127. 10.1542/peds.2012-0928
    1. de Kieviet J. F., Vuijk P. J., van den Berg A., Lafeber H. N., Oosterlaan J., van Elburg R. M. (2014). Glutamine effects on brain growth in very preterm children in the first year of life. Clin. Nutr. 33, 69–74. 10.1016/j.clnu.2013.03.019
    1. Dogra S., Thakur A., Garg P., Kler N. (2017). Effect of differential enteral protein on growth and neurodevelopment in infants <1500 g: a randomized controlled trial. J. Pediatr. Gastroenterol. Nutr. 64, e126–e132. 10.1097/MPG.0000000000001451
    1. Euro-Peristat Project with SCPE EUROCAT (2013). European Perinatal Health Report. The Health and Care of Pregnant Women and Babies in Europe in 2010. Available online at: (accessed July 18, 2019).
    1. Franz A. R., Pohlandt F., Bode H., Mihatsch W. A., Sander S., Kron M., et al. . (2009). Intrauterine, early neonatal, and postdischarge growth and neurodevelopmental outcome at 5.4 years in extremely preterm infants after intensive neonatal nutritional support. Pediatrics 123, e101–e109. 10.1542/peds.2008-1352
    1. Georgieff M. K. (2007). Nutrition and the developing brain: nutrient priorities and measurement. Am. J. Clin. Nutr. 85, 614S−620S. 10.1093/ajcn/85.2.614S
    1. Ginet V., van de Looij Y., Petrenko V., Toulotte A., Kiss J., Hüppi P. S., et al. . (2016). Lactoferrin during lactation reduces lipopolysaccharide-induced brain injury. Biofactors 42, 323–336. 10.1002/biof.1278
    1. Glass H. C., Costarino A. T., Stayer S. A., Brett C. M., Cladis F., Davis P. J. (2015). Outcomes for extremely premature infants. Anesth Analg. 120, 1337–1351. 10.1213/ANE.0000000000000705
    1. Griffith J. L., Shimony J. S., Cousins S. A., Rees S. E., McCurnin D. C., Inder T. E., et al. . (2012). MR imaging correlates of white-matter pathology in a preterm baboon model. Pediatr. Res. 71, 185–191. 10.1038/pr.2011.33
    1. Gussenhoven R., Westerlaken R. J. J., Ophelders D. R. M. G., Jobe A. H., Kemp M. W., Kallapur S. G., et al. . (2018). Chorioamnionitis, neuroinflammation, and injury: timing is key in the preterm ovine fetus. J. Neuroinflamm. 15:113. 10.1186/s12974-018-1149-x
    1. Higgins J. P. T., Altman D. G., Sterne J. A. C. (2011). Chapter 8: assessing risk of bias in included studies, in Cochrane Handbook for Systematic Reviews of Interventions, eds Higgins J. P. T., Green S. (The Cochrane Collaboration; ). Available online at:
    1. Hooijmans C. R., Rovers M. M., de Vries R. B., Leenaars M., Ritskes-Hoitinga M., Langendam M. W. (2014). SYRCLE's risk of bias tool for animal studies. BMC Med. Res. Methodol. 14:43. 10.1186/1471-2288-14-43
    1. Huun M. U., Garberg H. T., Buonocore G., Longini M., Belvisi E., Bazzini F., et al. . (2018). Regional differences of hypothermia on oxidative stress following hypoxia-ischemia: a study of DHA and hypothermia on brain lipid peroxidation in newborn piglets. J. Perinat. Med. 47, 82–89. 10.1515/jpm-2017-0355
    1. Jacobs S. E., Hickey L., Donath S., Opie G. F., Anderson P. J., Garland S. M., et al. . (2017). Probiotics, prematurity and neurodevelopment: follow-up of a randomised trial. BMJ Paediatr. Open 1:e000176. 10.1136/bmjpo-2017-000176
    1. Jasani B., Simmer K., Patole S. K., Rao S. C. (2017). Long chain polyunsaturated fatty acid supplementation in infants born at term. Cochrane Database Syst. Rev. 3:CD000376. 10.1002/14651858.CD000376.pub4
    1. Jaworska J., Ziemka-Nalecz M., Sypecka J., Zalewska T. (2017). The potential neuroprotective role of a histone deacetylase inhibitor, sodium butyrate, after neonatal hypoxia-ischemia. J. Neuroinflamm. 14:34. 10.1186/s12974-017-0807-8
