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White matter thickness was significantly improved, with increased numbers of total Olig2 + and mature CC1 + oligodendrocytes. Mechanistically, sildenafil restored p-AKT levels, which suggests involvement of the PI3K/AKT/mTOR pathway. Sildenafil significantly reduced neuroinflammation, improved white matter integrity, and supported oligodendrocyte recovery after neonatal HI. These findings highlight the potential of sildenafil as a neurorestorative therapy during the tertiary phase of injury in neonatal HIE. Neonatal hypoxic-ischemic encephalopathy (HIE) due to birth asphyxia remains a leading cause of neonatal death and long-term neurological disability affecting approximately 3 per 1000 live births worldwide1. Therapeutic hypothermia (TH), initiated within 6 h of life and for 72 h, is the only proven treatment for HIE and reduces mortality and neurodevelopmental impairments2,3,4.

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However, TH is not effective for all affected neonates and offers no neurorestorative properties3. A critical need exists for adjunct therapies that promote brain repair (“neurorestorative” therapies) after an initial injury. The initial phase (0–6 h) involves energy failure and necrosis5. The secondary phase (6–48 h) triggers apoptosis through excitotoxicity, oxidative stress, and mitochondrial damages6,7. The tertiary phase (beyond 48 h) is marked by chronic neuroinflammation and epigenetic changes that impair recovery and lead to further neuronal and oligodendrocyte loss through apoptosis and autophagy8. Persistent glial activation and inflammatory cytokine release disrupt essential neurodevelopmental processes such as neurogenesis, oligodendrogenesis, and synaptogenesis9,10,11,12,13,14.

5.1 Hypotension

HI also elevated Iba1 + microglia in the cortex (413 [383–506], p < 0.0001] (Fig. Microglial process length was reduced after HI (0.033 mm [0.031–0.035] vs sham: 0.068 mm [0.066–0.071], p < 0.0001] (Fig. Galectin-3/MAC-2 + macrophages were significantly increased in the ECL (273 [96–706] vs. 0 [0–27], p < 0.05) (Fig. While TH targets the early phases of injury, sildenafil 100g therapies that address the tertiary phase may enhance long-term recovery. Sildenafil (Viagra®), a phosphodiesterase type 5 (PDE5) inhibitor that increases intracellular cGMP, shows promise as a neurorestorative therapy.

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It has been found to enhance both functional and structural recovery in adult stroke models15,16 and is already used safely in neonates with persistent pulmonary hypertension17,18. In a rat model of term neonatal HIE, sildenafil enhanced brain and retinal function and structure after hypoxia–ischemia19,20,21 and increased neuronal density near injury sites19. However, its effects on neuroinflammation and white matter injury in this model remain unclear. In adult models of neurodegenerative disease, sildenafil has been shown to reduce neuroinflammation22,23,24,25,26,27 and promote white matter repair by supporting oligodendrocyte survival23,28,29. The present study aimed to evaluate the effects of sildenafil on neuroinflammation and white matter injury in a rat model of term HIE. All procedures followed institutional standard operating procedures (SOPs) and the Canadian Council on Animal Care’s (CCAC) guidelines in accordance with the Animals for Research Act, were approved by the local Animal Care Committee, and were reported in accordance with ARRIVE guidelines30.

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We made group comparisons using Kruskal–Wallis non-parametric tests, followed by Dunn’s post hoc tests to adjust the α–level as necessary. We considered a p-value < 0.05 to be statistically significant. We conducted analyses using GraphPad Prism® (GraphPad Software Inc., San Diego, CA, USA). At P30, HI significantly increased the number of GFAP + reactive astrocytes in the ipsilateral cortex (median [interquartile ranges]: 533 cells/mm2 [529–601], p < 0.05) (Fig. 2), compared to sham (cortex: 239 [187–275]; CC: 425 [269–553]; ECL: 692 [576–850]). Adult female Long-Evans rats male-only litters (Harlan Laboratories) were housed under standard conditions with food and water ad libitum. Pups remained with their mother until weaning at postnatal day 21 (P21).

