Skip to main content

Advertisement

SpringerLink
Log in

Safe range of shortening the middle thoracic spine, an experimental study in canine

  • Original Article
  • Published:
European Spine Journal Aims and scope Submit manuscript

Abstract

Purpose

To determine the safe range of shortening the spinal column at middle thoracic spine and to observe the changes in blood-spinal cord barrier (BSCB), microglia/macrophage activation and inducible nitric oxide synthase (iNOS) activity after shortening-induced spinal cord injury.

Methods

Dogs were allocated to four groups. Group A (control) underwent laminectomy of T7 without shortening the spinal column. Groups B, C and D had 1/3, 1/2, and 2/3 of T7 resected, respectively, followed by spinal shortening. Somatosensory evoked potential (SSEP) and hind-limb function were recorded periodically for 14 days after operation. Spinal cord blood flow (SCBF) and BSCB were detected at the acute phase of shortening. Microglia/macrophage reactions and iNOS activity were observed by immunohistochemistry.

Results

Shortening of 1/3 of a vertebral height caused no significant changes in SSEP and hind-limb function after operation, whereas shortening of 1/2 of the height caused SSEP abnormality and paraparesis, and severe neurologic deficit of hind-limb was observed when the shortening reached 2/3 of the height. SCBF increased temporarily and showed a trend of recovery when the shortening was within 1/2 of a vertebral segment height. When it reached 1/2 or 2/3 of the height, SCBF at 6 h post-operation was 86.33% or 74.95% of the baseline, and an increasing BSCB permeability was observed. In the subsequent 7 days, obvious activation of macrophage and increased number of iNOS-positive cells were observed.

Conclusion

It is safe to shorten the spinal cord within 1/3 of a vertebral height in middle thoracic spine under two-segment laminectomy in canine. The BSCB disruption, macrophage activation, and increased iNOS activity were observed in the acute phase of the injury.

Graphic abstract

These slides can be retrieved under Electronic Supplementary Material.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  1. Yang C, Zheng Z, Liu H, Wang J, Kim YJ, Cho S (2016) Posterior vertebral column resection in spinal deformity: a systematic review. Eur Spine J 25(8):2368–2375

    Article  Google Scholar 

  2. Enercan M, Ozturk C, Kahraman S, Sarier M, Hamzaoglu A, Alanay A (2013) Osteotomies/spinal column resections in adult deformity. Eur Spine J 22(Suppl 2):S254–264

    Article  Google Scholar 

  3. Oka S, Matsumiya H, Shinohara S, Kuwata T, Takenaka M, Chikaishi Y, Hirai A, Imanishi N, Kuroda K, Yamada S, Uramoto H, Nakamura E, Tanaka F (2016) Total or partial vertebrectomy for lung cancer invading the spine. Ann Med Surg (Lond) 12:1–4

    Article  Google Scholar 

  4. Lin W, Xu H, Duan G, Xie J, Chen Y, Jiao B, Lan H (2018) Spine-shortening osteotomy for patients with tethered cord syndrome: a systematic review and meta-analysis. Neurol Res 40(5):340–363

    Article  Google Scholar 

  5. Kelly MP, Lenke LG, Godzik J, Pellise F, Shaffrey CI, Smith JS, Lewis SJ, Ames CP, Carreon LY, Fehlings MG, Schwab F, Shimer AL (2017) Retrospective analysis underestimates neurological deficits in complex spinal deformity surgery: a Scoli-RISK-1 study. J Neurosurg Spine 27(1):68–73

    Article  Google Scholar 

  6. Kawahara N, Tomita K, Kobayashi T, Abdel-Wanis ME, Murakami H, Akamaru T (2005) Influence of acute shortening on the spinal cord: an experimental study. Spine 30(6):613–620

    Article  Google Scholar 

  7. Ji L, Dang XQ, Lan BS, Wang KZ, Huang YJ, Wen B, Duan HH, Ren F (2013) Study on the safe range of shortening of the spinal cord in canine models. Spinal Cord 51(2):134–138

    Article  CAS  Google Scholar 

  8. Qiu F, Yang JC, Ma XY, Xu JJ, Yang QL, Zhou X, Xiao YS, Hu HS, Xia LH (2015) Relationship between spinal cord volume and spinal cord injury due to spinal shortening. PLoS ONE 10(5):e0127624

    Article  Google Scholar 

  9. Modi HN, Suh SW, Hong JY, Yang JH (2011) The effects of spinal cord injury induced by shortening on motor evoked potentials and spinal cord blood flow: an experimental study in Swine. J Bone Joint Surg Am 93(19):1781–1789

