Interleukin-1 receptor blockade in perinatal brain injury

Frontiers in Pediatrics

Volumn 2, Issue OCT, 2014, Pages

  Rosenzweig, Jason M ^a   Lei, Jun ^a   Burd, Irina ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

IL 1; IL 1beta; Kineret; Perinatal brain injury; RIL RA

Indexed keywords

EID: 84938983161     PISSN: None     EISSN: 22962360     Source Type: Journal    
DOI: 10.3389/fped.2014.00108     Document Type: Review

References (97)

1. Beeson PB. Temperature-elevating effect of a substance obtained from polymorphonuclear leucocytes. J Clin Invest (1948) 27(4):524
2. Atkins E. Pathogenesis of fever. Physiol Rev (1960) 40:580-646
3. Dinarello CA. Interleukin-1 and interleukin-1 antagonism. Blood (1991) 77(8):1627-52
4. Sims JE, Smith DE. The IL-1 family: regulators of immunity. Nat Rev Immunol (2010) 10(2):89-102. doi:10.1038/nri2691
5. Dinarello CA, Simon A, van der Meer JW. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov (2012) 11(8):633-52. doi:10.1038/nrd3800
6. Garlanda C, Dinarello CA, Mantovani A. The interleukin-1 family: back to the future. Immunity (2013) 39(6):1003-18. doi:10.1016/j.immuni.2013.11.010
7. Girard S, Sebire H, Brochu ME, Briota S, Sarret P, Sebire G. Postnatal administration of IL-1Ra exerts neuroprotective effects following perinatal inflammation and/or hypoxic-ischemic injuries. Brain Behav Immun (2012) 26(8):1331-9. doi:10.1016/j.bbi.2012.09.001
8. Leitner K, Al Shammary M, McLane M, Johnston MV, Elovitz MA, Burd I. IL-1 receptor blockade prevents fetal cortical brain injury but not preterm birth in a mouse model of inflammation-induced preterm birth and perinatal brain injury. Am J Reprod Immunol (2014) 71(5):418-26. doi:10.1111/aji.12216
9. Dunne A, O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE (2003) 2003(171):re3. doi:10.1126/stke.2003.171.re3
10. Watters TM, Kenny EF, O'Neill LA. Structure, function and regulation of the Toll/IL-1 receptor adaptor proteins. Immunol Cell Biol (2007) 85(6):411-9. doi:10.1038/sj.icb.7100095
11. Casanova JL, Abel L, Quintana-Murci L. Human TLRs and IL-1Rs in host defense: natural insights from evolutionary, epidemiological, and clinical genetics. Annu Rev Immunol (2011) 29:447-91. doi:10.1146/annurev-immunol-030409-101335
12. McMahan CJ, Slack JL, Mosley B, Cosman D, Lupton SD, Brunton LL, et al. A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J (1991) 10(10):2821-32
13. Hannum CH, Wilcox CJ, Arend WP, Joslin FG, Dripps DJ, Heimdal PL, et al. Interleukin-1 receptor antagonist activity of a human interleukin-1 inhibitor. Nature (1990) 343(6256):336-40. doi:10.1038/343336a0
14. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, Lee WP, et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature (2004) 430(6996):213-8. doi:10.1038/nature02664
15. Tschopp J, Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat Rev Immunol (2010) 10(3):210-5. doi:10.1038/nri2725
16. Dinarello CA. Anti-inflammatory agents: present and future. Cell (2010) 140(6):935-50. doi:10.1016/j.cell.2010.02.043
17. Aksentijevich I, Masters SL, Ferguson PJ, Dancey P, Frenkel J, van Royen-Kerkhoff A, et al. An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N Engl J Med (2009) 360(23):2426-37. doi:10.1056/NEJMoa0807865
18. Gabay C, Palmer G. Mutations in the IL1RN locus lead to autoinflammation. Nat Rev Rheumatol (2009) 5(9):480-2. doi:10.1038/nrrheum.2009.177
19. Reddy S, Jia S, Geoffrey R, Lorier R, Suchi M, Broeckel U, et al. An autoinflammatory disease due to homozygous deletion of the IL1RN locus. N Engl J Med (2009) 360(23):2438-44. doi:10.1056/NEJMoa0809568