    1. Kersbergen K. J., Makropoulos A., Aljabar P., Groenendaal F., de Vries L. S., Counsell S. J., et al. . (2016). Longitudinal regional brain development and clinical risk factors in extremely preterm infants. J Pediatr. 178, 93–100.e6. 10.1016/j.jpeds.2016.08.024
    1. Koning G., Leverin A. L., Nair S., Schwendimann L., Ek J., Carlsson Y., et al. . (2017). Magnesium induces preconditioning of the neonatal brain via profound mitochondrial protection. J. Cereb. Blood Flow Metab. 39, 1038–1055. 10.1177/0271678X17746132
    1. LeCouffe N. E., Westerbeek E. A., van Schie P. E., Schaaf V. A., Lafeber H. N., van Elburg R. M. (2014). Neurodevelopmental outcome during the first year of life in preterm infants after supplementation of a prebiotic mixture in the neonatal period: a follow-up study. Neuropediatrics 45, 22–29. 10.1055/s-0033-1349227
    1. Li J., Yawno T., Sutherland A., Loose J., Nitsos I., Bischof R., et al. . (2016). Preterm white matter brain injury is prevented by early administration of umbilical cord blood cells. Exp. Neurol. 283(Pt A), 179–187. 10.1016/j.expneurol.2016.06.017
    1. Linsell L., Malouf R., Morris J., Kurinczuk J. J., Marlow N. (2015). 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. 10.1001/jamapediatrics.2015.2175
    1. Liu L., Johnson H. L., Cousens S., Perin J., Scott S., Lawn J. E., et al. . (2012). Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 379, 2151–2161. 10.1016/S0140-6736(12)60560-1
    1. Liu S., Xin D., Wang L., Zhang T., Bai X., Li T., et al. . (2017). Therapeutic effects of L-Cysteine in newborn mice subjected to hypoxia-ischemia brain injury via the CBS/H2S system: role of oxidative stress and endoplasmic reticulum stress. Redox Biol. 13, 528–540. 10.1016/j.redox.2017.06.007
    1. Luttikhuizen dos Santos E. S., de Kieviet J. F., Königs M., van Elburg R. M., Oosterlaan J. (2013). Predictive value of the Bayley scales of infant development on development of very preterm/very low birth weight children: a meta-analysis. Early Hum. Dev. 89, 487–496. 10.1016/j.earlhumdev.2013.03.008
    1. Mayurasakorn K., Niatsetskaya Z. V., Sosunov S. A., Williams J. J., Zirpoli H., Vlasakov I., et al. (2016). DHA but not EPA emulsions preserve neurological and mitochondrial function after brain hypoxia-ischemia in neonatal mice. PLoS ONE 11:e0160870 10.1371/journal.pone.0160870
    1. Mimouni F. B., Lubetzky R., Yochpaz S., Mandel D. (2017). Preterm human milk macronutrient and energy composition: a systematic review and meta-analysis. Clin. Perinatol. 44, 165–172. 10.1016/j.clp.2016.11.010
    1. Miura S., Ishida-Nakajima W., Ishida A., Kawamura M., Ohmura A., Oguma R., et al. . (2009). Ascorbic acid protects the newborn rat brain from hypoxic-ischemia. Brain Dev. 31, 307–317. 10.1016/j.braindev.2008.06.010
    1. Moher D., Liberati A., Tetzlaff J., Altman D. G., Group P. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6:e1000097 10.1371/journal.pmed.1000097
    1. Mori H., Momosaki K., Kido J., Naramura T., Tanaka K., Matsumoto S., et al. . (2017). Amelioration by glycine of brain damage in neonatal rat brain following hypoxia-ischemia. Pediatr. In. 59, 321–327. 10.1111/ped.13164
    1. Nagasawa T., Kiyosawa I., Kuwahara K. (1972). Amounts of lactoferrin in human colostrum and milk. J. Dairy Sci. 55, 1651–1659. 10.3168/jds.S0022-0302(72)85741-2
    1. Oliveira F. L., Rumsey S. C., Schlotzer E., Hansen I., Carpentier Y. A., Deckelbaum R. J. (1997). Triglyceride hydrolysis of soy oil vs fish oil emulsions. JPEN J. Parenter. Enteral. Nutr. 21, 224–229. 10.1177/0148607197021004224