    Article  Google Scholar 

  10. Santillan A, Nacarino V, Greenberg E, Riina HA, Gobin YP, Patsalides A (2012) Vascular anatomy of the spinal cord. J Neurointerv Surg 4(1):67–74

    Article  Google Scholar 

  11. Bican O, Minagar A, Pruitt AA (2013) The spinal cord: a review of functional neuroanatomy. Neurol Clin 31(1):1–18

    Article  Google Scholar 

  12. Huang S, Xiang L, Huang Y, Wang F, Ji L (2018) Electrophysiological monitoring techniques for spinal cord function in a canine model. Int J Clin Exp Med 11(6):5986–5991

    Google Scholar 

  13. Freria CM, Hall JC, Wei P, Guan Z, McTigue DM, Popovich PG (2017) Deletion of the fractalkine receptor, CX3CR1, improves endogenous repair, axon sprouting, and synaptogenesis after spinal cord injury in mice. J Neurosci Off J Soc Neurosci 37(13):3568–3587

    Article  CAS  Google Scholar 

  14. Kobrine AI, Doyle TF, Martins AN (1975) Local spinal cord blood flow in experimental traumatic myelopathy. J Neurosurg 42(2):144–149

    Article  CAS  Google Scholar 

  15. Cawthon DF, Senter HJ, Stewart WB (1980) Comparison of hydrogen clearance and 14C-antipyrine autoradiography in the measurement of spinal cord blood flow after severe impact injury. J Neurosurg 52(6):801–807

    Article  CAS  Google Scholar 

  16. Martirosyan NL, Feuerstein JS, Theodore N, Cavalcanti DD, Spetzler RF, Preul MC (2011) Blood supply and vascular reactivity of the spinal cord under normal and pathological conditions. J Neurosurg Spine 15(3):238–251

    Article  Google Scholar 

  17. Fujimaki Y, Kawahara N, Tomita K, Murakami H, Ueda Y (2006) How many ligations of bilateral segmental arteries cause ischemic spinal cord dysfunction? An experimental study using a dog model. Spine 31(21):E781–789

    Article  Google Scholar 

  18. Ueda Y, Kawahara N, Tomita K, Kobayashi T, Murakami H, Nambu K (2005) Influence on spinal cord blood flow and function by interruption of bilateral segmental arteries at up to three levels: experimental study in dogs. Spine 30(20):2239–2243

    Article  Google Scholar 

  19. Kato S, Kawahara N, Tomita K, Murakami H, Demura S, Fujimaki Y (2008) Effects on spinal cord blood flow and neurologic function secondary to interruption of bilateral segmental arteries which supply the artery of Adamkiewicz: an experimental study using a dog model. Spine 33(14):1533–1541

    Article  Google Scholar 

  20. Mazensky D, Flesarova S, Sulla I (2017) Arterial blood supply to the spinal cord in animal models of spinal cord injury. A review. Anat Rec (Hoboken, NJ: 2007) 300(12):2091–2106

    Article  Google Scholar 

  21. Kobayashi S, Yoshizawa H, Shimada S, Guerrero AR, Miyachi M (2013) Changes of blood flow, oxygen tension, action potential and vascular permeability induced by arterial ischemia or venous congestion on the spinal cord in canine model. J Orthop Res Off Publ Orthop Res Soc 31(1):139–146

    Article  Google Scholar 

  22. Bartanusz V, Jezova D, Alajajian B, Digicaylioglu M (2011) The blood-spinal cord barrier: morphology and clinical implications. Ann Nneurol 70(2):194–206

    Article  Google Scholar 

  23. Maikos JT, Shreiber DI (2007) Immediate damage to the blood-spinal cord barrier due to mechanical trauma. J Neurotrauma 24(3):492–507

    Article  Google Scholar 

  24. Fan B, Wei Z, Yao X, Shi G, Cheng X, Zhou X, Zhou H, Ning G, Kong X, Feng S (2018) Microenvironment imbalance of spinal cord injury. Cell Transpl 27(6):853–866

    Article  Google Scholar 

  25. Casha S, Zygun D, McGowan MD, Bains I, Yong VW, Hurlbert RJ (2012) Results of a phase II placebo-controlled randomized trial of minocycline in acute spinal cord injury. Brain J Neurol 135(Pt 4):1224–1236

    Article  Google Scholar 

  26. Kumar H, Ropper AE, Lee SH, Han I (2017) Propitious therapeutic modulators to prevent blood-spinal cord barrier disruption in spinal cord injury. Mol Neurobiol 54(5):3578–3590

