Generic placeholder image

Current Pediatric Reviews

Editor-in-Chief

ISSN (Print): 1573-3963
ISSN (Online): 1875-6336

Research Article

Adenosine Blood Level: A Biomarker of White Matter Damage in Very Low Birth Weight Infants

Author(s): Marina Colella, Isabella Panfoli*, Matteo Doglio, Michela Cassanello, Maurizio Bruschi, Laura C. De Angelis, Giovanni Candiano, Alessandro Parodi, Mariya Malova, Andrea Petretto, Giovanni Morana, Domenico Tortora, Mariasavina Severino, Mohamad Maghnie, Giuseppe Buonocore, Andrea Rossi, Oliver Baud and Luca A. Ramenghi

Volume 18, Issue 2, 2022

Published on: 11 March, 2022

Page: [153 - 163] Pages: 11

DOI: 10.2174/1573396318666220127155943

open access plus

Abstract

Background: Very low birth weight infants are at risk of developing periventricular white matter lesions. We previously reported high blood adenosine levels in premature infants and infants with low birth weight. We asked whether blood adenosine levels could be related to the vulnerability of the maturing white matter to develop lesions. The present study aims at finding a biomarker for the early detection of brain white matter lesions that can profoundly influence the neurodevelopmental outcome, whose pathophysiology is still unclear.

Methods: Dried blood spots were prospectively collected for the newborn screening program and adenosine concentration measurements. Fifty-six newborns who tested four times for blood adenosine concentration (at days 3, 15, 30, and 40 post-birth) were included in the program. All infants underwent brain MRI at term equivalent age. Neurodevelopmental outcomes were studied with Griffiths Mental Development Scales (GMDS) at 12 ± 2 months corrected age.

Results: Blood adenosine concentration increased over time from a median of 0.75 μM at Day 3 to 1.46 μM at Day 40. Adenosine blood concentration >1.58 μM at Day 15 was significantly associated with brain white matter lesions at MRI (OR (95 % CI) of 50.0 (3.6-688.3), p-value < 0.001). A moderate negative correlation between adenosine at 15 days of life and GMDS at 12 ± 2 months corrected age was found.

Conclusion: These findings suggest a potential role for blood adenosine concentration as a biomarker of creberal white matter lesions in very low birth weight infants.

Keywords: Adenosine, biomarker, brain injury, brain MRI, periventricular white matter lesions, prematurity, very low weight at birth.