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In a rat model of term neonatal HIE, sildenafil enhanced brain and retinal function and structure after hypoxia–ischemia19,20,21 and increased neuronal density near injury sites19. However, its effects on neuroinflammation and white matter injury in this model remain unclear. In adult models of neurodegenerative disease, sildenafil has been shown to reduce neuroinflammation22,23,24,25,26,27 and promote white matter repair by supporting oligodendrocyte survival23,28,29. The present study aimed to evaluate the effects of sildenafil on neuroinflammation and white matter injury in a rat model of term HIE. All procedures followed institutional standard operating procedures (SOPs) and the Canadian Council on Animal Care’s (CCAC) guidelines in accordance with the Animals for Research Act, were approved by the local Animal Care Committee, and were reported in accordance with ARRIVE guidelines30.

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Adult female Long-Evans rats male-only litters (Harlan Laboratories) were housed under standard conditions with food and water ad libitum. Pups remained with their mother until weaning at postnatal day 21 (P21). Daily monitoring was performed by facility technicians and researchers. To model brain injury in term human neonates with HIE31,32,33,34,35,36, we used the well-established Vannucci model31,32,33,34,37,38. On P10, rat pups underwent left carotid artery ligation (ischemia) followed by 2 h of hypoxia (8% oxygen)19.

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Sham-operated controls underwent identical procedures without hypoxia–ischemia (HI), and sham pups were kept normothermic using warming blankets (Cincinnati Sub-Zero, Cincinnati, USA) during separation from dams. Sample size (n = 6–12 per group) was based on feasibility, ethical constraints, and the 3Rs principle (replacement, reduction, refinement). Sildenafil (Viagra®, Pfizer; 100-mg tablets) was prepared as previously described19,20. From 12 h post-HI, we randomized pups to receive sildenafil sildenafil pink pill or vehicle by oral gavage twice daily for 7 days (P10-17). Doses in HI pups included 2, 10, and 50 mg/kg for histology/immunohistochemistry, and 50 mg/kg for Western blot/ELISA, based on human-equivalent dosing39 and previous efficacy studies in cortex/retina19,20. Daily monitoring was performed by facility technicians and researchers. To model brain injury in term human neonates with HIE31,32,33,34,35,36, we used the well-established Vannucci model31,32,33,34,37,38. On P10, rat pups underwent left carotid artery ligation (ischemia) followed by 2 h of hypoxia (8% oxygen)19. Sham-operated controls underwent identical procedures without hypoxia–ischemia (HI), and sham pups were kept normothermic using warming blankets (Cincinnati Sub-Zero, Cincinnati, USA) during separation from dams. Sample size (n = 6–12 per group) was based on feasibility, ethical constraints, and the 3Rs principle (replacement, reduction, refinement). Sildenafil (Viagra®, Pfizer; 100-mg tablets) was prepared as previously described19,20. From 12 h post-HI, we randomized pups to receive sildenafil sildenafil pink pill or vehicle by oral gavage twice daily for 7 days (P10-17). Doses in HI pups included 2, 10, and 50 mg/kg for histology/immunohistochemistry, and 50 mg/kg for Western blot/ELISA, based on human-equivalent dosing39 and previous efficacy studies in cortex/retina19,20. We collected brains at P3019,20 and sectioned them at –2.16 mm from Bregma. We imaged hematoxylin and eosin-stained coronal sections using a Leica DM4000B microscope and a Leica DFC450C digital camera (Leica DFC450C, Leica Microsystems, Wetzlar, Hessen, Germany).

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We collected brains at P3019,20 and sectioned them at –2.16 mm from Bregma. We imaged hematoxylin and eosin-stained coronal sections using a Leica DM4000B microscope and a Leica DFC450C digital camera (Leica DFC450C, Leica Microsystems, Wetzlar, Hessen, Germany). We stitched overlapping 5 × images using a Microsoft Image Composite Editor. Using ImageJ (Image Processing and Analysis in Java)40, we blindly measured the thicknesses of the corpus callosum and ipsilateral external capsule on two sections per animal and averaged them. At P30, we initially incubated the sections in a universal antigen retrieval reagent at 95 °C for 20 min, and then blocked them in phosphate-buffered saline containing tween20 and gelatin (PBS-GT).

