New Model of Ventral Spinal Cord Lesion Induced by Balloon Compression in Rats
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-10365S
Grantová Agentura České Republiky
CZ.02.1.01/0.0./0.0/15_003/0000419
Operational Programme Research, Development and Education in the framework of the project "Center of Reconstructive Neuroscience"
WFL-UK-008-15
Wings for Life
MR/R004544/1
Medical Research Council - United Kingdom
NRB119
International Spinal Research Trust
MR/S011110/1
Medical Research Council - United Kingdom
MR/R004463/1
Medical Research Council - United Kingdom
PubMed
33167447
PubMed Central
PMC7694490
DOI
10.3390/biomedicines8110477
PII: biomedicines8110477
Knihovny.cz E-zdroje
- Klíčová slova
- astrogliosis, ischemic compression injury, motoneurons, spinal tissue loss, ventral spinal cord injury,
- Publikační typ
- časopisecké články MeSH
Despite the variety of experimental models of spinal cord injury (SCI) currently used, the model of the ventral compression cord injury, which is commonly seen in humans, is very limited. Ventral balloon compression injury reflects the common anatomical mechanism of a human lesion and has the advantage of grading the injury severity by controlling the inflated volume of the balloon. In this study, ventral compression of the SCI was performed by the anterior epidural placement of the balloon of a 2F Fogarty's catheter, via laminectomy, at the level of T10. The balloon was rapidly inflated with 10 or 15 μL of saline and rested in situ for 5 min. The severity of the lesion was assessed by behavioral and immunohistochemical tests. Compression with the volume of 15 μL resulted in severe motor and sensory deficits represented by the complete inability to move across a horizontal ladder, a final Basso, Beattie and Bresnahan (BBB) score of 7.4 and a decreased withdrawal time in the plantar test (11.6 s). Histology and immunohistochemistry revealed a significant loss of white and gray matter with a loss of motoneuron, and an increased size of astrogliosis. An inflation volume of 10 μL resulted in a mild transient deficit. There are no other balloon compression models of ventral spinal cord injury. This study provided and validated a novel, easily replicable model of the ventral compression SCI, introduced by an inflated balloon of Fogarty´s catheter. For a severe incomplete deficit, an inflated volume should be maintained at 15 μL.
Department of Neuroscience Charles University 2nd Faculty of Medicine 15006 Prague Czech Republic
Faculty of Biological Sciences University of Leeds Leeds LS2 9JT UK
Institute of Experimental Medicine Czech Academy of Sciences Vídeňská 1083 Prague Czech Republic
Zobrazit více v PubMed
Hachem L.D., Ahuja C.S., Fehlings M.G. Assessment and management of acute spinal cord injury: From point of injury to rehabilitation. J. Spinal Cord Med. 2017;40:665–675. doi: 10.1080/10790268.2017.1329076. PubMed DOI PMC
Machova Urdzikova L., Karova K., Ruzicka J., Kloudova A., Shannon C., Dubisova J., Murali R., Kubinova S., Sykova E., Jhanwar-Uniyal M., et al. The Anti-Inflammatory Compound Curcumin Enhances Locomotor and Sensory Recovery after Spinal Cord Injury in Rats by Immunomodulation. Int. J. Mol. Sci. 2016;17:49. doi: 10.3390/ijms17010049. PubMed DOI PMC