Graphical Abstract

[1]
Walani SR. Global burden of preterm birth. Int J Gynaecol Obstet 2020; 150(1): 31-3.
[http://dx.doi.org/10.1002/ijgo.13195] [PMID: 32524596]
[2]
Rutherford MA, Supramaniam V, Ederies A, et al. Magnetic resonance imaging of white matter diseases of prematurity. Neuroradiology 2010; 52(6): 505-21.
[http://dx.doi.org/10.1007/s00234-010-0700-y] [PMID: 20422407]
[3]
Mallard C, Davidson JO, Tan S, et al. Astrocytes and microglia in acute cerebral injury underlying cerebral palsy associated with preterm birth. Pediatr Res 2014; 75(1-2): 234-40.
[http://dx.doi.org/10.1038/pr.2013.188] [PMID: 24336433]
[4]
Sannia A, Natalizia AR, Parodi A, et al. Different gestational ages and changing vulnerability of the premature brain. J Matern Neonatal Med 2015; 28(Suppl. 1): 2268-72.
[http://dx.doi.org/10.3109/14767058.2013.796166] [PMID: 23968292]
[5]
Parodi A, Govaert P, Horsch S, Bravo MC, Ramenghi LA, Agut T, et al. Cranial ultrasound findings in preterm germinal matrix haemorrhage, sequelae and outcome. Pediatr Res 2020; 87(Suppl. 1): 13-24.
[http://dx.doi.org/10.1038/s41390-020-0780-2] [PMID: 32218535]
[6]
Parodi A, Ramenghi LA, Malova M, et al. Crossed pontine hemiatrophy associated with unilateral cerebellar hemorrhage in premature infants. Neuropediatrics 2016; 47(6): 404-7.
[http://dx.doi.org/10.1055/s-0036-1587595] [PMID: 27552027]
[7]
Ramenghi LA. Germinal Matrix-Intraventricular Haemorrhage: still a very important brain lesion in premature infants! J Matern Fetal Neonatal Med 2015; 28(Suppl. 1): 2259-60.
[http://dx.doi.org/10.3109/14767058.2013.1031952] [PMID: 26365359]
[8]
Tortora D, Severino M, Malova M, et al. Differences in subependymal vein anatomy may predispose preterm infants to GMH-IVH. Arch Dis Child Fetal Neonatal Ed 2018; 103(1): F59-65.
[http://dx.doi.org/10.1136/archdischild-2017-312710] [PMID: 28588126]
[9]
Hamrick SEG, Miller SP, Leonard C, et al. Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. J Pediatr 2004; 145(5): 593-9.
[http://dx.doi.org/10.1016/j.jpeds.2004.05.042] [PMID: 15520756]
[10]
Ramenghi LA, Fumagalli M, Groppo M, et al. Germinal matrix hemorrhage: intraventricular hemorrhage in very-low-birth-weight infants: the independent role of inherited thrombophilia. Stroke 2011; 42(7): 1889-93.
[http://dx.doi.org/10.1161/STROKEAHA.110.590455] [PMID: 21597013]
[11]
Parodi A, Rossi A, Severino M, et al. Accuracy of ultrasound in assessing cerebellar haemorrhages in very low birthweight babies. Arch Dis Child Fetal Neonatal Ed 2015; 100(4): F289-92.
[http://dx.doi.org/10.1136/archdischild-2014-307176] [PMID: 25637005]
[12]
Parodi A, Morana G, Severino MS, et al. Low-grade intraventricular hemorrhage: is ultrasound good enough? J Matern Fetal Neonatal Med 2015; 28(Suppl. 1): 2261-4.
[http://dx.doi.org/10.3109/14767058.2013.796162] [PMID: 23968243]
[13]
Tortora D, Martinetti C, Severino M, et al. The effects of mild germinal matrix-intraventricular haemorrhage on the developmental white matter microstructure of preterm neonates: a DTI study. Eur Radiol 2018; 28(3): 1157-66.
[http://dx.doi.org/10.1007/s00330-017-5060-0] [PMID: 28956133]
[14]
Tortora D, Severino M, Sedlacik J, et al. Quantitative susceptibility map analysis in preterm neonates with germinal matrix-intraventricular hemorrhage. J Magn Reson Imaging 2018; 48(5): 1199-207.