20. Horai R, Asano M, Sudo K, Kanuka H, Suzuki M, Nishihara M, et al. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J Exp Med (1998) 187(9):1463-75. doi:10.1084/jem.187.9.1463
21. Horai R, Saijo S, Tanioka H, Nakae S, Sudo K, Okahara A, et al. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J Exp Med (2000) 191(2):313-20. doi:10.1084/jem.191.2.313
22. Nicklin MJ, Hughes DE, Barton JL, Ure JM, Duff GW. Arterial inflammation in mice lacking the interleukin 1 receptor antagonist gene. J Exp Med (2000) 191(2):303-12. doi:10.1084/jem.191.2.303
23. Banks WA, Kastin AJ, Broadwell RD. Passage of cytokines across the blood-brain barrier. Neuroimmunomodulation (1995) 2(4):241-8. doi:10.1159/000096887
24. Greenhalgh AD, Galea J, Denes A, Tyrrell PJ, Rothwell NJ. Rapid brain penetration of interleukin-1 receptor antagonist in rat cerebral ischaemia: pharmacokinetics, distribution, protection. Br J Pharmacol (2010) 160(1):153-9. doi:10.1111/j.1476-5381.2010.00684.x
25. Galea J, Ogungbenro K, Hulme S, Greenhalgh A, Aarons L, Scarth S, et al. Intravenous anakinra can achieve experimentally effective concentrations in the central nervous system within a therapeutic time window: results of a dose-ranging study. J Cereb Blood Flow Metab (2011) 31(2):439-47. doi:10.1038/jcbfm.2010.103
26. Amash A, Holcberg G, Sapir O, Huleihel M. Placental secretion of interleukin-1 and interleukin-1 receptor antagonist in preeclampsia: effect of magnesium sulfate. J Interferon Cytokine Res (2012) 32(9):432-41. doi:10.1089/jir.2012.0013
27. Reisenberger K, Egarter C, Vogl S, Sternberger B, Kiss H, Husslein P. The transfer of interleukin-8 across the human placenta perfused in vitro. Obstet Gynecol (1996) 87(4):613-6. doi:10.1016/0029-7844(95)00473-4
28. Zaretsky MV, Alexander JM, Byrd W, Bawdon RE. Transfer of inflammatory cytokines across the placenta. Obstet Gynecol (2004) 103(3):546-50. doi:10.1097/01.AOG.0000114980.40445.83
29. Aaltonen R, Heikkinen T, Hakala K, Laine K, Alanen A. Transfer of proinflammatory cytokines across term placenta. Obstet Gynecol (2005) 106(4):802-7. doi:10.1097/01.AOG.0000178750.84837.ed
30. Bresnihan B, Alvaro-Gracia JM, Cobby M, Doherty M, Domljan Z, Emery P, et al. Treatment of rheumatoid arthritis with recombinant human interleukin-1 receptor antagonist. Arthritis Rheum (1998) 41(12):2196-204. doi:10.1002/1529-0131(199812)41:12<2196::AID-ART15>3.3.CO;2-U
31. Cohen S, Hurd E, Cush J, Schiff M, Weinblatt ME, Moreland LW, et al. Treatment of rheumatoid arthritis with anakinra, a recombinant human interleukin-1 receptor antagonist, in combination with methotrexate: results of a twenty-four-week, multicenter, randomized, double-blind, placebo-controlled trial. Arthritis Rheum (2002) 46(3):614-24. doi:10.1002/art.10103
32. Fleischmann RM, Schechtman J, Bennett R, Handel ML, Burmester GR, Tesser J, et al. Anakinra, a recombinant human interleukin-1 receptor antagonist (r-metHuIL-1ra), in patients with rheumatoid arthritis: a large, international, multicenter, placebo-controlled trial. Arthritis Rheum (2003) 48(4):927-34. doi:10.1002/art.10870
33. Cohen SB, Moreland LW, Cush JJ, Greenwald MW, Block S, Shergy WJ, et al. A multicentre, double blind, randomised, placebo controlled trial of anakinra (Kineret), a recombinant interleukin 1 receptor antagonist, in patients with rheumatoid arthritis treated with background methotrexate. Ann Rheum Dis (2004) 63(9):1062-8. doi:10.1136/ard.2003.016014
