Skip to main content

Cellular Inflammatory Response of the Spleen After Acute Spinal Cord Injury in Rat

Inflammation volume 42, pages 1630–1640 (2019)Cite this article

Abstract

Spinal cord injury (SCI) involves both primary and secondary damages. After the phase of primary injury, a series of inflammatory responses initiate, which belong to the secondary injury. There has been little investigation into the cellular inflammatory response of the spleen to SCI. To disclose the impact of SCI on the spleen, we examined the inflammatory reactions of the spleen during the acute phase of SCI in rat. Adult rats were used as experimental animals and divided into un-injured, sham, and SCI groups (n = 36). Contusion injuries were produced at the T3 vertebral level. Spinal cords were harvested 6 h, 24 h, 48 h, 72 h, 120 h, and 168 h after surgery and were prepared for immunohistochemistry. Spleen wet weight was measured. Blood and spleens were prepared for quantitative analyses. The spleen index was significantly decreased in the SCI groups. Immunohistochemical results showed an increase of the infiltrating cells in the spinal cord tissues from SCI rats at all time points, peaking in 72 h post injury. In the blood, T and B lymphocytes significantly decreased in the SCI group as compared with the sham group, while monocyte increased. Surprisingly, in the SCI group, neutrophil initially decreased and subsequently tended to return toward baseline levels, then remained elevated until the end of the study. Spleen analyses revealed a significant increase in monocyte and neutrophil but a minor (not statistically significant) reduction in T and B lymphocytes. Our data show that the four most prevalent inflammatory cells infiltrate the spinal cord after injury. Increased levels of inflammatory cells (monocyte and neutrophil) in the blood and spleen appear to be very sensitive to SCI. The spleen plays a critical role in the acute phase of SCI.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Moritz, C. 2018. A giant step for spinal cord injury research. Nature Neuroscience 21 (12): 1647–1648.

    Article  CAS  PubMed  Google Scholar 

  2. Savic, G., M.J. DeVivo, H.L. Frankel, M.A. Jamous, B.M. Soni, and S. Charlifue. 2017. Causes of death after traumatic spinal cord injury—a 70-year British study. Spinal Cord 55 (10): 891–897.

    Article  CAS  PubMed  Google Scholar 

  3. Zhao, F., X.Y. Ding, F. Wu, X.H. Li, Y.H. Li, M. Hu, and S.L. Huang. 2018. Relieving compression against injured spinal cord via non-suturing muscle layer in rat. Biomedical Research 29 (8): 1693–1696.

    Article  CAS  Google Scholar 

  4. Huang, S.L., L. Xiang, Y.J. Huang, F. Wang, L. Ji, J.L. Xue, and B.S. Lan. 2018. Electrophysiological monitoring techniques for spinal cord function in a canine model. International Journal of Clinical and Experimental Medicine 11 (6): 5986–5991.

    Google Scholar 

  5. Liu, J.J., X.Y. Ding, L. Xiang, F. Zhao, and S.L. Huang. 2017. A novel method for oxygen glucose deprivation model in organotypic spinal cord slices. Brain Research Bulletin 135: 163–169.

    Article  CAS  PubMed  Google Scholar 

  6. Liu, J.J., Y.J. Huang, L. Xiang, F. Zhao, and S.L. Huang. 2017. A novel method of organotypic spinal cord slice culture in rat. NeuroReport 28 (16): 1097–1102.

    Article  PubMed  Google Scholar 

  7. Li, X.H., F. Wu, F. Zhao, and S.L. Huang. 2017. Fractional anisotropy is a marker in early-stage spinal cord injury. Brain Research 1672: 44–49.

    Article  CAS  PubMed  Google Scholar 

  8. Huang, S.L., H.G. Qi, J.J. Liu, J.L. Li, Y.J. Huang, and L. Xiang. 2016. Alarm value of somatosensory-evoked potential in idiopathic scoliosis surgery. World Neurosurgery 92: 397–401.

