Hypothermic treatment after computer‑controlled compression in minipig: A preliminary report on the effect of epidural vs. direct spinal cord cooling
- Authors:
- Monika Zavodska
- Jan Galik
- Martin Marsala
- Stefania Papcunova
- Jaroslav Pavel
- Eniko Racekova
- Marcela Martoncikova
- Igor Sulla
- Miroslav Gajdos
- Imrich Lukac
- Jozef Kafka
- Valent Ledecky
- Igor Sulla
- Peter Reichel
- Alexandra Trbolova
- Igor Capik
- Katarina Bimbova
- Maria Bacova
- Andrea Stropkovska
- Alexandra Kisucka
- Dana Miklisova
- Nadezda Lukacova
-
Affiliations: Institute of Neurobiology, Biomedical Research Center, Slovak Academy of Sciences, 040 01 Košice, Slovakia, Department of Neurosurgery, Faculty of Medicine, University of Pavol Jozef Safarik, 040 66 Košice, Slovakia, Department of Small Animal Clinic, University of Veterinary Medicine and Pharmacy, 041 81 Košice, Slovakia, Department of Vector-borne Diseases, Institute of Parasitology, Slovak Academy of Sciences, 040 01 Košice, Slovakia - Published online on: October 5, 2018 https://doi.org/10.3892/etm.2018.6831
- Pages: 4927-4942
-
Copyright: © Zavodska et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Tator CH: Review of treatment trials in human spinal cord injury: Issues, difficulties, and recommendations. Neurosurgery. 59:957–987. 2006. View Article : Google Scholar : PubMed/NCBI | |
Tator CH: Update on the pathophysiology and pathology of acute spinal cord injury. Brain Pathol. 5:407–413. 1995. View Article : Google Scholar : PubMed/NCBI | |
McDonald JW and Sadowsky C: Spinal-cord injury. Lancet. 359:417–425. 2002. View Article : Google Scholar : PubMed/NCBI | |
Balentine JD: Pathology of experimental spinal cord trauma. I. The necrotic lesion as a function of vascular injury. Lab Invest. 39:236–253. 1978.PubMed/NCBI | |
Simard JM, Woo SK, Aarabi B and Gerzanich V: The Sur1-Trpm4 channel in spinal cord injury. J Spine Suppl. 4:0022013. | |
Rowland JW, Hawryluk GW, Kwon B and Fehlings MG: Current status of acute spinal cord injury pathophysiology and emerging therapies: Promise on the horizon. Neurosurg Focus. 25:E22008. View Article : Google Scholar : PubMed/NCBI | |
Bracken MB, Shepard MJ, Collins WF, Holford TR, Young W, Baskin DS, Eisenberg HM, Flamm E, Leo-Summers L, Maroon J, et al: A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury. Results of the Second National Acute Spinal Cord Injury Study. N Engl J Med. 322:1405–1411. 1990. View Article : Google Scholar : PubMed/NCBI | |
Wang J and Pearse DD: Therapeutic hypothermia in spinal cord injury: The status of its use and open questions. Int J Mol Sci. 16:16848–16879. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kwon BK, Okon E, Hillyer J, Mann C, Baptiste D, Weaver LC, Fehlings M and Tetzlaff W: A systematic review of non-invasive pharmacologic neuroprotective treatments for acute spinal cord injury. J Neurotrauma. 28:1545–1588. 2011. View Article : Google Scholar : PubMed/NCBI | |
Tetzlaff W, Okon EB, Karimi-Abdolrezaee S, Hill CE, Sparling JS, Plemel JR, Plunet WT, Tsai EC, Baptiste D, Smithson LJ, et al: A systematic review of cellular transplantation therapies for spinal cord injury. J Neurotrauma. 28:1611–1682. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wang B, Armstrong JS, Reyes M, Kulikowicz E, Lee JH, Spicer D, Bhalala U, Yang ZJ, Koehler RC, Martin LJ and Lee JK: White matter apoptosis is increased by delayed hypothermia and rewarming in a neonatal piglet model of hypoxic ischemic encephalopathy. Neuroscience. 316:296–310. 2016. View Article : Google Scholar : PubMed/NCBI | |