[http://dx.doi.org/10.1002/jmri.26163] [PMID: 29746715]
[15]
Boswinkel V, Steggerda SJ, Fumagalli M, et al. The CHOPIn Study: A multicenter study on cerebellar hemorrhage and outcome in preterm infants. Cerebellum 2019; 18(6): 989-98.
[http://dx.doi.org/10.1007/s12311-019-01053-1] [PMID: 31250213]
[16]
Ley D, Romantsik O, Vallius S, et al. High presence of extracellular hemoglobin in the periventricular white matter following preterm intraventricular hemorrhage. Front Physiol 2016; 7: 330.
[http://dx.doi.org/10.3389/fphys.2016.00330] [PMID: 27536248]
[17]
Guo T, Duerden EG, Adams E, et al. Quantitative assessment of white matter injury in preterm neonates: Association with outcomes. Neurology 2017; 88(7): 614-22.
[http://dx.doi.org/10.1212/WNL.0000000000003606] [PMID: 28100727]
[18]
McNamara NB, Miron VE. Microglia in developing white matter and perinatal brain injury. Neurosci Lett 2020; 714: 134539.
[http://dx.doi.org/10.1016/j.neulet.2019.134539] [PMID: 31614181]
[19]
de Vries LS, Benders MJNL, Groenendaal F. Progress in neonatal neurology with a focus on neuroimaging in the preterm infant. Neuropediatrics 2015; 46(4): 234-41.
[http://dx.doi.org/10.1055/s-0035-1554102] [PMID: 26121069]
[20]
Morgillo D, Morgillo-Mitchell J, Fontanta M, et al. Outcome of extremely low gestational age newborns (ELGANs) following a pro-active treatment approach: A Swiss single centre experience over 10 years. Swiss Med Wkly 2014; 144: w14014.
[http://dx.doi.org/10.4414/smw.2014.14014] [PMID: 25255015]
[21]
Marseglia L, D’Angelo G, Manti S, et al. Oxidative stress-mediated aging during the fetal and perinatal periods. Oxid Med Cell Longev 2014; 2014: 358375.
[http://dx.doi.org/10.1155/2014/358375] [PMID: 25202436]
[22]
Back SA, Rivkees SA. Emerging concepts in periventricular white matter injury. Semin Perinatol 2004; 28(6): 405-14.
[http://dx.doi.org/10.1053/j.semperi.2004.10.010] [PMID: 15693397]
[23]
Cornette LG, Tanner SF, Ramenghi LA, et al. Magnetic resonance imaging of the infant brain: ANatomical characteristics and clinical significance of punctate lesions. Arch Dis Child Fetal Neonatal Ed 2002; 86(3): F171-7.
[http://dx.doi.org/10.1136/fn.86.3.f171] [PMID: 11978747]
[24]
Bassi L, Chew A, Merchant N, et al. Diffusion tensor imaging in preterm infants with punctate white matter lesions. Pediatr Res 2011; 69(6): 561-6.
[http://dx.doi.org/10.1203/PDR.0b013e3182182836] [PMID: 21386750]
[25]
Tusor N, Benders MJ, Counsell SJ, et al. Punctate white matter lesions associated with altered brain development and adverse motor outcome in preterm infants. Sci Rep 2017; 7(1): 13250.
[http://dx.doi.org/10.1038/s41598-017-13753-x] [PMID: 29038505]
[26]
Wagenaar N, Chau V, Groenendaal F, et al. Clinical risk factors for punctate white matter lesions on early magnetic resonance imaging in preterm newborns. J Pediatr 2017; 182: 34-40.e1.
[http://dx.doi.org/10.1016/j.jpeds.2016.11.073] [PMID: 28063691]
[27]
Elitt CM, Rosenberg PA. The challenge of understanding cerebral white matter injury in the premature infant. Neuroscience 2014; 276: 216-38.
[http://dx.doi.org/10.1016/j.neuroscience.2014.04.038] [PMID: 24838063]
[28]
Perrone S, Tataranno LM, Stazzoni G, Ramenghi L, Buonocore G. Brain susceptibility to oxidative stress in the perinatal period. J Matern Fetal Neonatal Med 2015; 28(Suppl. 1): 2291-5.
