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RESEARCH ARTICLE
Pathophysiological and behavioral deficits in developing mice following rotational acceleration-deceleration traumatic brain injury
Guoxiang Wang, Yi Ping Zhang, Zhongwen Gao, Lisa B. E. Shields, Fang Li, Tianci Chu, Huayi Lv, Thomas Moriarty, Xiao-Ming Xu, Xiaoyu Yang, Christopher B. Shields, Jun Cai
Disease Models & Mechanisms 2018 11: dmm030387 doi: 10.1242/dmm.030387 Published 30 January 2018
Guoxiang Wang
1Department of Spine Surgery, Orthopedics Hospital affiliated to the Second Bethune Hospital, Jilin University, Changchun 130041, China
2Department of Pediatrics, University of Louisville School of Medicine, Louisville, KY 40202, USA
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  • ORCID record for Guoxiang Wang
Yi Ping Zhang
3Norton Neuroscience Institute, Norton Healthcare, Louisville, KY 40202, USA
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Zhongwen Gao
2Department of Pediatrics, University of Louisville School of Medicine, Louisville, KY 40202, USA
4Department of Orthopedics, China-Japan Union Hospital of Jilin University, Changchun 130033, China
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Lisa B. E. Shields
3Norton Neuroscience Institute, Norton Healthcare, Louisville, KY 40202, USA
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  • ORCID record for Lisa B. E. Shields
Fang Li
2Department of Pediatrics, University of Louisville School of Medicine, Louisville, KY 40202, USA
5Department of Neurological Surgery, China-Japan Friendship Hospital, Beijing 100029, China
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Tianci Chu
2Department of Pediatrics, University of Louisville School of Medicine, Louisville, KY 40202, USA
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Huayi Lv
6Eye Center of the Second Bethune Hospital, Jilin University, Changchun 130041, China
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Thomas Moriarty
3Norton Neuroscience Institute, Norton Healthcare, Louisville, KY 40202, USA
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Xiao-Ming Xu
7Stark Neurosciences Research Institute, Department of Neurological Surgery, Indiana University School of Medicine, Indianapolis, IN 46202, USA
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Xiaoyu Yang
1Department of Spine Surgery, Orthopedics Hospital affiliated to the Second Bethune Hospital, Jilin University, Changchun 130041, China
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  • ORCID record for Xiaoyu Yang
  • For correspondence: j0cai002@louisville.edu cbshields1@gmail.com yangxiaoyu88@sina.com
Christopher B. Shields
3Norton Neuroscience Institute, Norton Healthcare, Louisville, KY 40202, USA
8Department of Neurological Surgery, University of Louisville School of Medicine, Louisville, KY 40202, USA
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  • For correspondence: j0cai002@louisville.edu cbshields1@gmail.com yangxiaoyu88@sina.com
Jun Cai
1Department of Spine Surgery, Orthopedics Hospital affiliated to the Second Bethune Hospital, Jilin University, Changchun 130041, China
2Department of Pediatrics, University of Louisville School of Medicine, Louisville, KY 40202, USA
9Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, KY 40202, USA
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  • For correspondence: j0cai002@louisville.edu cbshields1@gmail.com yangxiaoyu88@sina.com
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    Fig. 1.

    Study design and RAD brain injury model. (A) Experimental workflow for rotational acceleration-deceleration TBI in developing mice. (B) Illustration of the major components of the RADi device. (C) Schematic of the RADi procedure. Hyperextension of the neck occurs when the plunger strikes the ‘driver bar’ at the ‘hit location’ site (white down arrow) on activation of the pneumatic cylinder. When the plunger is released (white up arrow), the neck is forced back to the flexed position by the compression spring attached to the anterior part of the rotating axle (black down arrow). Each hyperextension-flexion cycle represents one rotation. (D) Pneumatic pressure of the plunger (psi) versus the peak angular velocities (rad/s) of the head.

  • Table 1.
  • Fig. 2.
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    Fig. 2.

    Survival rate and recovery of the righting reflex. (A) Survival rate following 60 psi for 30, 60, 80 and 100 RADi (n=20 per group). (B) Recovery time of the righting reflex in sham and after 30, 60, 80, and 100 RADi with 60 psi (n=9 per group). Data are presented as mean±s.d. and were analyzed by one-way ANOVA followed by Tukey's post hoc test. ***P<0.001.

  • Fig. 3.
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    Fig. 3.

