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MR imaging and outcome in neonatal HIBD models are correlated with sex: the value of diffusion tensor MR imaging and diffusion kurtosis MR imaging

Bao, Jieaoxue, Zhang, Xiaoan, Zhao, Xin·2023·Frontiers in Neuroscience
DOI 10.3389/fnins.2023.1234049PMC PMC10543095
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Abstract

Objective: Hypoxic-ischemic encephalopathy can lead to lifelong morbidity and premature death in full-term newborns. Here, we aimed to determine the efficacy of diffusion kurtosis (DK) [mean kurtosis (MK)] and diffusion tensor (DT) [fractional anisotropy (FA), mean diffusion (MD), axial diffusion (AD), and radial diffusion (RD)] parameters for the early diagnosis of early brain histopathological changes and the prediction of neurodegenerative events in a full-term neonatal hypoxic-ischemic brain injury (HIBD) rat model. Methods: The HIBD model was generated in postnatal day 7 Sprague-Dawley rats to assess the changes in DK and DT parameters in 10 specific brain structural regions involving the gray matter, white matter, and limbic system during acute (12 h) and subacute (3 d and 5 d) phases after hypoxic ischemia (HI), which were validated against histology. Sensory and cognitive parameters were assessed by the open field, novel object recognition, elevated plus maze, and CatWalk tests. Results: Repeated-measures ANOVA revealed that specific brain structures showed similar trends to the lesion, and the temporal pattern of MK was substantially more varied than DT parameters, particularly in the deep gray matter. The change rate of MK in the acute phase (12 h) was significantly higher than that of DT parameters. We noted a delayed pseudo-normalization for MK. Additionally, MD, AD, and RD showed more pronounced differences between males and females after HI compared to MK, which was confirmed in behavioral tests. HI females exhibited anxiolytic hyperactivity-like baseline behavior, while the memory ability of HI males was affected in the novel object recognition test. CatWalk assessments revealed chronic deficits in limb gait parameters, particularly the left front paw and right hind paw, as well as poorer performance in HI males than HI females. Conclusions: Our results suggested that DK and DT parameters were complementary in the immature brain and provided great value in assessing early tissue microstructural changes and predicting long-term neurobehavioral deficits, highlighting their ability to detect both acute and long-term changes. Thus, the various diffusion coefficient parameters estimated by the DKI model are powerful tools for early HIBD diagnosis and prognosis assessment, thus providing an experimental and theoretical basis for clinical treatment.