    1. Ong M. L., Purdy I. B., Levit O. L., Robinson D. T., Grogan T., Flores M., et al. . (2018). Two-year neurodevelopment and growth outcomes for preterm neonates who received low-dose intravenous soybean oil. JPEN J. Parenter. Enteral. Nutr. 42, 352–360. 10.1177/0148607116674482
    1. Peterson J., Taylor H. G., Minich N., Klein N., Hack M. (2006). Subnormal head circumference in very low birth weight children: neonatal correlates and school-age consequences. Early Hum. Dev. 82, 325–334. 10.1016/j.earlhumdev.2005.09.014
    1. Ramani M., van Groen T., Kadish I., Ambalavanan N., McMahon L. L. (2017). Vitamin, A., and retinoic acid combination attenuates neonatal hyperoxia-induced neurobehavioral impairment in adult mice. Neurobiol. Learn. Mem. 141, 209–216. 10.1016/j.nlm.2017.04.013
    1. Rangon C. M., Schang A. L., Van Steenwinckel J., Schwendimann L., Lebon S., Fu T., et al. . (2018). Myelination induction by a histamine H3 receptor antagonist in a mouse model of preterm white matter injury. Brain Behav. Immun. 74, 265–276. 10.1016/j.bbi.2018.09.017
    1. Rassin D. K. (1981). The function of taurine in the central nervous system. Adv. Biochem. Psychopharmacol. 29, 127–134.
    1. Review Manager (RevMan) [computer program] (2014). Version 5.3. Copgenhagen: The Nordic Cochrane Centre The Cochrane Collaboration.
    1. Revuelta M., Arteaga O., Montalvo H., Alvarez A., Hilario E., Martinez-Ibargüen A. (2016). Antioxidant treatments recover the alteration of auditory-evoked potentials and reduce morphological damage in the inferior colliculus after perinatal asphyxia in rat. Brain Pathol. 26, 186–198. 10.1111/bpa.12272
    1. Salas A. A., Woodfin T., Phillips V., Peralta-Carcelen M., Carlo W. A., Ambalavanan N. (2018). Dose-response effects of early vitamin D supplementation on neurodevelopmental and respiratory outcomes of extremely preterm infants at 2 years of age: a randomized trial. Neonatology 113, 256–262. 10.1159/000484399
    1. Salmaso N., Jablonska B., Scafidi J., Vaccarino F. M., Gallo V. (2014). Neurobiology of premature brain injury. Nat. Neurosci. 17, 341–346. 10.1038/nn.3604
    1. Sari F. N., Eras Z., Dizdar E. A., Erdeve O., Oguz S. S., Uras N., et al. . (2012). Do oral probiotics affect growth and neurodevelopmental outcomes in very low-birth-weight preterm infants? Am. J. Perinatol. 29, 579–586. 10.1055/s-0032-1311981
    1. Schneider J., Fischer Fumeaux C. J., Duerden E. G., Guo T., Foong J., Graz M. B., et al. . (2018). Nutrient intake in the first two weeks of life and brain growth in preterm neonates. Pediatrics 141:e20172169. 10.1542/peds.2017-2169
    1. Schneider N., Garcia-Rodenas C. L. (2017). Early nutritional interventions for brain and cognitive development in preterm infants: a review of the literature. Nutrients 9:E187. 10.3390/nu9030187
    1. Semple B. D., Blomgren K., Gimlin K., Ferriero D. M., Noble-Haeusslein L. J. (2013). Brain development in rodents and humans: identifying benchmarks of maturation and vulnerability to injury across species. Prog. Neurobiol. 106–107, 1–16. 10.1016/j.pneurobio.2013.04.001
    1. Seyama T., Kamei Y., Iriyama T., Imada S., Ichinose M., Toshimitsu M., et al. . (2018). Pretreatment with magnesium sulfate attenuates white matter damage by preventing cell death of developing oligodendrocytes. J. Obstet. Gynaecol. Res. 44, 601–607. 10.1111/jog.13568
    1. Singh A. K., Yoshida Y., Garvin A. J., Singh I. (1989). Effect of fatty acids and their derivatives on mitochondrial structures. J. Exp. Pathol. 4, 9–15.