34. Genovese MC, Cohen S, Moreland L, Lium D, Robbins S, Newmark R, et al. Combination therapy with etanercept and anakinra in the treatment of patients with rheumatoid arthritis who have been treated unsuccessfully with methotrexate. Arthritis Rheum (2004) 50(5):1412-9. doi:10.1002/art.20221
35. Mertens M, Singh JA. Anakinra for rheumatoid arthritis. Cochrane Database Syst Rev (2009) 1:CD005121. doi:10.1002/14651858.CD005121.pub3
36. Van den Broeck C, Himpens E, Vanhaesebrouck P, Calders P, Oostra A. Influence of gestational age on the type of brain injury and neuromotor outcome in high-risk neonates. Eur J Pediatr (2008) 167(9):1005-9. doi:10.1007/s00431-007-0629-2
37. Schendel DE, Schuchat A, Thorsen P. Public health issues related to infection in pregnancy and cerebral palsy. Ment Retard Dev Disabil Res Rev (2002) 8(1):39-45. doi:10.1002/mrdd.10011
38. Bracci R, Buonocore G. Chorioamnionitis: a risk factor for fetal and neonatal morbidity. Biol Neonate (2003) 83(2):85-96. doi:10.1159/000067956
39. McLean C, Ferriero D. Mechanisms of hypoxic-ischemic injury in the term infant. Semin Perinatol (2004) 28(6):425-32. doi:10.1053/j.semperi.2004.10.005
40. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun (2010) 24(6):881-97. doi:10.1016/j.bbi.2010.03.005
41. Arrode-Bruses G, Bruses JL. Maternal immune activation by poly I:C induces expression of cytokines IL-1beta and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain. J Neuroinflammation (2012) 9:83. doi:10.1186/1742-2094-9-83
42. Hagberg H, Gressens P, Mallard C. Inflammation during fetal and neonatal life: implications for neurologic and neuropsychiatric disease in children and adults. Ann Neurol (2012) 71(4):444-57. doi:10.1002/ana.22620
43. Meyer U. Developmental neuroinflammation and schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry (2013) 42:20-34. doi:10.1016/j.pnpbp.2011.11.003
44. Allan SM, Pinteaux E. The interleukin-1 system: an attractive and viable therapeutic target in neurodegenerative disease. Curr Drug Targets CNS Neurol Disord (2003) 2(5):293-302. doi:10.2174/1568007033482742
45. Rothwell N. Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential. Brain Behav Immun (2003) 17(3):152-7. doi:10.1016/S0889-1591(02)00098-3
46. Cai Z, Lin S, Pang Y, Rhodes PG. Brain injury induced by intracerebral injection of interleukin-1beta and tumor necrosis factor-alpha in the neonatal rat. Pediatr Res (2004) 56(3):377-84. doi:10.1203/01.PDR.0000134249.92944.14
47. Allan SM, Tyrrell PJ, Rothwell NJ. Interleukin-1 and neuronal injury. Nat Rev Immunol (2005) 5(8):629-40. doi:10.1038/nri1664
48. Thornton P, Pinteaux E, Gibson RM, Allan SM, Rothwell NJ. Interleukin-1-induced neurotoxicity is mediated by glia and requires caspase activation and free radical release. J Neurochem (2006) 98(1):258-66. doi:10.1111/j.1471-4159.2006.03872.x
49. Denes A, Pinteaux E, Rothwell NJ, Allan SM. Interleukin-1 and stroke: biomarker, harbinger of damage, and therapeutic target. Cerebrovasc Dis (2011) 32(6):517-27. doi:10.1159/000332205
50. Savard A, Lavoie K, Brochu ME, Grbic D, Lepage M, Gris D, et al. Involvement of neuronal IL-1beta in acquired brain lesions in a rat model of neonatal encephalopathy. J Neuroinflammation (2013) 10:110. doi:10.1186/1742-2094-10-110
51. Green HF, Treacy E, Keohane AK, Sullivan AM, O'Keeffe GW, Nolan YM. A role for interleukin-1beta in determining the lineage fate of embryonic rat hippocampal neural precursor cells. Mol Cell Neurosci (2012) 49(3):311-21. doi:10.1016/j.mcn.2012.01.001