Gonzalez R., Hickey M.J., Espinosa J.M., Nistor G., Lane T.E., Keirstead H.S. Therapeutic neutralization of CXCL10 decreases secondary degeneration and functional deficit after spinal cord injury in mice. Regen. Med. 2007;2:771–783. doi: 10.2217/17460751.2.5.771. PubMed DOI
Lima R., Monteiro S., Lopes J.P., Barradas P., Vasconcelos N.L., Gomes E.D., Assuncao-Silva R.C., Teixeira F.G., Morais M., Sousa N., et al. Systemic Interleukin-4 Administration after Spinal Cord Injury Modulates Inflammation and Promotes Neuroprotection. Pharmaceuticals. 2017;10:83. doi: 10.3390/ph10040083. PubMed DOI PMC
Krupa P., Svobodova B., Dubisova J., Kubinova S., Jendelova P., Machova Urdzikova L. Nano-formulated curcumin (Lipodisq) modulates the local inflammatory response, reduces glial scar and preserves the white matter after spinal cord injury in rats. Neuropharmacology. 2019;155:54–64. doi: 10.1016/j.neuropharm.2019.05.018. PubMed DOI
Dumont C.M., Margul D.J., Shea L.D. Tissue Engineering Approaches to Modulate the Inflammatory Milieu following Spinal Cord Injury. Cells Tissues Organs. 2016;202:52–66. doi: 10.1159/000446646. PubMed DOI PMC
Krupa P., Vackova I., Ruzicka J., Zaviskova K., Dubisova J., Koci Z., Turnovcova K., Urdzikova L.M., Kubinova S., Rehak S., et al. The Effect of Human Mesenchymal Stem Cells Derived from Wharton’s Jelly in Spinal Cord Injury Treatment Is Dose-Dependent and Can Be Facilitated by Repeated Application. Int. J. Mol. Sci. 2018;19:1503. doi: 10.3390/ijms19051503. PubMed DOI PMC
Zhao X.M., He X.Y., Liu J., Xu Y., Xu F.F., Tan Y.X., Zhang Z.B., Wang T.H. Neural Stem Cell Transplantation Improves Locomotor Function in Spinal Cord Transection Rats Associated with Nerve Regeneration and IGF-1 R Expression. Cell Transplant. 2019;28:1197–1211. doi: 10.1177/0963689719860128. PubMed DOI PMC
Li N., Leung G.K. Oligodendrocyte Precursor Cells in Spinal Cord Injury: A Review and Update. BioMed Res. Int. 2015;2015:235195. doi: 10.1155/2015/235195. PubMed DOI PMC
Ruzicka J., Machova-Urdzikova L., Gillick J., Amemori T., Romanyuk N., Karova K., Zaviskova K., Dubisova J., Kubinova S., Murali R., et al. A Comparative Study of Three Different Types of Stem Cells for Treatment of Rat Spinal Cord Injury. Cell Transplant. 2017;26:585–603. doi: 10.3727/096368916X693671. PubMed DOI PMC
Choi J.S., Leem J.W., Lee K.H., Kim S.S., Suh-Kim H., Jung S.J., Kim U.J., Lee B.H. Effects of human mesenchymal stem cell transplantation combined with polymer on functional recovery following spinal cord hemisection in rats. Korean J. Physiol. Pharmacol. Off. J. Korean Physiol. Soc. Korean Soc. Pharmacol. 2012;16:405–411. doi: 10.4196/kjpp.2012.16.6.405. PubMed DOI PMC
Lynskey J.V., Sandhu F.A., Dai H.N., McAtee M., Slotkin J.R., MacArthur L., Bregman B.S. Delayed intervention with transplants and neurotrophic factors supports recovery of forelimb function after cervical spinal cord injury in adult rats. J. Neurotrauma. 2006;23:617–634. doi: 10.1089/neu.2006.23.617. PubMed DOI
Tsai E.C., Dalton P.D., Shoichet M.S., Tator C.H. Matrix inclusion within synthetic hydrogel guidance channels improves specific supraspinal and local axonal regeneration after complete spinal cord transection. Biomaterials. 2006;27:519–533. doi: 10.1016/j.biomaterials.2005.07.025. PubMed DOI