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Figures

Figure 1 Illustration of regions of interest (ROIs) delineation and representative DT and DK parametric maps. (A) Representative images of ROIs. The regions shown are the bilateral corpus callosum (cc), internal capsule (ic), external capsule (ec), hypothalamus (hyp), striatum (str), claustrum (cla), thalamus (tha), motor cortex (mc), somatosensory cortex (sc), and hippocampus (hip). (B) Fractional anisotropy (FA), mean diffusion (MD), axial diffusion (AD), radial diffusion (RD), and mean kurtosis (MK) maps of a representative HI rat at 12 h, 3 and 5 d.
Figure 1 Illustration of regions of interest (ROIs) delineation and representative DT and DK parametric maps. (A) Representative images of ROIs. The regions shown are the bilateral corpus callosum (cc), internal capsule (ic), external capsule (ec), hypothalamus (hyp), striatum (str), claustrum (cla), thalamus (tha), motor cortex (mc), somatosensory cortex (sc), and hippocampus (hip). (B) Fractional anisotropy (FA), mean diffusion (MD), axial diffusion (AD), radial diffusion (RD), and mean kurtosis (MK) maps of a representative HI rat at 12 h, 3 and 5 d.CC BY · PubMed Central
Figure 2 Assessment of diffusion tensor (DT) and diffusion kurtosis (DK) metrics in the focal area after HI injury. (A–E) Effect of time and HI on DT and DK metrics. (F–J) Effects of time, HI and sex on DT and DK metrics. Graphs show FA (A, F), MD (B, G), AD (C, H), RD (D, I), and MK (E, J) of the focal area. (K, L) Percentage changes of different diffusion metrics at three-time points. Graphs show the focal area in the HI group (K) and the corresponding area in the control group (L), respectively. (A–L) Data are presented as means ± SEM (two-way rm ANOVA or two-way ANOVA followed by the Bonferroni post-hoc test). *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001; #P < 0.05. *HI group vs. control group, HI-female vs. C-female, HI-male vs. C-male; #HI-female vs. HI-male.
Figure 2 Assessment of diffusion tensor (DT) and diffusion kurtosis (DK) metrics in the focal area after HI injury. (A–E) Effect of time and HI on DT and DK metrics. (F–J) Effects of time, HI and sex on DT and DK metrics. Graphs show FA (A, F), MD (B, G), AD (C, H), RD (D, I), and MK (E, J) of the focal area. (K, L) Percentage changes of different diffusion metrics at three-time points. Graphs show the focal area in the HI group (K) and the corresponding area in the control group (L), respectively. (A–L) Data are presented as means ± SEM (two-way rm ANOVA or two-way ANOVA followed by the Bonferroni post-hoc test). *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001; #P < 0.05. *HI group vs. control group, HI-female vs. C-female, HI-male vs. C-male; #HI-female vs. HI-male.CC BY · PubMed Central
Figure 3 Assessment of DT and DK metrics at the level of cortical gray matter, white matter and hippocampus after HI injury. (A–F) Effect of time and HI on DT and DK metrics. (G–L) Effects of time, HI and sex on DT and DK metrics. Graphs show FA (a), MD (b), AD (c), RD (d), and MK (e) at the levels of mc (A, G), sc (B, H), cc (C, I), ic (D, J), ec (E, K), and hip (F, L), respectively. (A–L) Data are presented as means ± SEM (two-way rm ANOVA or two-way ANOVA followed by the Bonferroni post-hoc test). *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001; #P < 0.05, ###P < 0.001, ####P < 0.0001. *HI group vs. control group, HI-female vs. C-female, HI-male vs. C-male; #HI-female vs. HI-male.
Figure 3 Assessment of DT and DK metrics at the level of cortical gray matter, white matter and hippocampus after HI injury. (A–F) Effect of time and HI on DT and DK metrics. (G–L) Effects of time, HI and sex on DT and DK metrics. Graphs show FA (a), MD (b), AD (c), RD (d), and MK (e) at the levels of mc (A, G), sc (B, H), cc (C, I), ic (D, J), ec (E, K), and hip (F, L), respectively. (A–L) Data are presented as means ± SEM (two-way rm ANOVA or two-way ANOVA followed by the Bonferroni post-hoc test). *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001; #P < 0.05, ###P < 0.001, ####P < 0.0001. *HI group vs. control group, HI-female vs. C-female, HI-male vs. C-male; #HI-female vs. HI-male.CC BY · PubMed Central
Figure 4 Evaluation of open-field performance in PND61 rats. (A) Distance of activity. (B) Mean speed. Graphs show the overall (a), peripheral (b), and central (c) regions, respectively. (C) Immobility time. (D) Percentage of peripheral immobility time. (E) Number of center entries. (F) Representative traces of HI male and female rat movement during the open-field test. (G) Percentage of periphery time. (H) Percentage of center time. (I) Circle counts. (J) Center square cross counts. (A–H) Data are presented as means ± SEM (two-way ANOVA followed by the Bonferroni post-hoc test). (I, J) Data are presented as median ± IQR (Kruskal–Wallis test followed by the Dunn's test). *P < 0.05, **P < 0.01; #P < 0.05, ##P < 0.01, ###P < 0.001, ####P < 0.0001. *HI-female vs. C-female, HI-male vs. C-male; #HI-female vs. HI-male (n = 6 per group).