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We incubated the primary antibodies overnight at 4 °C in PBS-GT. We also used the appropriate AlexaFluor® or Cy™3 secondary antibodies. We counterstained the sections with DAPI and mounted them with Vectashield (H1200; Vector Laboratories, Burlingame, CA, USA). We performed the imaging using a fluorescent microscope (20x). For quantitative measurements, coronal brain sections were selected at a consistent anatomical level characterized by visible hippocampi, reduced lateral ventricles, a visible third ventricle, and clear delineation of the thalamus (Figs.

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Stained brain sections were imaged using a fluorescent microscope (Leica DM4000B LED, Leica Microsystems, Wetzlar, Germany) with a 20 × objective. For each animal, 2–3 fields were captured in the left (ipsilateral) cortex of HI animals near the infarct boundary zone and extending toward the midline (Fig. 1G); corresponding cortical fields were captured in sham-vehicle animals at matched anatomical landmarks to ensure valid comparisons across groups. Additional 20 sildenafil from canada × micrographs were also obtained from the corpus callosum (CC) and the left (ipsilateral) external capsule (ECL) to evaluate white matter, using identical anatomical reference points across animals; the CC was measured at the midline between hemispheres, and the ECL on the left side at the same coronal level (Fig. We also assessed the microglial activation by measuring the maximal process length from five randomly selected microglia cells per animal. We stitched overlapping 5 × images using a Microsoft Image Composite Editor. Using ImageJ (Image Processing and Analysis in Java)40, we blindly measured the thicknesses of the corpus callosum and ipsilateral external capsule on two sections per animal and averaged them. At P30, we initially incubated the sections in a universal antigen retrieval reagent at 95 °C for 20 min, and then blocked them in phosphate-buffered saline containing tween20 and gelatin (PBS-GT). We incubated the primary antibodies overnight at 4 °C in PBS-GT. We also used the appropriate AlexaFluor® or Cy™3 secondary antibodies. We counterstained the sections with DAPI and mounted them with Vectashield (H1200; Vector Laboratories, Burlingame, CA, USA).

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One investigator took pictures of the respective fields of view and another blinded investigator, performed the cell counts. For western blotting, we euthanized the rats at P12, P17, and P30. The middle third of the ipsilateral cortex and white matter (excluding basal ganglia, hippocampus, and cerebellum) was flash frozen. We lysed the tissues by sonication in an ice-cold RIPA buffer (89,901, ThermoFisher Scientific, Waltham, Massachusetts, USA) with protease inhibitors (S8820, Sigma-Aldrich, St. Louis, Missouri, USA), centrifuged (12,000 RCF, 10 min, 4 °C), and measured the protein concentration (BCA assay) (23,225; Thermo Fisher Scientific, PierceTM, Waltham, Massachusetts, USA).

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We loaded equal protein amounts on SDS–polyacrylamide CriterionTM TGXTM precast gels (567–1085; Bio-Rad®, Hercules, California, USA) and then transferred them to a Polyvinylidene difluoride (PVDF) membrane (10,600,023; AmershamTM HybondTM, Boston, Massachusetts, USA). We blocked the membranes with 5% dried non-fat milk in Tris-buffered saline containing 0.1% Tween-20 (9005-64-5; Fisher BioReagentsTM, Hampton, New Hampshire, USA), and then incubated them overnight at 4 °C with the following primary antibodies: cleaved poly-ADP-ribose polymerase (PARP) (rabbit anti-PARP, 9542; Cell Signaling Technology, Danvers, Massachusetts, USA; dilution 1:1000), a marker of apoptosis; superoxide dismutase 1 (SOD1) (rabbit anti-SOD1, ab13498; Abcam, Cambridge, UK; dilution 1:1000), a marker of oxidative stress; synaptophysin (rabbit anti-synaptophysin, 5461; Cell Signaling Technology, Danvers, Massachusetts, USA; dilution 1:1000), a marker of synaptic density; oligodendrocyte lineage transcription factor 2 (Olig2) (mouse anti-Olig2, MABN50; Sigma-Aldrich, St. Louis, Missouri, USA; dilution 1:2000), a marker of total oligodendrocytes; neuronal nuclei antibody (NeuN) (mouse anti-NeuN, MAB377; Millipore, Burlington, Massachusetts, USA; dilution 1:500), a marker of mature neurons; and phosphorylated protein kinase B (pAKT) (rabbit anti-phospho-Akt Ser473 D9E, 4060; Cell Signaling Technology, Danvers, Massachusetts, USA; dilution 1:1000), an upstream regulator of the mechanistic target of rapamycin (mTOR) pathway. We used chemiluminescence detection and an imaging system (Amersham Imager 600, General Electric, Boston, Massachusetts, USA), and we quantified band intensities using Image Lab® software (Bio-Rad®, Hercules, California, USA), normalized to ß-actin (mouse anti-ß-actin; Millipore Sigma, Oakville, Ontario, Canada; dilution: 1:5000). We randomly assigned pups to treatment groups. We performed the imaging using a fluorescent microscope (20x).