    Cerebral blood perfusion preinjury, immediately after RADi, and 4 h and 24 h following 60 psi×60 RADi. (A) Representative images of LASCA of blood perfusion in two RADi mouse brains. Baseline and RADi images show areas of yellow-red as high blood perfusion and areas of blue-black as low blood perfusion. (B) Statistical analysis of mean PU per square millimeter. Data are presented as mean±s.d. and were analyzed by one-way with repeated-measures ANOVA followed by Tukey's post hoc test. *P<0.05, **P<0.01; n=6.

  • Fig. 4.
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    Fig. 4.

    Hemorrhage and cerebral edema following RADi. (A) Subdural/subarachnoid hemorrhages of brains of sham mice (left) and mice following different repetitions of RADi at 60 psi (right). (B) Breakdown of BBB integrity owing to increased vascular permeability in sham mice and in mice subjected to 60 psi×60 RADi taken 7 h postinjury. The dramatic retention of Evans Blue in traumatized brains compared with that in sham brains indicates increased permeability of the BBB. (C) Water content in sham and RADi mice. Data are presented as mean±s.d. and were analyzed by unpaired two-tailed Student's t-test. *P<0.05, **P<0.01; n=5 per group. Arrowheads indicate subarachnoid hemorrhage.

  • Fig. 5.
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    Fig. 5.

    Proinflammatory and glial activation following RADi in the brain. (A) Western blots of proinflammatory cytokines IL-6 and TNFα, the glial-specific intermediate filament protein GFAP, and macrophage/microglia-specific protein Iba1 in two sham and RADi mouse brains at 3 dpi following 60 psi×60 RADi. (B) Statistical analysis of western blots. Data are presented as mean±s.d. and were analyzed by unpaired two-tailed Student's t-test. *P<0.05, **P<0.01; n=4 per group. (C) Photomicrographs of immunostaining showing increased GFAP- and Iba1-positive glia in the pons of sham and RADi brains at 3 dpi. Insets show higher magnifications of the boxed areas. Scale bars: 100 µm.

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    Fig. 6.

    Neuronal degeneration in RADi mouse cortex at 30 dpi following 60 psi×60 RADi. Silver staining showed neuronal degeneration (dark cells, arrowheads) in primary motor cortex, primary somatosensory cortex, and olfactory tubercle. Insets show higher magnifications of the boxed areas. Scale bars: 100 μm (red), 25 μm (black).

  • Fig. 7.
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    Fig. 7.

    Neurobehavioral changes in sham and RADi mice. (A) Rotarod performance at 9 dpi and 30 dpi. Mice that experienced RADi showed much shorter duration on the rotarod than sham mice at 9 dpi but recovered at 30 dpi. (B) Y-maze test at 14 dpi and 28 dpi. Y-maze score but not number of arm entries significantly declined in RADi mice only at 28 dpi. (C) EPM at 14 dpi and 28 dpi. Mice that experienced RADi showed a robust increase in the time spent in the closed arms with a decreased interval spent in the open arms only at 28 dpi. However, a significant decrease in the frequency and total duration of head dips beyond the borders of the open arms was observed in mice with RADi at 14 dpi, which became progressively worse at 28 dpi. Data are presented as mean±s.d. and were analyzed by one-way with repeated-measures ANOVA followed by Tukey's post hoc test. *P<0.05, **P<0.01; n=9 for sham, n=9 for RADi at 9 dpi and 14 dpi, n=7 for RADi at 28 dpi and 30 dpi (two mice were lost for the late stages).

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Keywords

  • Abusive head trauma
  • Shaken baby syndrome
  • Rotational acceleration-deceleration injury
  • Ischemia
  • Hemorrhage
  • Neuronal degeneration

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RESEARCH ARTICLE
Pathophysiological and behavioral deficits in developing mice following rotational acceleration-deceleration traumatic brain injury
Guoxiang Wang, Yi Ping Zhang, Zhongwen Gao, Lisa B. E. Shields, Fang Li, Tianci Chu, Huayi Lv, Thomas Moriarty, Xiao-Ming Xu, Xiaoyu Yang, Christopher B. Shields, Jun Cai
Disease Models & Mechanisms 2018 11: dmm030387 doi: 10.1242/dmm.030387 Published 30 January 2018
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RESEARCH ARTICLE
Pathophysiological and behavioral deficits in developing mice following rotational acceleration-deceleration traumatic brain injury
Guoxiang Wang, Yi Ping Zhang, Zhongwen Gao, Lisa B. E. Shields, Fang Li, Tianci Chu, Huayi Lv, Thomas Moriarty, Xiao-Ming Xu, Xiaoyu Yang, Christopher B. Shields, Jun Cai
Disease Models & Mechanisms 2018 11: dmm030387 doi: 10.1242/dmm.030387 Published 30 January 2018

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