Brock J.H., Rosenzweig E.S., Blesch A., Moseanko R., Havton L.A., Edgerton V.R., Tuszynski M.H. Local and remote growth factor effects after primate spinal cord injury. J. Neurosci. 2010;30:9728–9737. doi: 10.1523/JNEUROSCI.1924-10.2010. PubMed DOI PMC
Zhang H., Wu F., Kong X., Yang J., Chen H., Deng L., Cheng Y., Ye L., Zhu S., Zhang X. Nerve growth factor improves functional recovery by inhibiting endoplasmic reticulum stress-induced neuronal apoptosis in rats with spinal cord injury. J. Transl. Med. 2014;12:130. doi: 10.1186/1479-5876-12-130. PubMed DOI PMC
Ansorena E., De Berdt P., Ucakar B., Simón-Yarza T., Jacobs D., Schakman O., Jankovski A., Deumens R., Blanco-Prieto M.J., Préat V. Injectable alginate hydrogel loaded with GDNF promotes functional recovery in a hemisection model of spinal cord injury. Int. J. Pharm. 2013;455:148–158. doi: 10.1016/j.ijpharm.2013.07.045. PubMed DOI
Ichiyama R., Gerasimenko Y.P., Zhong H., Roy R., Edgerton V.R. Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci. Lett. 2005;383:339–344. doi: 10.1016/j.neulet.2005.04.049. PubMed DOI
Lavrov I., Musienko P.E., Selionov V.A., Zdunowski S., Roy R.R., Edgerton V.R., Gerasimenko Y. Activation of spinal locomotor circuits in the decerebrated cat by spinal epidural and/or intraspinal electrical stimulation. Brain Res. 2015;1600:84–92. doi: 10.1016/j.brainres.2014.11.003. PubMed DOI
Krupa P., Siddiqui A.M., Grahn P.J., Islam R., Chen B.K., Madigan N.N., Windebank A.J., Lavrov I.A. The Translesional Spinal Network and Its Reorganization after Spinal Cord Injury. Neurosci. Rev. J. Bringing Neurobiol. Neurol. Psychiatry. 2020 doi: 10.1177/1073858420966276. PubMed DOI
Metz G.A., Curt A., van de Meent H., Klusman I., Schwab M.E., Dietz V. Validation of the weight-drop contusion model in rats: A comparative study of human spinal cord injury. J. Neurotrauma. 2000;17:1–17. doi: 10.1089/neu.2000.17.1. PubMed DOI
Tator C.H. Update on the pathophysiology and pathology of acute spinal cord injury. Brain Pathol. 1995;5:407–413. doi: 10.1111/j.1750-3639.1995.tb00619.x. PubMed DOI
Dumont R.J., Okonkwo D.O., Verma S., Hurlbert R.J., Boulos P.T., Ellegala D.B., Dumont A.S. Acute spinal cord injury, part I: Pathophysiologic mechanisms. Clin. Neuropharmacol. 2001;24:254–264. doi: 10.1097/00002826-200109000-00002. PubMed DOI
Fehlings M.G., Smith J.S., Kopjar B., Arnold P.M., Yoon S.T., Vaccaro A.R., Brodke D.S., Janssen M.E., Chapman J.R., Sasso R.C. Perioperative and delayed complications associated with the surgical treatment of cervical spondylotic myelopathy based on 302 patients from the AOSpine North America Cervical Spondylotic Myelopathy Study: Presented at the 2011 Spine Section Meeting. J. Neurosurg. Spine. 2012;16:425–432. doi: 10.3171/2012.1.SPINE11467. PubMed DOI
Scheff S.W., Rabchevsky A.G., Fugaccia I., Main J.A., Lumpp J.E., Jr. Experimental modeling of spinal cord injury: Characterization of a force-defined injury device. J. Neurotrauma. 2003;20:179–193. doi: 10.1089/08977150360547099. PubMed DOI
Gruner J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma. 1992;9:123–128. doi: 10.1089/neu.1992.9.123. PubMed DOI
Vanicky I., Urdzikova L., Saganova K., Cizkova D., Galik J. A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J. Neurotrauma. 2001;18:1399–1407. doi: 10.1089/08977150152725687. PubMed DOI