[http://dx.doi.org/10.3109/14767058.2013.796170] [PMID: 23968388]
[29]
Tataranno ML, Perrone S, Buonocore G. Plasma biomarkers of oxidative stress in neonatal brain injury. Clin Perinatol 2015; 42(3): 529-39.
[http://dx.doi.org/10.1016/j.clp.2015.04.011] [PMID: 26250915]
[30]
Parodi A, Malova M, Cardiello V, et al. Punctate white matter lesions of preterm infants: Risk factor analysis. Eur J Paediatr Neurol 2019; 23(5): 733-9.
[http://dx.doi.org/10.1016/j.ejpn.2019.06.003] [PMID: 31307922]
[31]
Perrone S, Laschi E, Buonocore G. Biomarkers of oxidative stress in the fetus and in the newborn. Free Radic Biol Med 2019; 142: 23-31.
[http://dx.doi.org/10.1016/j.freeradbiomed.2019.03.034] [PMID: 30954545]
[32]
Perrone S, Laschi E, Buonocore G. Oxidative stress biomarkers in the perinatal period: Diagnostic and prognostic value. Semin Fetal Neonatal Med 2020; 25(2): 101087.
[http://dx.doi.org/10.1016/j.siny.2020.101087] [PMID: 32008959]
[33]
Bruschi M, Santucci L, Petretto A, et al. Association between maternal omega-3 polyunsaturated fatty acids supplementation and preterm delivery: A proteomic study. FASEB J 2020; 34(5): 6322-34.
[http://dx.doi.org/10.1096/fj.201900738RR] [PMID: 32162735]
[34]
Panfoli I, Cassanello M, Bruschettini M, et al. Why do premature newborn infants display elevated blood adenosine levels? Med Hypotheses 2016; 90: 53-6.
[http://dx.doi.org/10.1016/j.mehy.2016.03.007] [PMID: 27063086]
[35]
Gholinejad M, Jafari Anarkooli I, Taromchi A, Abdanipour A. Adenosine decreases oxidative stress and protects H2O2-treated neural stem cells against apoptosis through decreasing Mst1 expression. Biomed Rep 2018; 8(5): 439-46.
[http://dx.doi.org/10.3892/br.2018.1083] [PMID: 29732147]
[36]
Stevens B, Porta S, Haak LL, Gallo V, Fields RD. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 2002; 36(5): 855-68.
[http://dx.doi.org/10.1016/s0896-6273(02)01067-x] [PMID: 12467589]
[37]
Rivkees SA, Wendler CC. Adverse and protective influences of adenosine on the newborn and embryo: Implications for preterm white matter injury and embryo protection. Pediatr Res 2011; 69(4): 271-8.
[http://dx.doi.org/10.1203/PDR.0b013e31820efbcf] [PMID: 21228731]
[38]
Antonioli L, Blandizzi C, Pacher P, Haskó G. Immunity, inflammation and cancer: A leading role for adenosine. Nat Rev Cancer 2013; 13(12): 842-57.
[http://dx.doi.org/10.1038/nrc3613] [PMID: 24226193]
[39]
Buonocore G, Perrone S, Bracci R. Free radicals and brain damage in the newborn. Biol Neonate 2001; 79(3-4): 180-6.
[http://dx.doi.org/10.1159/000047088] [PMID: 11275648]
[40]
Kaindl AM, Favrais G, Gressens P. Molecular mechanisms involved in injury to the preterm brain. J Child Neurol 2009; 24(9): 1112-8.
[http://dx.doi.org/10.1177/0883073809337920] [PMID: 19605776]
[41]
Azzari C, la Marca G, Resti M. Neonatal screening for severe combined immunodeficiency caused by an adenosine deaminase defect: A reliable and inexpensive method using tandem mass spectrometry. J Allergy Clin Immunol 2011; 127(6): 1394-9.
[http://dx.doi.org/10.1016/j.jaci.2011.03.040] [PMID: 21624616]
[42]
la Marca G. Mass spectrometry in clinical chemistry: the case of newborn screening. J Pharm Biomed Anal 2014; 101: 174-82.
[http://dx.doi.org/10.1016/j.jpba.2014.03.047] [PMID: 24844843]
[43]