    Article  PubMed  Google Scholar 

  9. Liu, J.J., Z. Guan, Z. Gao, L. Xiang, and S.L. Huang. 2016. Complications after spinal anesthesia in adult tethered cord syndrome. Medicine 95 (29): e4289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Huang, S.L., H.G. Qi, J.J. Liu, Y.J. Huang, and L. Xiang. 2015. A rare complication of spine surgery: Guillain–Barré syndrome. World Neurosurgery 84 (3): 697–701.

    Article  PubMed  Google Scholar 

  11. Li, X.H., J.B. Li, X.J. He, F. Wang, S.L. Huang, and Z.L. Bai. 2015. Timing of diffusion tensor imaging in the acute spinal cord injury of rats. Scientific Reports 5: 12639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Huang, S.L., Y.X. Liu, G.L. Yuan, J. Zhang, and H.W. Yan. 2015. Characteristics of lumbar disc herniation with exacerbation of presentation due to spinal manipulative therapy. Medicine 94 (12): e661.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Huang, S.L., J. Peng, G.L. Yuan, X.Y. Ding, and B.S. Lan. 2015. A new model of tethered cord syndrome produced by slow traction. Scientific Reports 5: 9116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Huang, S.L., X.J. He, L. Xiang, G.L. Yuan, N. Ning, and B.S. Lan. 2014. CT and MRI features of patients with diastematomyelia. Spinal Cord 52 (9): 689–692.

    Article  CAS  PubMed  Google Scholar 

  15. Huang, S.L., X.J. He, L. Lin, and B. Cheng. 2014. Neuroprotective effect of ginsenoside Rg1 against spinal cord ischemia and reperfusion in rats. Neurochemical Journal 8 (3): 199–204.

    Article  CAS  Google Scholar 

  16. Huang, S.L., X.J. He, Z.F. Li, L. Lin, and B. Cheng. 2014. Neuroprotective effects of ginsenoside Rg1 on oxygen-glucose deprivation reperfusion in PC12 cells. Pharmazie 69 (3): 208–211.

    CAS  PubMed  Google Scholar 

  17. Huang, S.L., H.X. Jiang, B. Cheng, N. Ning, and X.J. He. 2013. Characteristics and management of occult intrasacral extradural cyst in children. British Journal of Neurosurgery 27 (4): 509–512.

    Article  PubMed  Google Scholar 

  18. Huang, S.L., H.W. Yan, and K.Z. Wang. 2013. Use of Fidji cervical cage in the treatment of cervical spinal cord injury without radiographic abnormality. BioMed Research International 2013: 810172.

    PubMed  PubMed Central  Google Scholar 

  19. Huang, S.L., X.J. He, K.Z. Wang, and B.S. Lan. 2013. Diastematomyelia: A 35-year experience. Spine 38 (6): E344–E349.

    Article  PubMed  Google Scholar 

  20. Huang, S.L., W. Shi, and L.G. Zhang. 2012. Congenital dermal sinus of the cervical spine: Clinical characteristics and management. Journal of Neurosurgical Sciences 56 (1): 61–66.

    CAS  PubMed  Google Scholar 

  21. Huang, S.L., W. Shi, and L.G. Zhang. 2010. Characteristics and surgery of cervical myelomeningocele. Child’s Nervous System 26 (1): 87–91.

    Article  PubMed  Google Scholar 

  22. Huang, S.L., W. Shi, and L.G. Zhang. 2010. Surgical treatment for lipomyelomeningocele in children. World Journal of Pediatrics 6 (4): 361–365.

    Article  PubMed  Google Scholar 

  23. Hilton, B.J., A.J. Moulson, and W. Tetzlaff. 2017. Neuroprotection and secondary damage following spinal cord injury: Concepts and methods. Neuroscience Letters 652: 3–10.

    Article  CAS  PubMed  Google Scholar 

  24. Dantzer, R. 2018. Neuroimmune interactions: From the brain to the immune system and vice versa. Physiological Reviews 98 (1): 477–504.

