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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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ABSTRACT

Abusive head trauma (AHT) is the leading cause of death from trauma in infants and young children. An AHT animal model was developed on 12-day-old mice subjected to 90° head extension-flexion sagittal shaking repeated 30, 60, 80 and 100 times. The mortality and time until return of consciousness were dependent on the number of repeats and severity of the injury. Following 60 episodes of repeated head shakings, the pups demonstrated apnea and/or bradycardia immediately after injury. Acute oxygen desaturation was observed by pulse oximetry during respiratory and cardiac suppression. The cerebral blood perfusion was assessed by laser speckle contrast analysis (LASCA) using a PeriCam PSI system. There was a severe reduction in cerebral blood perfusion immediately after the trauma that did not significantly improve within 24 h. The injured mice began to experience reversible sensorimotor function at 9 days postinjury (dpi), which had completely recovered at 28 dpi. However, cognitive deficits and anxiety-like behavior remained. Subdural/subarachnoid hemorrhage, damage to the brain-blood barrier and parenchymal edema were found in all pups subjected to 60 insults. Proinflammatory response and reactive gliosis were upregulated at 3 dpi. Degenerated neurons were found in the cerebral cortex and olfactory tubercles at 30 dpi. This mouse model of repetitive brain injury by rotational head acceleration-deceleration partially mimics the major pathophysiological and behavioral events that occur in children with AHT. The resultant hypoxia/ischemia suggests a potential mechanism underlying the secondary rotational acceleration-deceleration-induced brain injury in developing mice.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: Y.P.Z., L.B.E.S., X.Y., C.B.S., J.C.; Methodology: Y.P.Z., Z.G., C.B.S., J.C.; Software: G.W., Y.P.Z., Z.G., T.C., J.C.; Validation: Y.P.Z., C.B.S., J.C.; Formal analysis: G.W., Y.P.Z., Z.G., F.L., T.C., H.L., J.C.; Investigation: G.W., Y.P.Z., Z.G., F.L., T.C., H.L., J.C.; Resources: X.Y., C.B.S., J.C.; Data curation: Y.P.Z., L.B.E.S., C.B.S., J.C.; Writing - original draft: G.W., Y.P.Z., J.C.; Writing - review & editing: Y.P.Z., L.B.E.S., T.C., T.M., X.-M.X., X.Y., C.B.S., J.C.; Visualization: G.W., L.B.E.S., T.C., C.B.S., J.C.; Supervision: Y.P.Z., X.Y., C.B.S., J.C.; Project administration: Y.P.Z., C.B.S., J.C.; Funding acquisition: G.W., Z.G., H.L., X.Y., C.B.S., J.C.

  • Funding

    This work was supported by the NeuroCures Foundation (J.C.), by a Kentucky Spinal Cord and Head Injury Research Board Research Grant (J.C. and C.B.S.), and partially by the National Natural Science Foundation of China (81350013, 31572217 to X.Y.; 81400998 to Z.G.; 81300769 to H.L.) and the China Scholarship Council (G.W.).

  • Supplementary information

    Supplementary information available online at http://dmm.biologists.org/lookup/doi/10.1242/dmm.030387.supplemental

  • Received April 27, 2017.
  • Accepted November 16, 2017.
  • © 2018. Published by The Company of Biologists Ltd

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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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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