Figure 4 Evaluation of open-field performance in PND61 rats. (A) Distance of activity. (B) Mean speed. Graphs show the overall (a), peripheral (b), and central (c) regions, respectively. (C) Immobility time. (D) Percentage of peripheral immobility time. (E) Number of center entries. (F) Representative traces of HI male and female rat movement during the open-field test. (G) Percentage of periphery time. (H) Percentage of center time. (I) Circle counts. (J) Center square cross counts. (A–H) Data are presented as means ± SEM (two-way ANOVA followed by the Bonferroni post-hoc test). (I, J) Data are presented as median ± IQR (Kruskal–Wallis test followed by the Dunn's test). *P < 0.05, **P < 0.01; #P < 0.05, ##P < 0.01, ###P < 0.001, ####P < 0.0001. *HI-female vs. C-female, HI-male vs. C-male; #HI-female vs. HI-male (n = 6 per group).CC BY · PubMed Central
Figure 5 Evaluation of recognition memory ability in PND62 rats. (A, B) The relative ratios of object preference for two identical objects (same 1 and same 2) in the training phase and familiar and novel objects (familiar and novel) in the test phase are shown, respectively. (C) Recognition index. (D, E) The ratios of novel and familiar object preference are shown, respectively. (A–E) Data are presented as means ± SEM. *P < 0.05, ****P < 0.0001; #P < 0.05. *Familiar vs. novel (Student's t-test); #HI-female vs. HI-male (two-way ANOVA followed by the Bonferroni post-hoc test) (n = 6 per group).
Figure 5 Evaluation of recognition memory ability in PND62 rats. (A, B) The relative ratios of object preference for two identical objects (same 1 and same 2) in the training phase and familiar and novel objects (familiar and novel) in the test phase are shown, respectively. (C) Recognition index. (D, E) The ratios of novel and familiar object preference are shown, respectively. (A–E) Data are presented as means ± SEM. *P < 0.05, ****P < 0.0001; #P < 0.05. *Familiar vs. novel (Student's t-test); #HI-female vs. HI-male (two-way ANOVA followed by the Bonferroni post-hoc test) (n = 6 per group).CC BY · PubMed Central
Figure 6 Evaluation of motor function in PND71 rats. (A–D) Relevant gait parameters for the front paw. (E–H) Relevant gait parameters for the hind paws. Graphs show the standing time (A, E), swing time (B, F), duty cycle (C, G), and maximum contact area (D, H) in overall (a), male (b), and female (c), respectively. (A–H) Data are presented as means ± SEM. *P < 0.05, **P < 0.01; #P < 0.05, ##P < 0.01, ###P < 0.001, ####P < 0.0001. *RF vs. LF, RH vs. LH (paired t-test); #HI vs. C, HI-female vs. C-female, HI-male vs. C-male (two-way ANOVA followed by the Bonferroni post-hoc test). RF, right fore; RH, right hind; LF, left fore; LH, left hind limbs (n = 6 per group).
Figure 6 Evaluation of motor function in PND71 rats. (A–D) Relevant gait parameters for the front paw. (E–H) Relevant gait parameters for the hind paws. Graphs show the standing time (A, E), swing time (B, F), duty cycle (C, G), and maximum contact area (D, H) in overall (a), male (b), and female (c), respectively. (A–H) Data are presented as means ± SEM. *P < 0.05, **P < 0.01; #P < 0.05, ##P < 0.01, ###P < 0.001, ####P < 0.0001. *RF vs. LF, RH vs. LH (paired t-test); #HI vs. C, HI-female vs. C-female, HI-male vs. C-male (two-way ANOVA followed by the Bonferroni post-hoc test). RF, right fore; RH, right hind; LF, left fore; LH, left hind limbs (n = 6 per group).CC BY · PubMed Central
Figure 7 Representative photomicrographs of H&E staining and TUNNEL staining in cortical and hippocampal sections at 12 h, 3 and 5 d (×400). The arrows represent histopathological changes.
Figure 7 Representative photomicrographs of H&E staining and TUNNEL staining in cortical and hippocampal sections at 12 h, 3 and 5 d (×400). The arrows represent histopathological changes.CC BY · PubMed Central

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Metadata

Authors
Bao, J., Zhang, X., & Zhao, X.
Venue
Frontiers in Neuroscience
Publisher
Frontiers Media SA
Published
2023-09-15
Volume
17
ISSN
1662-453X
DOI
10.3389/fnins.2023.1234049
PMC
PMC10543095
Cited by
6
References
2
Licence
creativecommons.org/licenses/by/4.0/ (vor)

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CoChat. (2026). Citation check: MR imaging and outcome in neonatal HIBD models are correlated with sex: the value of diffusion tensor MR imaging and diffusion kurtosis MR imaging. https://app.cochat.ai/papers/10.3389/fnins.2023.1234049
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Bao, J., Zhang, X., & Zhao, X. (2023). MR imaging and outcome in neonatal HIBD models are correlated with sex: the value of diffusion tensor MR imaging and diffusion kurtosis MR imaging. Frontiers in Neuroscience. https://doi.org/10.3389/fnins.2023.1234049