52. Fatemi SH, Emamian ES, Sidwell RW, Kist DA, Stary JM, Earle JA, et al. Human influenza viral infection in utero alters glial fibrillary acidic protein immunoreactivity in the developing brains of neonatal mice. Mol Psychiatry (2002) 7(6):633-40. doi:10.1038/sj.mp.4001046
53. Aden U, Favrais G, Plaisant F, Winerdal M, Felderhoff-Mueser U, Lampa J, et al. Systemic inflammation sensitizes the neonatal brain to excitotoxicity through a pro-/anti-inflammatory imbalance: key role of TNFalpha pathway and protection by etanercept. Brain Behav Immun (2010) 24(5):747-58. doi:10.1016/j.bbi.2009.10.010
54. Chang EY, Zhang J, Sullivan S, Newman R, Singh I. N-acetylcysteine attenuates the maternal and fetal proinflammatory response to intrauterine LPS injection in an animal model for preterm birth and brain injury. J Matern Fetal Neonatal Med (2011) 24(5):732-40. doi:10.3109/14767058.2010.528089
55. Burd I, Balakrishnan B, Kannan S. Models of fetal brain injury, intrauterine inflammation, and preterm birth. Am J Reprod Immunol (2012) 67(4):287-94. doi:10.1111/j.1600-0897.2012.01110.x
56. Dada T, Rosenzweig JM, Al Shammary M, Firdaus W, Al Rebh S, Borbiev T, et al. Mouse model of intrauterine inflammation: sex-specific differences in long-term neurologic and immune sequelae. Brain Behav Immun (2014) 38:142-50. doi:10.1016/j.bbi.2014.01.014
57. Bell MJ, Hallenbeck JM. Effects of intrauterine inflammation on developing rat brain. J Neurosci Res (2002) 70(4):570-9. doi:10.1002/jnr.10423
58. Auvin S, Shin D, Mazarati A, Nakagawa J, Miyamoto J, Sankar R. Inflammation exacerbates seizure-induced injury in the immature brain. Epilepsia (2007) 48(Suppl 5):27-34. doi:10.1111/j.1528-1167.2007.01239.x
59. Beloosesky R, Ginsberg Y, Khatib N, Maravi N, Ross MG, Itskovitz-Eldor J, et al. Prophylactic maternal N-acetylcysteine in rats prevents maternal inflammation-induced offspring cerebral injury shown on magnetic resonance imaging. Am J Obstet Gynecol (2013) 208(3):e211-6. doi:10.1016/j.ajog.2013.01.023
60. Hagberg H, Peebles D, Mallard C. Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev (2002) 8(1):30-8. doi:10.1002/mrdd.10020
61. Kannan S, Saadani-Makki F, Muzik O, Chakraborty P, Mangner TJ, Janisse J, et al. Microglial activation in perinatal rabbit brain induced by intrauterine inflammation: detection with 11C-(R)-PK11195 and small-animal PET. J Nucl Med (2007) 48(6):946-54. doi:10.2967/jnumed.106.038539
62. Young RS, Hernandez MJ, Yagel SK. Selective reduction of blood flow to white matter during hypotension in newborn dogs: a possible mechanism of periventricular leukomalacia. Ann Neurol (1982) 12(5):445-8. doi:10.1002/ana.410120506
63. Yawno T, Schuilwerve J, Moss TJ, Vosdoganes P, Westover AJ, Afandi E, et al. Human amnion epithelial cells reduce fetal brain injury in response to intrauterine inflammation. Dev Neurosci (2013) 35(2-3):272-82. doi:10.1159/000346683
64. Debillon T, Gras-Leguen C, Verielle V, Winer N, Caillon J, Roze JC, et al. Intrauterine infection induces programmed cell death in rabbit periventricular white matter. Pediatr Res (2000) 47(6):736-42. doi:10.1203/00006450-200006000-00009
65. Fan LW, Tien LT, Zheng B, Pang Y, Rhodes PG, Cai Z. Interleukin-1beta-induced brain injury and neurobehavioral dysfunctions in juvenile rats can be attenuated by alpha-phenyl-n-tert-butyl-nitrone. Neuroscience (2010) 168(1):240-52. doi:10.1016/j.neuroscience.2010.03.024
66. Shi L, Fatemi SH, Sidwell RW, Patterson PH. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci (2003) 23(1):297-302
67. Meyer U, Feldon J, Schedlowski M, Yee BK. Immunological stress at the maternal-foetal interface: a link between neurodevelopment and adult psychopathology. Brain Behav Immun (2006) 20(4):378-88. doi:10.1016/j.bbi.2005.11.003