    1. Solberg R., Longini M., Proietti F., Perrone S., Felici C., Porta A., et al. . (2017). DHA reduces oxidative stress after perinatal asphyxia: a study in newborn piglets. Neonatology 112, 1–8. 10.1159/000454982
    1. Stephens B. E., Walden R. V., Gargus R. A., Tucker R., McKinley L., Mance M., et al. . (2009). First-week protein and energy intakes are associated with 18-month developmental outcomes in extremely low birth weight infants. Pediatrics 123, 1337–1343. 10.1542/peds.2008-0211
    1. Tanaka K., Hosozawa M., Kudo N., Yoshikawa N., Hisata K., Shoji H., et al. . (2013). The pilot study: sphingomyelin-fortified milk has a positive association with the neurobehavioural development of very low birth weight infants during infancy, randomized control trial. Brain Dev. 35, 45–52. 10.1016/j.braindev.2012.03.004
    1. Tang S., Xu S., Lu X., Gullapalli R. P., McKenna M. C., Waddell J. (2016). Neuroprotective effects of Acetyl-L-Carnitine on neonatal hypoxia ischemia-induced brain injury in rats. Dev. Neurosci. 38, 384–396. 10.1159/000455041
    1. Twilhaar E. S., de Kieviet J. F., Aarnoudse-Moens C. S., van Elburg R. M., Oosterlaan J. (2018b). Academic performance of children born preterm: a meta-analysis and meta-regression. Arch. Dis. Child. Fetal. Neonatal. Ed. 103, F322–F330. 10.1136/archdischild-2017-312916
    1. Twilhaar E. S., de Kieviet J. F., Oosterlaan J., van Elburg R. M. (2018a). A randomised trial of enteral glutamine supplementation for very preterm children showed no beneficial or adverse long-term neurodevelopmental outcomes. Acta Paediatr. 107, 593–599. 10.1111/apa.14167
    1. Twilhaar E. S., Wade R. M., de Kieviet J. F., van Goudoever J. B., van Elburg R. M., Oosterlaan J. (2018c). Cognitive outcomes of children born extremely or very preterm since the 1990s and associated risk factors: a meta-analysis and meta-regression. JAMA Pediatr. 172, 361–367. 10.1001/jamapediatrics.2017.5323
    1. Vaisman N., Pelled D. (2009). n-3 phosphatidylserine attenuated scopolamine-induced amnesia in middle-aged rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 952–959. 10.1016/j.pnpbp.2009.04.021
    1. van de Looij Y., Ginet V., Chatagner A., Toulotte A., Somm E., Hüppi P. S., et al. . (2014). Lactoferrin during lactation protects the immature hypoxic-ischemic rat brain. Ann. Clin. Transl. Neurol. 1, 955–967. 10.1002/acn3.138
    1. van den Akker C. H., te Braake F. W., Weisglas-Kuperus N., van Goudoever J. B. (2014). Observational outcome results following a randomized controlled trial of early amino acid administration in preterm infants. J. Pediatr. Gastroenterol. Nutr. 59, 714–719. 10.1097/MPG.0000000000000549
    1. van Tilborg E., Achterberg E. J. M., van Kammen C. M., van der Toorn A., Groenendaal F., Dijkhuizen R. M., et al. . (2018a). Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism-like behavior in a rat model of diffuse white matter injury. Glia 66, 78–93. 10.1002/glia.23216