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For quantitative measurements, coronal brain sections were selected at a consistent anatomical level characterized by visible hippocampi, reduced lateral ventricles, a visible third ventricle, and clear delineation of the thalamus (Figs. Stained brain sections were imaged using a fluorescent microscope (Leica DM4000B LED, Leica Microsystems, Wetzlar, Germany) with a 20 × objective. For each animal, 2–3 fields were captured in the left (ipsilateral) cortex of HI animals near the infarct boundary zone and extending toward the midline (Fig. 1G); corresponding cortical fields were captured in sham-vehicle animals at matched anatomical landmarks to ensure valid comparisons across groups. Additional 20 sildenafil from canada × micrographs were also obtained from the corpus callosum (CC) and the left (ipsilateral) external capsule (ECL) to evaluate white matter, using identical anatomical reference points across animals; the CC was measured at the midline between hemispheres, and the ECL on the left side at the same coronal level (Fig. We also assessed the microglial activation by measuring the maximal process length from five randomly selected microglia cells per animal. One investigator took pictures of the respective fields of view and another blinded investigator, performed the cell counts. For western blotting, we euthanized the rats at P12, P17, and P30.

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The middle third of the ipsilateral cortex and white matter (excluding basal ganglia, hippocampus, and cerebellum) was flash frozen. We lysed the tissues by sonication in an ice-cold RIPA buffer (89,901, ThermoFisher Scientific, Waltham, Massachusetts, USA) with protease inhibitors (S8820, Sigma-Aldrich, St. Louis, Missouri, USA), centrifuged (12,000 RCF, 10 min, 4 °C), and measured the protein concentration (BCA assay) (23,225; Thermo Fisher Scientific, PierceTM, Waltham, Massachusetts, USA). We loaded equal protein amounts on SDS–polyacrylamide CriterionTM TGXTM precast gels (567–1085; Bio-Rad®, Hercules, California, USA) and then transferred them to a Polyvinylidene difluoride (PVDF) membrane (10,600,023; AmershamTM HybondTM, Boston, Massachusetts, USA). We blocked the membranes with 5% dried non-fat milk in Tris-buffered saline containing 0.1% Tween-20 (9005-64-5; Fisher BioReagentsTM, Hampton, New Hampshire, USA), and then incubated them overnight at 4 °C with the following primary antibodies: cleaved poly-ADP-ribose polymerase (PARP) (rabbit anti-PARP, 9542; Cell Signaling Technology, Danvers, Massachusetts, USA; dilution 1:1000), a marker of apoptosis; superoxide dismutase 1 (SOD1) (rabbit anti-SOD1, ab13498; Abcam, Cambridge, UK; dilution 1:1000), a marker of oxidative stress; synaptophysin (rabbit anti-synaptophysin, 5461; Cell Signaling Technology, Danvers, Massachusetts, USA; dilution 1:1000), a marker of synaptic density; oligodendrocyte lineage transcription factor 2 (Olig2) (mouse anti-Olig2, MABN50; Sigma-Aldrich, St.