Colella M, Zinni M, Pansiot J, et al. Modulation of microglial activation by adenosine A2a receptor in animal models of perinatal brain injury. Front Neurol 2018; 9: 605.
[http://dx.doi.org/10.3389/fneur.2018.00605] [PMID: 30254599]
[44]
De Vries LS, Groenendaal F, van Haastert IC, Eken P, Rademaker KJ, Meiners LC. Asymmetrical myelination of the posterior limb of the internal capsule in infants with periventricular haemorrhagic infarction: an early predictor of hemiplegia. Neuropediatrics 1999; 30(6): 314-9.
[http://dx.doi.org/10.1055/s-2007-973511] [PMID: 10706026]
[45]
Loureiro B, Martinez-Biarge M, Foti F, Papadaki M, Cowan FM, Wusthoff CJ. MRI patterns of brain injury and neurodevelopmental outcomes in neonates with severe anaemia at birth. Early Hum Dev 2017; 105: 17-22.
[http://dx.doi.org/10.1016/j.earlhumdev.2017.01.001] [PMID: 28107673]
[46]
Griffiths R. Griffiths Mental Development Scales - Revised: Birth to 2 years. Oxford: The Text Agency 1996.
[47]
Bruschi M, Petretto A, Caicci F, et al. Proteome of Bovine Mitochondria and rod outer segment disks: Commonalities and differences. J Proteome Res 2018; 17(2): 918-25.
[http://dx.doi.org/10.1021/acs.jproteome.7b00741] [PMID: 29299929]
[48]
Schwiebert EM, Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim Biophys Acta 2003; 1615(1-2): 7-32.
[http://dx.doi.org/10.1016/S0005-2736(03)00210-4] [PMID: 12948585]
[49]
Fredholm BB. Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ 2007; 14(7): 1315-23.
[http://dx.doi.org/10.1038/sj.cdd.4402132] [PMID: 17396131]
[50]
Baldwin SA, Beal PR, Yao SYM, King AE, Cass CE, Young JD. The equilibrative nucleoside transporter family, SLC29. Pflugers Arch 2004; 447(5): 735-43.
[http://dx.doi.org/10.1007/s00424-003-1103-2] [PMID: 12838422]
[51]
Pettengill M, Robson S, Tresenriter M, et al. Soluble ecto-5′-nucleotidase (5′-NT), alkaline phosphatase, and adenosine deaminase (ADA1) activities in neonatal blood favor elevated extracellular adenosine. J Biol Chem 2013; 288(38): 27315-26.
[http://dx.doi.org/10.1074/jbc.M113.484212] [PMID: 23897810]
[52]
Nguyen MD, Ross AE, Ryals M, Lee ST, Venton BJ. Clearance of rapid adenosine release is regulated by nucleoside transporters and metabolism. Pharmacol Res Perspect 2015; 3(6): e00189.
[http://dx.doi.org/10.1002/prp2.189] [PMID: 27022463]
[53]
Cunha RA. How does adenosine control neuronal dysfunction and neurodegeneration? J Neurochem 2016; 139(6): 1019-55.
[http://dx.doi.org/10.1111/jnc.13724] [PMID: 27365148]
[54]
Back SA, Rosenberg PA. Pathophysiology of glia in perinatal white matter injury. Glia 2014; 62(11): 1790-815.
[http://dx.doi.org/10.1002/glia.22658] [PMID: 24687630]
[55]
Panfoli I, Candiano G, Malova M, et al. Oxidative stress as a primary risk factor for brain damage in preterm newborns. Front Pediatr 2018; 6: 369.
[http://dx.doi.org/10.3389/fped.2018.00369] [PMID: 30555809]
[56]
Perrone S, Negro S, Tataranno ML, Buonocore G. Oxidative stress and antioxidant strategies in newborns. J Matern Neonatal Med 2010; 23(Suppl. 3): 63-5.
[http://dx.doi.org/10.3109/14767058.2010.509940] [PMID: 20807155]
[57]
Di Virgilio F, Ceruti S, Bramanti P, Abbracchio MP. Purinergic signalling in inflammation of the central nervous system. Trends Neurosci 2009; 32(2): 79-87.
[http://dx.doi.org/10.1016/j.tins.2008.11.003] [PMID: 19135728]