    1. van Tilborg E., de Theije C. G. M., van Hal M., Wagenaar N., de Vries L. S., Benders M. J., et al. . (2018b). Origin and dynamics of oligodendrocytes in the developing brain: implications for perinatal white matter injury. Glia 66, 221–238. 10.1002/glia.23256
    1. van Tilborg E., Heijnen C. J., Benders M. J., van Bel F., Fleiss B., Gressens P., et al. . (2016). Impaired oligodendrocyte maturation in preterm infants: potential therapeutic targets. Prog. Neurobiol. 136, 28–49. 10.1016/j.pneurobio.2015.11.002
    1. van den Berg J. P., Westerbeek E. A., Bröring-Starre T., Garssen J., van Elburg R. M. (2016). Neurodevelopment of preterm infants at 24 months after neonatal supplementation of a prebiotic mix: a randomized trial. J. Pediatr. Gastroenterol. Nutr. 63, 270–276. 10.1097/MPG.0000000000001148
    1. Wassink G., Davidson J. O., Dhillon S. K., Fraser M., Galinsky R., Bennet L., et al. . (2017). 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. 10.1177/0271678X16650455
    1. Williams F. L. R., Ogston S., Hume R., Watson J., Stanbury K., Willatts P., et al. (2017). Supplemental iodide for preterm infants and developmental outcomes at 2 years: an, R. C. T. Pediatrics 139:e20163703 10.1542/peds.2016-3703
    1. Williams J. J., Mayurasakorn K., Vannucci S. J., Mastropietro C., Bazan N. G., Ten V. S., et al. . (2013). N-3 fatty acid rich triglyceride emulsions are neuroprotective after cerebral hypoxic-ischemic injury in neonatal mice. PLoS ONE 8:e56233. 10.1371/journal.pone.0056233
    1. World Health Organization (2015). WHO Recommendations on Interventions to Improve Preterm Birth Outcomes. Geneva: World Health Organization.
    1. Wu J. Y., Prentice H. (2010). Role of taurine in the central nervous system. J Biomed Sci. 17 Suppl 1:S1. 10.1186/1423-0127-17-S1-S1
    1. Xin D., Chu X., Bai X., Ma W., Yuan H., Qiu J., et al. . (2018). l-Cysteine suppresses hypoxia-ischemia injury in neonatal mice by reducing glial activation, promoting autophagic flux and mediating synaptic modification via H2S formation. Brain Behav. Immun. 73, 222–234. 10.1016/j.bbi.2018.05.007
    1. Xu S., Waddell J., Zhu W., Shi D., Marshall A. D., McKenna M. C., et al. . (2015). In vivo longitudinal proton magnetic resonance spectroscopy on neonatal hypoxic-ischemic rat brain injury: Neuroprotective effects of acetyl-L-carnitine. Magn. Reson. Med. 74, 1530–1542. 10.1002/mrm.25537
    1. Zeng Y., Wang H., Zhang L., Tang J., Shi J., Xiao D., et al. . (2018). The optimal choices of animal models of white matter injury. Rev. Neurosci. 30, 245–259. 10.1515/revneuro-2018-0044
    1. Zhu X. Y., Ma P. S., Wu W., Zhou R., Hao Y. J., Niu Y., et al. . (2016). Neuroprotective actions of taurine on hypoxic-ischemic brain damage in neonatal rats. Brain Res. Bull. 124, 295–305. 10.1016/j.brainresbull.2016.06.010
    1. Ziemka-Nalecz M., Jaworska J., Sypecka J., Polowy R., Filipkowski R. K., Zalewska T. (2017). Sodium butyrate, a histone deacetylase inhibitor, exhibits neuroprotective/neurogenic effects in a rat model of neonatal hypoxia-ischemia. Mo. Neurobiol. 54, 5300–5318. 10.1007/s12035-016-0049-2

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