Adaptive brain shut-down counteracts neuroinflammation in the near-term ovine fetus

Frontiers in Neurology

Volumn 5 JUN, Issue , 2014, Pages

  Xu, Alex ^a   Durosier, Lucien Daniel ^b   Ross G , Michael ^c   Hammond, Robert ^a   Richardson, Bryan S ^a   Frasch, Martin G ^b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

Acidemia; ECoG; EEG; Fetus; Hypoxia; Labor; Microglia; Sheep

Indexed keywords

ACIDOSIS; ADAPTIVE BRAIN SHUT DOWN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PH; ARTICLE; CARDIOVASCULAR RESPONSE; CELL ACTIVATION; CELL COUNT; CELL SYNCHRONIZATION; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ELECTROCORTICOGRAPHY; EVOKED CORTICAL RESPONSE; FETUS; GRAY MATTER; HYPOXIA; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PATHOPHYSIOLOGY; REPETITIVE UMBILICAL CORD OCCLUSION; SCANNING ELECTRON MICROSCOPY; SHEEP; TREATMENT DURATION; UMBILICAL MALFORMATION;

EID: 84904431102     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2014.00110     Document Type: Article

References (37)

1. Liston R, Crane J, Hamilton E, Hughes O, Kuling S, Mackinnon C, et al. Fetal health surveillance in labour. J Obstet Gynaecol Can (2002) 24:250-76.
2. Liston R, Crane J, Hughes O, Kuling S, Mackinnon C, Milne K, et al. Fetal health surveillance in labour. J Obstet Gynaecol Can (2002) 24:342-55.
3. Liston R, Sawchuck D, Young D. Fetal health surveillance: antepartum and intrapartum consensus guideline. J Obstet Gynaecol Can (2007) 29:S3-56.
4. Kaneko M, White S, Homan J, Richardson B. Cerebral blood flow and metabolism in relation to electrocortical activity with severe umbilical cord occlusion in the near-term ovine fetus. Am J Obstet Gynecol (2003) 188:961-72. doi: 10.1067/mob.2003.219
5. Frasch MG, Mansano RZ, Gagnon R, Richardson BS, Ross MG. Measures of acidosis with repetitive umbilical cord occlusions leading to fetal asphyxia in the near-term ovine fetus. Am J Obstet Gynecol (2009) 200:e201-7. doi:10.1016/j.ajog.2008.10.022
6. Frasch MG, Keen AE, Matushewski B, Richardson BS. Comparability of electroenkephalogram (EEG) versus electrocorticogram (ECoG) in the ovine fetus near term. 57th Annual Scientific Meeting of the Society for Gynecologic Investigation, Vol. 17. Orlando, FL: Reproductive Sciences (2010). 304A p. doi:10.1177/193371912010173s067
7. Frasch MG, Keen AE, Gagnon R, Ross MG, Richardson BS. Monitoring fetal electrocortical activity during labour for predicting worsening acidemia: a prospective study in the ovine fetus near term. PLoS One (2011) 6:e22100. doi:10.1371/journal.pone.0022100
8. Wassink G, Bennet L, Davidson JO, Westgate JA, Gunn AJ. Pre-existing hypoxia is associated with greater EEG suppression and early onset of evolving seizure activity during brief repeated asphyxia in near-term fetal sheep. PLoS One (2013) 8:e73895. doi:10.1371/journal.pone.0073895
9. Prout AP, Frasch MG, Veldhuizen R, Hammond R, Matushewski B, Richardson BS. The impact of intermittent umbilical cord occlusions on the inflammatory response in pre-term fetal sheep. PLoS One (2012) 7:e39043. doi:10.1371/journal.pone.0039043
10. Frasch Mg RM, Mansano R, Gagnon R, Richardson BS. Electrocortical activity during gradually increasing asphyxia in the ovine fetus near term. 37th Annual Meeting of the Society of Neuroscience San Diego, CA (2007).
11. Prout AP, Frasch MG, Veldhuizen RA, Hammond R, Ross MG, Richardson BS. Systemic and cerebral inflammatory response to umbilical cord occlusions with worsening acidosis in the ovine fetus. Am J Obstet Gynecol (2010) 202:e81-9. doi:10.1016/j.ajog.2009.08.020
12. Ross MG, Jessie M, Amaya K, Matushewski B, Durosier LD, Frasch MG, et al. Correlation of arterial fetal base deficit and lactate changes with severity of variable heart rate decelerations in the near-term ovine fetus. Am J Obstet Gynecol (2013) 208:e281-6. doi:10.1016/j.ajog.2012.10.883
13. Durosier LD, Green G, Batkin I, Seely AJ, Ross MG, Richardson BS, et al. Sampling rate of heart rate variability impacts the ability to detect acidemia in ovine fetuses near-term. Front Pediatr (2014) 2:38. doi:10.3389/fped.2014.00038
14. Itskovitz J, Lagamma EF, Rudolph AM. Heart rate and blood pressure responses to umbilical cord compression in fetal lambs with special reference to the mechanism of variable deceleration. Am J Obstet Gynecol (1983) 147:451-7.
15. Richardson BS, Rurak D, Patrick JE, Homan J, Carmichael L. Cerebral oxidative metabolism during sustained hypoxaemia in fetal sheep. J Dev Physiol (1989) 11:37-43.
16. Richardson B, Gagnon R. Behavioural state activity and fetal health & development. In: Creasy RK, Resnik R, editors. Maternal-Fetal Medicine. Philadelphia: WB Saunders Company (2008). p. 171-9.
17. Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology (1990) 1:43-6. doi:10.1097/00001648-199001000-00010
18. Frasch MG, Mansano RZ, McPhaul L, Gagnon R, Richardson BS, Ross MG. Measures of acidosis with repetitive umbilical cord occlusions leading to fetal asphyxia in the near-term ovine fetus. Am J Obstet Gynecol (2009) 200:e201-7. doi:10.1016/j.ajog.2008.10.022
19. Giri S, Nath N, Smith B, Viollet B, Singh AK, Singh I. 5-Aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside inhibits proinflammatory response in glial cells: a possible role of AMP-activated protein kinase. J Neurosci (2004) 24:479-87. doi:10.1523/JNEUROSCI.4288-03.2004
20. Katerelos M, Mudge SJ, Stapleton D, Auwardt RB, Fraser SA, Chen CG, et al. 5-Aminoimidazole-4-carboxamide ribonucleoside and AMP-activated protein kinase inhibit signalling through NF-kappaB. Immunol Cell Biol (2010) 88:754-60. doi:10.1038/icb.2010.44
21. Meares GP, Qin H, Liu Y, Holdbrooks AT, Benveniste EN. AMP-activated protein kinase restricts IFN-gamma signaling. J Immunol (2013) 190:372-80. doi:10.4049/jimmunol.1202390
22. Nam HG, Kim W, Yoo DY, Choi JH, Won MH, Hwang IK, et al. Chronological changes and effects of AMP-activated kinase in the hippocampal CA1 region after transient forebrain ischemia in gerbils. Neurol Res (2013) 35:395-405. doi:10.1179/1743132813Y.0000000158
23. Keunen H, Hasaart TH. Fetal arterial pressure and heart rate changes in surviving and non-surviving immature fetal sheep following brief repeated total umbilical cord occlusions. Eur J Obstet Gynecol Reprod Biol (1999) 87:151-7. doi:10.1016/S0301-2115(99)00098-6
24. Pulgar VM, Zhang J, Massmann GA, Figueroa JP. Mild chronic hypoxia modifies the fetal sheep neural and cardiovascular responses to repeated umbilical cord occlusion. Brain Res (2007) 1176:18-26. doi:10.1016/j.brainres.2007.07.089
25. Ziemann AE, Schnizler MK, Albert GW, Severson MA, Howard MA III, Welsh MJ, et al. Seizure termination by acidosis depends on ASIC1a. Nat Neurosci (2008) 11:816-22. doi:10.1038/nn.2132
26. Eaton DG, Wertheim D, Oozeer R, Dubowitz LM, Dubowitz V. Reversible changes in cerebral activity associated with acidosis in preterm neonates. Acta Paediatr (1994) 83:486-92. doi:10.1111/j.1651-2227.1994.tb13064.x
27. Hunter CJ, Bennet L, Power GG, Roelfsema V, Blood AB, Quaedackers JS, et al. Key neuroprotective role for endogenous adenosine A1 receptor activation during asphyxia in the fetal sheep. Stroke (2003) 34:2240-5. doi:10.1161/01.STR.0000083623.77327.CE
28. Zandt BJ, Stigen T, Ten Haken B, Netoff T, Van Putten MJ. Single neuron dynamics during experimentally induced anoxic depolarization. J Neurophysiol (2013) 110:1469-75. doi:10.1152/jn.00250.2013
29. Prout A, Frasch MG, Veldhuizen R, Hammond R, Ross MG, Richardson BS. Inflammatory response to repetitive umbilical cord occlusions with worsening acidosis in the near term ovine fetus. Am J Obstet Gynecol (2009) 202:e81-9. doi:10.1016/j.ajog.2009.08.020
30. Miyamoto O, Auer RN. Hypoxia, hyperoxia, ischemia, and brain necrosis. Neurology (2000) 54:362-71. doi:10.1212/WNL.54.2.362
31. Del Bigio MR, Becker LE. Microglial aggregation in the dentate gyrus: a marker of mild hypoxic-ischaemic brain insult in human infants. Neuropathol Appl Neurobiol (1994) 20:144-51. doi:10.1111/j.1365-2990.1994.tb01173.x
32. Liu F, McCullough LD. Inflammatory responses in hypoxic ischemic ence phalopathy. Acta Pharmacol Sin (2013) 34:1121-30. doi:10.1038/aps.2013.89
33. Safar P, Behringer W, Bottiger BW, Sterz F. Cerebral resuscitation potentials for cardiac arrest. Crit Care Med (2002) 30:S140-4. doi:10.1097/00003246-200204001-00004
34. Glass HC, Ferriero DM. Treatment of hypoxic-ischemic encephalopathy in newborns. Curr Treat Options Neurol (2007) 9:414-23. doi:10.1007/s11940-007-0043-0
35. Bisignano M, Rees S. The effects of intrauterine growth retardation on synaptogenesis and mitochondrial formation in the cerebral and cerebellar cortices of fetal sheep. Int J Dev Neurosci (1988) 6:453-60. doi:10.1016/0736-5748(88)90051-2
36. Keen AE, Frasch MG, Sheehan MA, Matushewski B, Richardson BS. Maturational changes and effects of chronic hypoxemia on electrocortical activity in the ovine fetus. Brain Res (2011) 1402:38-45. doi:10.1016/j.brainres.2011.05.043
37. Piorkowska K, Hammond R, Matushewski B, Richardson B. The impact of fetal growth restriction on brain development in the guinea pig at term. Society for Gynecologic Investigation: Reproductive Sciences, Vol. 19. San Diego, CA: Reproductive Sciences (2012). 352A p. doi:10.1177/1933719112442493