Andrews E.M., Richards R.J., Yin F.Q., Viapiano M.S., Jakeman L.B. Alterations in chondroitin sulfate proteoglycan expression occur both at and far from the site of spinal contusion injury. Exp. Neurol. 2012;235:174–187. doi: 10.1016/j.expneurol.2011.09.008. PubMed DOI PMC
Amemori T., Ruzicka J., Romanyuk N., Jhanwar-Uniyal M., Sykova E., Jendelova P. Comparison of intraspinal and intrathecal implantation of induced pluripotent stem cell-derived neural precursors for the treatment of spinal cord injury in rats. Stem Cell Res. Ther. 2015;6:257. doi: 10.1186/s13287-015-0255-2. PubMed DOI PMC
Urdzikova L.M., Ruzicka J., LaBagnara M., Karova K., Kubinova S., Jirakova K., Murali R., Sykova E., Jhanwar-Uniyal M., Jendelova P. Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat. Int. J. Mol. Sci. 2014;15:11275–11293. doi: 10.3390/ijms150711275. PubMed DOI PMC
Su Y.F., Lin C.L., Lee K.S., Tsai T.H., Wu S.C., Hwang S.L., Chen S.C., Kwan A.L. A modified compression model of spinal cord injury in rats: Functional assessment and the expression of nitric oxide synthases. Spinal Cord. 2015;53:432–435. doi: 10.1038/sc.2014.245. PubMed DOI PMC
Chung W.H., Lee J.H., Chung D.J., Yang W.J., Lee A.J., Choi C.B., Chang H.S., Kim D.H., Chung H.J., Suh H.J., et al. Improved rat spinal cord injury model using spinal cord compression by percutaneous method. J. Vet. Sci. 2013;14:329–335. doi: 10.4142/jvs.2013.14.3.329. PubMed DOI PMC
Quertainmont R., Cantinieaux D., Botman O., Sid S., Schoenen J., Franzen R. Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions. PLoS ONE. 2012;7:e39500. doi: 10.1371/journal.pone.0039500. PubMed DOI PMC
Perrin F.E., Boniface G., Serguera C., Lonjon N., Serre A., Prieto M., Mallet J., Privat A. Grafted human embryonic progenitors expressing neurogenin-2 stimulate axonal sprouting and improve motor recovery after severe spinal cord injury. PLoS ONE. 2010;5:e15914. doi: 10.1371/journal.pone.0015914. PubMed DOI PMC
Bosch A., Stauffer E.S., Nickel V.L. Incomplete traumatic quadriplegia. A ten-year review. JAMA. 1971;216:473–478. doi: 10.1001/jama.1971.03180290049006. PubMed DOI
McKinley W., Santos K., Meade M., Brooke K. Incidence and outcomes of spinal cord injury clinical syndromes. J. Spinal Cord Med. 2007;30:215–224. doi: 10.1080/10790268.2007.11753929. PubMed DOI PMC
Adedigba J.A., Oremakinde A.A., Huang B., Maulucci C.M., Malomo A.O., Shokunbi T.M., Adeolu A.A. Preliminary Findings After Nonoperative Management of Traumatic Cervical Spinal Cord Injury on a Background of Degenerative Disc Disease: Providing Optimum Patient Care and Costs Saving in a Nigerian Setting. World Neurosurg. 2020;142:246–254. doi: 10.1016/j.wneu.2020.07.035. PubMed DOI
Pikija S., Mutzenbach J.S., Kunz A.B., Nardone R., Leis S., Deak I., McCoy M.R., Trinka E., Sellner J. Delayed Hospital Presentation and Neuroimaging in Non-surgical Spinal Cord Infarction. Front. Neurol. 2017;8:143. doi: 10.3389/fneur.2017.00143. PubMed DOI PMC
Kwiecien J.M., Dabrowski W., Dąbrowska-Bouta B., Sulkowski G., Oakden W., Kwiecien-Delaney C.J., Yaron J.R., Zhang L., Schutz L., Marzec-Kotarska B., et al. Prolonged inflammation leads to ongoing damage after spinal cord injury. PloS ONE. 2020;15:e0226584. doi: 10.1371/journal.pone.0226584. PubMed DOI PMC