[58]
Hagberg H, Mallard C, Ferriero DM, et al. The role of inflammation in perinatal brain injury. Nat Rev Neurol 2015; 11(4): 192-208.
[http://dx.doi.org/10.1038/nrneurol.2015.13] [PMID: 25686754]
[59]
Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA. The developing oligodendrocyte: Key cellular target in brain injury in the premature infant. Int J Dev Neurosci 2011; 29(4): 423-40.
[http://dx.doi.org/10.1016/j.ijdevneu.2011.02.012] [PMID: 21382469]
[60]
de Vries LS, Regev R, Dubowitz LM. Late onset cystic leucomalacia. Arch Dis Child 1986; 61(3): 298-9.
[http://dx.doi.org/10.1136/adc.61.3.298] [PMID: 3516079]
[61]
Khwaja O, Volpe JJ. Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 2008; 93(2): F153-61.
[http://dx.doi.org/10.1136/adc.2006.108837] [PMID: 18296574]
[62]
Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001; 21(4): 1302-12.
[http://dx.doi.org/10.1523/JNEUROSCI.21-04-01302.2001] [PMID: 11160401]
[63]
Back SA, Miller SP. Brain injury in premature neonates: A primary cerebral dysmaturation disorder? Ann Neurol 2014; 75(4): 469-86.
[http://dx.doi.org/10.1002/ana.24132] [PMID: 24615937]
[64]
Volpe JJ. Systemic inflammation, oligodendroglial maturation, and the encephalopathy of prematurity. Ann Neurol 2011; 70(4): 525-9.
[http://dx.doi.org/10.1002/ana.22533] [PMID: 22028217]
[65]
Ravera S, Bartolucci M, Cuccarolo P, et al. Oxidative stress in myelin sheath: The other face of the extramitochondrial oxidative phosphorylation ability. Free Radic Res 2015; 49(9): 1156-64.
[http://dx.doi.org/10.3109/10715762.2015.1050962] [PMID: 25971447]
[66]
Ravera S, Nobbio L, Visigalli D, et al. Oxydative phosphorylation in sciatic nerve myelin and its impairment in a model of dysmyelinating peripheral neuropathy. J Neurochem 2013; 126(1): 82-92.
[http://dx.doi.org/10.1111/jnc.12253] [PMID: 23578247]
[67]
Ravera S, Bartolucci M, Garbati P, et al. Evaluation of the acquisition of the aerobic metabolic capacity by myelin, during its development. Mol Neurobiol 2016; 53(10): 7048-56.
[http://dx.doi.org/10.1007/s12035-015-9575-6] [PMID: 26676569]
[68]
Corriden R, Insel PA. Basal release of ATP: An autocrine-paracrine mechanism for cell regulation. Sci Signal 2010; 3(104): re1.
[http://dx.doi.org/10.1126/scisignal.3104re1] [PMID: 20068232]
[69]
Glass HC, Fujimoto S, Ceppi-Cozzio C, et al. White-matter injury is associated with impaired gaze in premature infants. Pediatr Neurol 2008; 38(1): 10-5.
[http://dx.doi.org/10.1016/j.pediatrneurol.2007.08.019] [PMID: 18054686]
[70]
Kadri H, Mawla AA, Kazah J. The incidence, timing, and predisposing factors of germinal matrix and intraventricular hemorrhage (GMH/IVH) in preterm neonates. Childs Nerv Syst 2006; 22(9): 1086-90.
[http://dx.doi.org/10.1007/s00381-006-0050-6] [PMID: 16636880]
[71]
Bruschi M, Bartolucci M, Petretto A, et al. Differential expression of the five redox complexes in the retinal mitochondria or rod outer segment disks is consistent with their different functionality. FASEB Bioadv 2020; 2(5): 315-24.
[http://dx.doi.org/10.1096/fba.2019-00093] [PMID: 32395704]
[72]
Ravera S, Bartolucci M, Adriano E, et al. Support of nerve conduction by respiring myelin sheath: Role of connexons. Mol Neurobiol 2016; 53(4): 2468-79.
[http://dx.doi.org/10.1007/s12035-015-9216-0] [PMID: 26033217]