    Article  CAS  Google Scholar 

  27. Sharma HS (2011) Early microvascular reactions and blood-spinal cord barrier disruption are instrumental in pathophysiology of spinal cord injury and repair: novel therapeutic strategies including nanowired drug delivery to enhance neuroprotection. J Neural Transm 118(1):155–176

    Article  CAS  Google Scholar 

  28. Sharma HS, Vannemreddy P, Patnaik P, Patnaik S, Mohanty S (2006) Histamine receptors influence blood-spinal cord barrier permeability, edema formation, and spinal cord blood flow following trauma to the rat spinal cord. Acta Neurochir Supplement 96:316–321

    Article  CAS  Google Scholar 

  29. Loane DJ, Byrnes KR (2010) Role of microglia in neurotrauma. Neurother J Am Soc Exp Neurother 7(4):366–377

    Article  CAS  Google Scholar 

  30. Carlson SL, Parrish ME, Springer JE, Doty K, Dossett L (1998) Acute inflammatory response in spinal cord following impact injury. Exp Neurol 151(1):77–88

    Article  CAS  Google Scholar 

  31. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, Anderson AJ (2010) Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain A J Neurol 133(Pt 2):433

    Article  Google Scholar 

  32. Anwar MA, Shehabi TSA, Eid AH (2016) Inflammogenesis of secondary spinal cord injury. Front Cell Neurosci 10(98):1–24

    Google Scholar 

  33. David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12(7):388–399

    Article  CAS  Google Scholar 

  34. Bains M, Hall ED (1822) Antioxidant therapies in traumatic brain and spinal cord injury. Biochem Biophys Acta 5:675–684

    Google Scholar 

  35. Hall ED, Wang JA, Bosken JM, Singh IN (2016) Lipid peroxidation in brain or spinal cord mitochondria after injury. J Bioenerg Biomembr 48(2):169–174

    Article  CAS  Google Scholar 

  36. Ogura Y, Watanabe K, Hosogane N, Tsuji T, Ishii K, Nakamura M, Toyama Y, Chiba K, Matsumoto M (2011) Severe progressive scoliosis due to huge subcutaneous cavernous hemangioma: a case report. Scoliosis 6:3

    Article  Google Scholar 

  37. Arlet V, Odent T, Aebi M (2003) Congenital scoliosis. Eur Spine J 12(5):456–463

    Article  CAS  Google Scholar 

  38. Chu WC, Man GC, Lam WW, Yeung BH, Chau WW, Ng BK, Lam TP, Lee KM, Cheng JC (2008) Morphological and functional electrophysiological evidence of relative spinal cord tethering in adolescent idiopathic scoliosis. Spine 33(6):673–680

    Article  Google Scholar 

  39. Dearolf WW, Betz RR, Vogel LC, Levin J, Clancy M, Steel HH (1990) Scoliosis in pediatric spinal cord-injured patients. J Pediatr Orthop 10(2):214–218

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Natural Science Foundation of China (No. 81371347) and Key Research and Development Plan of Shaanxi Province (No. 2018ZDXM-SF-057).

Author information

Authors and Affiliations

  1. Department of Orthopedic Surgery, The Third Affiliated Hospital of Xi’an Jiaotong University (Shaanxi Provincial People’s Hospital), Xi’an, China

    Le Ji, Min Feng & Jingyuan Li

  2. Department of Gastroenterology, The Third Affiliated Hospital of Xi’an Jiaotong University (Shaanxi Provincial People’s Hospital), Xi’an, China

    Xiaoying Ma

  3. Department of Orthopedic Surgery, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, China

    Wenchen Ji

  4. Department of Orthopedic Surgery, The Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, China

    Shengli Huang, Yajuan Huang & Binshang Lan

  5. Department of Orthopedic Surgery, Honghui Hospital, Xi’an, China

    Lisong Heng

Authors
  1. Le Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoying Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenchen Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shengli Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Min Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingyuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lisong Heng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yajuan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Binshang Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. The animal models were performed by Le Ji, Wenchen Ji, Binshang Lan and Lisong Heng. SSEP monitoring was performed by Yajuan Huang and Min Feng. Material preparation, data collection and analysis were performed by Xiaoying Ma, Shengli Huang and Jingyuan Li. The first draft of the manuscript was written by Le Ji and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Binshang Lan.

Ethics declarations

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.

Conflict of interest

All 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.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 3239 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ji, L., Ma, X., Ji, W. et al. Safe range of shortening the middle thoracic spine, an experimental study in canine. Eur Spine J 29, 616–627 (2020). https://doi.org/10.1007/s00586-019-06268-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00586-019-06268-8

Keywords

Search

Navigation