Schucht P., Raineteau O., Schwab M.E., Fouad K. Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp. Neurol. 2002;176:143–153. doi: 10.1006/exnr.2002.7909. PubMed DOI
Schrimsher G.W., Reier P.J. Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat. Exp. Neurol. 1993;120:264–276. doi: 10.1006/exnr.1993.1060. PubMed DOI
Ijima Y., Furuya T., Koda M., Matsuura Y., Saito J., Kitamura M., Miyamoto T., Orita S., Inage K., Suzuki T., et al. Experimental rat model for cervical compressive myelopathy. Neuroreport. 2017;28:1239–1245. doi: 10.1097/WNR.0000000000000907. PubMed DOI PMC
Benzel E.C., Lancon J.A., Thomas M.M., Beal J.A., Hoffpauir G.M., Kesterson L. A new rat spinal cord injury model: A ventral compression technique. J. Spinal Disord. 1990;3:334–338. PubMed
al-Mefty O., Harkey H.L., Marawi I., Haines D.E., Peeler D.F., Wilner H.I., Smith R.R., Holaday H.R., Haining J.L., Russell W.F. Experimental chronic compressive cervical myelopathy. J. Neurosurg. 1993;79:550–561. doi: 10.3171/jns.1993.79.4.0550. PubMed DOI
Shinomiya K., Mutoh N., Furuya K. Study of experimental cervical spondylotic myelopathy. Spine. 1992;17:S383–S387. doi: 10.1097/00007632-199210001-00007. PubMed DOI
Lee J., Satkunendrarajah K., Fehlings M.G. Development and characterization of a novel rat model of cervical spondylotic myelopathy: The impact of chronic cord compression on clinical, neuroanatomical, and neurophysiological outcomes. J. Neurotrauma. 2012;29:1012–1027. doi: 10.1089/neu.2010.1709. PubMed DOI
Dhillon R.S., Parker J., Syed Y.A., Edgley S., Young A., Fawcett J.W., Jeffery N.D., Franklin R.J.M., Kotter M.R.N. Axonal plasticity underpins the functional recovery following surgical decompression in a rat model of cervical spondylotic myelopathy. Acta Neuropathol. Commun. 2016;4:89. doi: 10.1186/s40478-016-0359-7. PubMed DOI PMC
Urdzikova L., Vanicky I. Post-traumatic moderate systemic hyperthermia worsens behavioural outcome after spinal cord injury in the rat. Spinal Cord. 2006;44:113–119. doi: 10.1038/sj.sc.3101792. PubMed DOI
Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma. 1995;12:1–21. doi: 10.1089/neu.1995.12.1. PubMed DOI
Metz G.A., Whishaw I.Q. The ladder rung walking task: A scoring system and its practical application. J. Vis. Exp. 2009 doi: 10.3791/1204. PubMed DOI PMC
May Z., Fouad K., Shum-Siu A., Magnuson D.S.K. Challenges of animal models in SCI research: Effects of pre-injury task-specific training in adult rats before lesion. Behav. Brain Res. 2015;291:26–35. doi: 10.1016/j.bbr.2015.04.058. PubMed DOI PMC
Ruzicka J., Urdzikova L.M., Svobodova B., Amin A.G., Karova K., Dubisova J., Zaviskova K., Kubinova S., Schmidt M., Jhanwar-Uniyal M., et al. Does combined therapy of curcumin and epigallocatechin gallate have a synergistic neuroprotective effect against spinal cord injury? Neural Regen. Res. 2018;13:119–127. PubMed PMC
Svobodova B., Kloudova A., Ruzicka J., Kajtmanova L., Navratil L., Sedlacek R., Suchy T., Jhanwar-Uniyal M., Jendelova P., Machova Urdzikova L. The effect of 808 nm and 905 nm wavelength light on recovery after spinal cord injury. Sci. Rep. 2019;9:7660. doi: 10.1038/s41598-019-44141-2. PubMed DOI PMC