    Article  CAS  PubMed  Google Scholar 

  25. Li, B., K. Concepcion, X. Meng, and L. Zhang. 2017. Brain-immune interactions in perinatal hypoxic-ischemic brain injury. Progress in Neurobiology 159: 50–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rust, R., and J. Kaiser. 2017. Insights into the dual role of inflammation after spinal cord injury. Journal of Neuroscience 37 (18): 4658–4660.

    Article  CAS  PubMed  Google Scholar 

  27. Orr, M.B., and J.C. Gensel. 2018. Spinal cord injury scarring and inflammation: Therapies targeting glial and inflammatory responses. Neurotherapeutics 15 (3): 541–553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hausmann, O.N. 2003. Post-traumatic inflammation following spinal cord injury. Spinal Cord 41 (7): 369–378.

    Article  CAS  PubMed  Google Scholar 

  29. Donnelly, D.J., and P.G. Popovich. 2008. Inflammation and its role in neuroprotection, axonal regeneration and functional recovery after spinal cord injury. Experimental Neurology 209 (2): 378–388.

    Article  CAS  PubMed  Google Scholar 

  30. de Menezes, M.F., F. Nicola, I.R.V. da Silva, A. Vizuete, V.R. Elsner, L.L. Xavier, C.A.S. Gonçalves, C.A. Netto, and R.G. Mestriner. 2018. Glial fibrillary acidic protein levels are associated with global histone H4 acetylation after spinal cord injury in rats. Neural Regeneration Research 13 (11): 1945–1952.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Seifert, H.A., A.A. Hall, C.B. Chapman, L.A. Collier, A.E. Willing, and K.R. Pennypacker. 2012. A transient decrease in spleen size following stroke corresponds to splenocyte release into systemic circulation. Journal of Neuroimmune Pharmacology 7 (4): 1017–1024.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wei, S., I. Kryczek, and W. Zou. 2006. Regulatory T-cell compartmentalization and trafficking. Blood 108 (2): 426–431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang, B., and J.C. Gensel. 2014. Is neuroinflammation in the injured spinal cord different than in the brain? Examining intrinsic differences between the brain and spinal cord. Experimental Neurology 258: 112–120.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by research grants from the National Natural Science Foundation of China (No. 81271340 and No. 81471247).

Author information

Author notes

  1. Feng Wu and Xiao-Yan Ding contributed equally to this work.

Affiliations

  1. Center of Teaching and Experiment for Medical Post Graduates, School of Medicine, Xi’an Jiaotong University, Xi’an, 710061, China

    Feng Wu

  2. Department of Ophthalmology, Xi’an No. 3 Hospital, Xi’an, 710021, China

    Xiao-Yan Ding

  3. Department of Radiology, The Second Affiliated Hospital, School of Medicine, Xi’an Jiaotong University, Xi’an, 710004, China

    Xiao-Hui Li

  4. Department of Neurology, The First Affiliated Hospital, School of Medicine, Xi’an Jiaotong University, Xi’an, 7100061, China

    Min-Jie Gong & Jia-Qi An

  5. Key Laboratory of Ministry of Health for Forensic Sciences, Xi’an Jiaotong University, Xi’an, 710061, China

    Jiang-Hua Lai

  6. Department of Orthopaedics, The Second Affiliated Hospital, School of Medicine, Xi’an Jiaotong University, Xi’an, 710004, China

    Sheng-Li Huang

Authors
  1. Feng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-Yan Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiao-Hui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Min-Jie Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jia-Qi An
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiang-Hua Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sheng-Li Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jiang-Hua Lai or Sheng-Li Huang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wu, F., Ding, XY., Li, XH. et al. Cellular Inflammatory Response of the Spleen After Acute Spinal Cord Injury in Rat. Inflammation 42, 1630–1640 (2019). https://doi.org/10.1007/s10753-019-01024-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-019-01024-y

KEY WORDS

  • spinal cord injury
  • spleen
  • immune
  • inflammatory
  • acute phase