68. Cai Z, Pan ZL, Pang Y, Evans OB, Rhodes PG. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res (2000) 47(1):64-72. doi:10.1203/00006450-200001000-00013
69. Burd I, Brown A, Gonzalez JM, Chai J, Elovitz MA. A mouse model of term chorioamnionitis: unraveling causes of adverse neurological outcomes. Reprod Sci (2011) 18(9):900-7. doi:10.1177/1933719111398498
70. Cai Z, Fan LW, Lin S, Pang Y, Rhodes PG. Intranasal administration of insulin-like growth factor-1 protects against lipopolysaccharide-induced injury in the developing rat brain. Neuroscience (2011) 194:195-207. doi:10.1016/j.neuroscience.2011.08.003
71. Hagan P, Barks JD, Yabut M, Davidson BL, Roessler B, Silverstein FS. Adenovirus-mediated over-expression of interleukin-1 receptor antagonist reduces susceptibility to excitotoxic brain injury in perinatal rats. Neuroscience (1996) 75(4):1033-45. doi:10.1016/0306-4522(96)00225-4
72. Ide CF, Scripter JL, Coltman BW, Dotson RS, Snyder DC, Jelaso A. Cellular and molecular correlates to plasticity during recovery from injury in the developing mammalian brain. Prog Brain Res (1996) 108:365-77. doi:10.1016/S0079-6123(08)62552-2
73. Scripter JL, Ko J, Kow K, Arimura A, Ide CF. Regulation by interleukin-1beta of formation of a line of delimiting astrocytes following prenatal trauma to the brain of the mouse. Exp Neurol (1997) 145(2 Pt 1):329-41. doi:10.1006/exnr.1997.6470
74. Yoon BH, Romero R, Jun JK, Park KH, Park JD, Ghezzi F, et al. Amniotic fluid cytokines (interleukin-6, tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-8) and the risk for the development of bronchopulmonary dysplasia. Am J Obstet Gynecol (1997) 177(4):825-30. doi:10.1016/S0002-9378(97)70276-X
75. Kadhim H, Tabarki B, De Prez C, Sebire G. Cytokine immunoreactivity in cortical and subcortical neurons in periventricular leukomalacia: are cytokines implicated in neuronal dysfunction in cerebral palsy? Acta Neuropathol (2003) 105(3):209-16. doi:10.1007/s00401-002-0633-6
76. Girard S, Sebire G, Kadhim H. Proinflammatory orientation of the interleukin 1 system and downstream induction of matrix metalloproteinase 9 in the pathophysiology of human perinatal white matter damage. J Neuropathol Exp Neurol (2010) 69(11):1116-29. doi:10.1097/NEN.0b013e3181f971e4
77. Rice JE III, Vannucci RC, Brierley JB. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol (1981) 9(2):131-41. doi:10.1002/ana.410090206
78. Comi AM, Johnston MV, Wilson MA. Immature mouse unilateral carotid ligation model of stroke. J Child Neurol (2005) 20(12):980-3. doi:10.1177/08830738050200120901
79. Johnston MV, Ferriero DM, Vannucci SJ, Hagberg H. Models of cerebral palsy: which ones are best? J Child Neurol (2005) 20(12):984-7. doi:10.1177/08830738050200091101
80. Falahati S, Breu M, Waickman AT, Phillips AW, Arauz EJ, Snyder S, et al. Ischemia-induced neuroinflammation is associated with disrupted development of oligodendrocyte progenitors in a model of periventricular leukomalacia. Dev Neurosci (2013) 35(2-3):182-96. doi:10.1159/000346682
81. Szaflarski J, Burtrum D, Silverstein FS. Cerebral hypoxia-ischemia stimulates cytokine gene expression in perinatal rats. Stroke (1995) 26(6):1093-100. doi:10.1161/01.STR.26.6.1093
82. Silverstein FS, Barks JD, Hagan P, Liu XH, Ivacko J, Szaflarski J. Cytokines and perinatal brain injury. Neurochem Int (1997) 30(4-5):375-83. doi:10.1016/S0197-0186(96)00072-1