Ruzicka J., Urdzikova L.M., Kloudova A., Amin A.G., Vallova J., Kubinova S., Schmidt M.H., Jhanwar-Uniyal M., Jendelova P. Anti-inflammatory compound curcumin and mesenchymal stem cells in the treatment of spinal cord injury in rats. Acta Neurobiol. Exp. 2018;78:358–374. doi: 10.21307/ane-2018-035. PubMed DOI
Amemori T., Romanyuk N., Jendelova P., Herynek V., Turnovcova K., Prochazka P., Kapcalova M., Cocks G., Price J., Sykova E. Human conditionally immortalized neural stem cells improve locomotor function after spinal cord injury in the rat. Stem Cell Res. Ther. 2013;4:68. doi: 10.1186/scrt219. PubMed DOI PMC
Lee D.H., Lee J.K. Animal models of axon regeneration after spinal cord injury. Neurosci. Bull. 2013;29:436–444. doi: 10.1007/s12264-013-1365-4. PubMed DOI PMC
Kwon B.K., Hillyer J., Tetzlaff W. Translational research in spinal cord injury: A survey of opinion from the SCI community. J. Neurotrauma. 2010;27:21–33. doi: 10.1089/neu.2009.1048. PubMed DOI
Young W. Animal Models of Acute Neurological Injuries. Springer; Berlin/Heidelberg, Germany: 2009. MASCIS spinal cord contusion model; pp. 411–421.
Khan T., Havey R.M., Sayers S.T., Patwardhan A., King W.W. Animal models of spinal cord contusion injuries. Lab. Anim. Sci. 1999;49:161–172. PubMed
Talac R., Friedman J.A., Moore M.J., Lu L., Jabbari E., Windebank A.J., Currier B.L., Yaszemski M.J. Animal models of spinal cord injury for evaluation of tissue engineering treatment strategies. Biomaterials. 2004;25:1505–1510. doi: 10.1016/S0142-9612(03)00497-6. PubMed DOI
Krishna V., Andrews H., Jin X., Yu J., Varma A., Wen X., Kindy M. A contusion model of severe spinal cord injury in rats. J. Vis. Exp. 2013 doi: 10.3791/50111. PubMed DOI PMC
Rivlin A., Tator C. Effect of duration of acute spinal cord compression in a new acute cord injury model in the rat. Surg. Neurol. 1978;10:38–43. PubMed
Aslan A., Cemek M., Eser O., Altunbaş K., Buyukokuroglu M.E., Cosar M., Baş O., Ela Y., Fidan H. Does dexmedetomidine reduce secondary damage after spinal cord injury? An experimental study. Eur. Spine J. 2009;18:336. doi: 10.1007/s00586-008-0872-x. PubMed DOI PMC
Fukuda S., Nakamura T., Kishigami Y., Endo K., Azuma T., Fujikawa T., Tsutsumi S., Shimizu Y. New canine spinal cord injury model free from laminectomy. Brain Res. Protoc. 2005;14:171–180. doi: 10.1016/j.brainresprot.2005.01.001. PubMed DOI
Nesathurai S., Graham W.A., Mansfield K., Magill D., Sehgal P., Westmoreland S.V., Prusty S., Rosene D.L., Sledge J.B. Model of traumatic spinal cord injury in Macaca fascicularis: Similarity of experimental lesions created by epidural catheter to human spinal cord injury. J. Med. Primatol. 2006;35:401–404. doi: 10.1111/j.1600-0684.2006.00162.x. PubMed DOI
Hukuda S., Wilson C.B. Experimental cervical myelopathy: Effects of compression and ischemia on the canine cervical cord. J. Neurosurg. 1972;37:631–652. doi: 10.3171/jns.1972.37.6.0631. PubMed DOI
Wolfla C.E., Snell B.E., Honeycutt J.H. Cervical ventral epidural pressure response to graded spinal canal compromise and spinal motion. Spine. 2004;29:1524–1529. doi: 10.1097/01.BRS.0000131442.87202.39. PubMed DOI
Šedý J., Zicha J., Kuneš J., Jendelová P., Syková E. Rapid but not slow spinal cord compression elicits neurogenic pulmonary edema in the rat. Physiol. Res. 2009;58:269–277. PubMed