Antenatal dexamethasone after asphyxia increases neural injury in preterm fetal sheep

PLoS One. 2013 Oct 18;8(10):e77480. doi: 10.1371/journal.pone.0077480. eCollection 2013.

Abstract

Background and purpose: Maternal glucocorticoid treatment for threatened premature delivery dramatically improves neonatal survival and short-term morbidity; however, its effects on neurodevelopmental outcome are variable. We investigated the effect of maternal glucocorticoid exposure after acute asphyxia on injury in the preterm brain.

Methods: Chronically instrumented singleton fetal sheep at 0.7 of gestation received asphyxia induced by complete umbilical cord occlusion for 25 minutes. 15 minutes after release of occlusion, ewes received a 3 ml i.m. injection of either dexamethasone (12 mg, n = 10) or saline (n = 10). Sheep were killed after 7 days recovery; survival of neurons in the hippocampus and basal ganglia, and oligodendrocytes in periventricular white matter were assessed using an unbiased stereological approach.

Results: Maternal dexamethasone after asphyxia was associated with more severe loss of neurons in the hippocampus (CA3 regions, 290 ± 76 vs 484 ± 98 neurons/mm(2), mean ± SEM, P<0.05) and basal ganglia (putamen, 538 ± 112 vs 814 ± 34 neurons/mm(2), P<0.05) compared to asphyxia-saline, and with greater loss of both total (913 ± 77 vs 1201 ± 75/mm(2), P<0.05) and immature/mature myelinating oligodendrocytes in periventricular white matter (66 ± 8 vs 114 ± 12/mm(2), P<0.05, vs sham controls 165 ± 10/mm(2), P<0.001). This was associated with transient hyperglycemia (peak 3.5 ± 0.2 vs. 1.4 ± 0.2 mmol/L at 6 h, P<0.05) and reduced suppression of EEG power in the first 24 h after occlusion (maximum -1.5 ± 1.2 dB vs. -5.0 ± 1.4 dB in saline controls, P<0.01), but later onset and fewer overt seizures.

Conclusions: In preterm fetal sheep, exposure to maternal dexamethasone during recovery from asphyxia exacerbated brain damage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / adverse effects*
  • Asphyxia / drug therapy
  • Asphyxia / pathology*
  • Basal Ganglia / drug effects
  • Basal Ganglia / pathology
  • Cell Count
  • Cell Death
  • Cerebral Ventricles / drug effects
  • Cerebral Ventricles / pathology
  • Dexamethasone / adverse effects*
  • Electroencephalography
  • Female
  • Fetus
  • Hippocampus / drug effects
  • Hippocampus / pathology
  • Injections, Intramuscular
  • Neurons / drug effects*
  • Neurons / pathology
  • Oligodendroglia / drug effects*
  • Oligodendroglia / pathology
  • Pregnancy
  • Premature Birth / pathology
  • Sheep
  • Sheep, Domestic
  • Umbilical Cord / pathology

Substances

  • Anti-Inflammatory Agents
  • Dexamethasone

Grants and funding

This study was supported by public good grants from the Health Research Council of New Zealand, the Auckland Medical Research Foundation, and Lottery Health New Zealand. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.