83. Carlsson Y, Leverin AL, Hedtjarn M, Wang X, Mallard C, Hagberg H. Role of mixed lineage kinase inhibition in neonatal hypoxia-ischemia. Dev Neurosci (2009) 31(5):420-6. doi:10.1159/000232560
84. Park EM, Cho BP, Volpe BT, Cruz MO, Joh TH, Cho S. Ibuprofen protects ischemia-induced neuronal injury via up-regulating interleukin-1 receptor antagonist expression. Neuroscience (2005) 132(3):625-31. doi:10.1016/j.neuroscience.2005.01.021
85. Quiniou C, Kooli E, Joyal JS, Sapieha P, Sennlaub F, Lahaie I, et al. Interleukin-1 and ischemic brain injury in the newborn: development of a small molecule inhibitor of IL-1 receptor. Semin Perinatol (2008) 32(5):325-33. doi:10.1053/j.semperi.2008.07.001
86. Wang CH, Wang WT, Cheng SY, Hung WT, Wu TL, Hsueh CM. Leptin and interleukin-1beta modulate neuronal glutamate release and protect against glucose-oxygen-serum deprivation. Curr Neurovasc Res (2010) 7(3):223-37. doi:10.2174/156720210791184925
87. Martin D, Chinookoswong N, Miller G. The interleukin-1 receptor antagonist (rhIL-1ra) protects against cerebral infarction in a rat model of hypoxia-ischemia. Exp Neurol (1994) 130(2):362-7. doi:10.1006/exnr.1994.1215
88. Hu X, Nesic-Taylor O, Qiu J, Rea HC, Fabian R, Rassin DK, et al. Activation of nuclear factor-kappaB signaling pathway by interleukin-1 after hypoxia/ischemia in neonatal rat hippocampus and cortex. J Neurochem (2005) 93(1):26-37. doi:10.1111/j.1471-4159.2004.02968.x
89. Campion GV, Lebsack ME, Lookabaugh J, Gordon G, Catalano M. Dose-range and dose-frequency study of recombinant human interleukin-1 receptor antagonist in patients with rheumatoid arthritis. The IL-1Ra Arthritis Study Group. Arthritis Rheum (1996) 39(7):1092-101. doi:10.1002/art.1780390704
90. Nuki G, Bresnihan B, Bear MB, McCabe D. Long-term safety and maintenance of clinical improvement following treatment with anakinra (recombinant human interleukin-1 receptor antagonist) in patients with rheumatoid arthritis: extension phase of a randomized, double-blind, placebo-controlled trial. Arthritis Rheum (2002) 46(11):2838-46. doi:10.1002/art.10578
91. Ferriero DM. Neonatal brain injury. N Engl J Med (2004) 351(19):1985-95. doi:10.1056/NEJMra041996
92. Pierrat V, Haouari N, Liska A, Thomas D, Subtil D, Truffert P. Prevalence, causes, and outcome at 2 years of age of newborn encephalopathy: population based study. Arch Dis Child Fetal Neonatal Ed (2005) 90(3):F257-61. doi:10.1136/adc.2003.047985
93. Graham EM, Ruis KA, Hartman AL, Northington FJ, Fox HE. A systematic review of the role of intrapartum hypoxia-ischemia in the causation of neonatal encephalopathy. Am J Obstet Gynecol (2008) 199(6):587-95. doi:10.1016/j.ajog.2008.06.094
94. D'Alton ME, Hankins GDV, Berkowitz RL, Bienstock J, Ghidini A, Goldsmith J, et al. Executive summary: neonatal encephalopathy and neurologic outcome, second edition. Report of the American College of Obstetricians and Gynecologists' task force on neonatal encephalopathy. Obstet Gynecol (2014) 123(4):896-901
95. Edwards AD, Brocklehurst P, Gunn AJ, Halliday H, Juszczak E, Levene M, et al. Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: synthesis and meta-analysis of trial data. BMJ (2010) 340:c363. doi:10.1136/bmj.c363
96. Fan X, van Bel F, van der Kooij MA, Heijnen CJ, Groenendaal F. Hypothermia and erythropoietin for neuroprotection after neonatal brain damage. Pediatr Res (2013) 73(1):18-23. doi:10.1038/pr.2012.139
97. Fang AY, Gonzalez FF, Sheldon RA, Ferriero DM. Effects of combination therapy using hypothermia and erythropoietin in a rat model of neonatal hypoxia-ischemia. Pediatr Res (2013) 73(1):12-7. doi:10.1038/pr.2012.138