[73]
Calzia D, Degan P, Caicci F, et al. Modulation of the rod outer segment aerobic metabolism diminishes the production of radicals due to light absorption. Free Radic Biol Med 2018; 117: 110-8.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.01.029] [PMID: 29378336]
[74]
Back SA. Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment Retard Dev Disabil Res Rev 2006; 12(2): 129-40.
[http://dx.doi.org/10.1002/mrdd.20107] [PMID: 16807910]
[75]
De Rooy L, Hamdallah H, Dyall SC. Extremely preterm infants receiving standard care receive very low levels of arachidonic and docosahexaenoic acids. Clin Nutr 2017; 36(6): 1593-600.
[http://dx.doi.org/10.1016/j.clnu.2016.09.033] [PMID: 27756480]
[76]
Kar S, Wong M, Rogozinska E, Thangaratinam S. Effects of omega-3 fatty acids in prevention of early preterm delivery: A systematic review and meta-analysis of randomized studies. Eur J Obstet Gynecol Reprod Biol 2016; 198: 40-6.
[http://dx.doi.org/10.1016/J.EJOGRB.2015.11.033] [PMID: 26773247]
[77]
Lassmann H. Pathology and disease mechanisms in different stages of multiple sclerosis. J Neurol Sci 2013; 333(1-2): 1-4.
[http://dx.doi.org/10.1016/J.JNS.2013.05.010] [PMID: 23735777]
[78]
Kuban K, Sanocka U, Leviton A, et al. White matter disorders of prematurity: Association with intraventricular hemorrhage and ventriculomegaly. J Pediatr 1999; 134(5): 539-46.
[http://dx.doi.org/10.1016/s0022-3476(99)70237-4] [PMID: 10228286]
[79]
Penn AA, Gressens P, Fleiss B, Back SA, Gallo V. Controversies in preterm brain injury Neurobiol Dis 2016; 92(Pt A): 90-101.
[http://dx.doi.org/10.1016/j.nbd.2015.10.012] [PMID: 26477300]
[80]
Linsell L, Malouf R, Morris J, Kurinczuk JJ, Marlow N. Risk factor models for neurodevelopmental outcomes in children born very preterm or with very low birth weight: A systematic review of methodology and reporting. Am J Epidemiol 2017; 185(7): 601-12.
[http://dx.doi.org/10.1093/aje/kww135] [PMID: 28338817]
[81]
Wood R, Bassett K, Foerster V, Spry C, Tong L. 1.5 Tesla magnetic resonance imaging scanners compared with 3.0 tesla magnetic resonance imaging scanners: systematic review of clinical effectiveness. CADTH Technol Overv 2012; 2(2): e2201.
[PMID: 23002376]
[82]
la Marca G, Canessa C, Giocaliere E, et al. Diagnosis of immunodeficiency caused by a purine nucleoside phosphorylase defect by using tandem mass spectrometry on dried blood spots. J Allergy Clin Immunol 2014; 134(1): 155-9.
[http://dx.doi.org/10.1016/j.jaci.2014.01.040] [PMID: 24767876]
[83]
Carman AJ, Mills JH, Krenz A, Kim D-G, Bynoe MS. Adenosine receptor signaling modulates permeability of the blood-brain barrier. J Neurosci 2011; 31(37): 13272-80.
[http://dx.doi.org/10.1523/JNEUROSCI.3337-11.2011] [PMID: 21917810]
[84]
Malhotra A, Castillo-Melendez M, Allison BJ, et al. Neuropathology as a consequence of neonatal ventilation in premature growth-restricted lambs. Am J Physiol Regul Integr Comp Physiol 2018; 315(6): R1183-94.
[http://dx.doi.org/10.1152/ajpregu.00171.2018] [PMID: 30230932]
[85]
Stewart A, Tekes A, Huisman TAGM, et al. Glial fibrillary acidic protein as a biomarker for periventricular white matter injury. Am J Obstet Gynecol 2013; 209(1): 27.e1-7.
[http://dx.doi.org/10.1016/j.ajog.2013.02.049] [PMID: 23467054]

© 2024 Bentham Science Publishers | Privacy Policy