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Louis, Missouri, USA; dilution 1:2000), a marker of total oligodendrocytes; neuronal nuclei antibody (NeuN) (mouse anti-NeuN, MAB377; Millipore, Burlington, Massachusetts, USA; dilution 1:500), a marker of mature neurons; and phosphorylated protein kinase B (pAKT) (rabbit anti-phospho-Akt Ser473 D9E, 4060; Cell Signaling Technology, Danvers, Massachusetts, USA; dilution 1:1000), an upstream regulator of the mechanistic target of rapamycin (mTOR) pathway. We used chemiluminescence detection and an imaging system (Amersham Imager 600, General Electric, Boston, Massachusetts, USA), and we quantified band intensities using Image Lab® software (Bio-Rad®, Hercules, California, USA), normalized to ß-actin (mouse anti-ß-actin; Millipore Sigma, Oakville, Ontario, Canada; dilution: 1:5000). We randomly assigned pups to treatment groups. We made group comparisons using Kruskal–Wallis non-parametric tests, followed by Dunn’s post hoc tests to adjust the α–level as necessary. We considered a p-value < 0.05 to be statistically significant. We conducted analyses using GraphPad Prism® (GraphPad Software Inc., San Diego, CA, USA). At P30, HI significantly increased the number of GFAP + reactive astrocytes in the ipsilateral cortex (median [interquartile ranges]: 533 cells/mm2 [529–601], p < 0.05) (Fig. 2), compared to sham (cortex: 239 [187–275]; CC: 425 [269–553]; ECL: 692 [576–850]). HI also elevated Iba1 + microglia in the cortex (413 [383–506], p < 0.0001] (Fig. Microglial process length was reduced after HI (0.033 mm [0.031–0.035] vs sham: 0.068 mm [0.066–0.071], p < 0.0001] (Fig. Galectin-3/MAC-2 + macrophages were significantly increased in the ECL (273 [96–706] vs. 0 [0–27], p < 0.05) (Fig.

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White matter thickness was significantly improved, with increased numbers of total Olig2 + and mature CC1 + oligodendrocytes. Mechanistically, sildenafil restored p-AKT levels, which suggests involvement of the PI3K/AKT/mTOR pathway. Sildenafil significantly reduced neuroinflammation, improved white matter integrity, and supported oligodendrocyte recovery after neonatal HI. These findings highlight the potential of sildenafil as a neurorestorative therapy during the tertiary phase of injury in neonatal HIE. Neonatal hypoxic-ischemic encephalopathy (HIE) due to birth asphyxia remains a leading cause of neonatal death and long-term neurological disability affecting approximately 3 per 1000 live births worldwide1.

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Therapeutic hypothermia (TH), initiated within 6 h of life and for 72 h, is the only proven treatment for HIE and reduces mortality and neurodevelopmental impairments2,3,4. However, TH is not effective for all affected neonates and offers no neurorestorative properties3. A critical need exists for adjunct therapies that promote brain repair (“neurorestorative” therapies) after an initial injury. The initial phase (0–6 h) involves energy failure and necrosis5. The secondary phase (6–48 h) triggers apoptosis through excitotoxicity, oxidative stress, and mitochondrial damages6,7.

Sildenafil normalized apoptosis, antioxidant defense, and neuronal and synaptic markers altered by HI

The tertiary phase (beyond 48 h) is marked by chronic neuroinflammation and epigenetic changes that impair recovery and lead to further neuronal and oligodendrocyte loss through apoptosis and autophagy8. Persistent glial activation and inflammatory cytokine release disrupt essential neurodevelopmental processes such as neurogenesis, oligodendrogenesis, and synaptogenesis9,10,11,12,13,14. While TH targets the early phases of injury, sildenafil 100g therapies that address the tertiary phase may enhance long-term recovery. Sildenafil (Viagra®), a phosphodiesterase type 5 (PDE5) inhibitor that increases intracellular cGMP, shows promise as a neurorestorative therapy. It has been found to enhance both functional and structural recovery in adult stroke models15,16 and is already used safely in neonates with persistent pulmonary hypertension17,18.