Martirosyan NL, Patel AA, Carotenuto A, Kalani MY, Bohl MA, Preul MC and Theodore N: The role of therapeutic hypothermia in the management of acute spinal cord injury. Clin Neurol Neurosurg. 154:79–88. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ok JH, Kim YH and Ha KY: Neuroprotective effects of hypothermia after spinal cord injury in rats: Comparative study between epidural hypothermia and systemic hypothermia. Spine (Phila Pa 1976). 37:E1551–E1559. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ha KY and Kim YH: Neuroprotective effect of moderate epidural hypothermia after spinal cord injury in rats. Spine (Phila Pa 1976). 33:2059–2065. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lo TP Jr, Cho KS, Garg MS, Lynch MS, Marcillo AE, Koivisto DL, Stagg M, Abril RM, Patel S, Dietrich WD and Pearse DD: Systemic hypothermia improves histological and functional outcome after cervical spinal cord contusion in rats. J Comp Neurol. 514:433–448. 2009. View Article : Google Scholar : PubMed/NCBI | |
Crowe MJ, Bresnahan JC, Shuman SL, Masters JN and Beattie MS: Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med. 3:73–76. 1997. View Article : Google Scholar : PubMed/NCBI | |
Shuman SL, Bresnahan JC and Beattie MS: Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res. 50:798–808. 1997. View Article : Google Scholar : PubMed/NCBI | |
Dumont RJ, Okonkwo DO, Verma S, Hurlbert RJ, Boulos PT, Ellegala DB and Dumont AS: Acute spinal cord injury, part I: Pathophysiologic mechanisms. Clin Neuropharmacol. 24:254–264. 2001. View Article : Google Scholar : PubMed/NCBI | |
Shibuya S, Miyamoto O, Janjua NA, Itano T, Mori S and Norimatsu H: Posttraumatic moderate systemic hypothermia reduces TUNEL positive cells following spinal cord injury in rat. Spinal Cord. 42:29–34. 2004. View Article : Google Scholar : PubMed/NCBI | |
Dietrich WD, Atkins CM and Bramlett HM: Protection in animal models of brain and spinal cord injury with mild to moderate hypothermia. J Neurotrauma. 26:301–312. 2009. View Article : Google Scholar : PubMed/NCBI | |
Grulova I, Slovinska L, Nagyova M, Cizek M and Cizkova D: The effect of hypothermia on sensory-motor function and tissue sparing after spinal cord injury. Spine J. 13:1881–1891. 2013. View Article : Google Scholar : PubMed/NCBI | |
Seo JY, Kim YH, Kim JW, Kim SI and Ha KY: Effects of therapeutic hypothermia on apoptosis and autophagy after spinal cord injury in rats. Spine (Phila Pa 1976). 40:883–890. 2015. View Article : Google Scholar : PubMed/NCBI | |
Strauch JT, Lauten A, Spielvogel D, Rinke S, Zhang N, Weisz D, Bodian CA and Griepp RB: Mild hypothermia protects the spinal cord from ischemic injury in a chronic porcine model. Eur J Cardiothorac Surg. 25:708–715. 2004. View Article : Google Scholar : PubMed/NCBI | |
Yoshitake A, Mori A, Shimizu H, Ueda T, Kabei N, Hachiya T, Okano H and Yozu R: Use of an epidural cooling catheter with a closed countercurrent lumen to protectagainst ischemic spinal cord injury in pigs. J Thorac Cardiovasc Surg. 134:1220–1226. 2007. View Article : Google Scholar : PubMed/NCBI | |
Inoue S, Mori A, Shimizu H, Yoshitake A, Tashiro R, Kabei N and Yozu R: Combined use of an epidural cooling catheter and systemic moderate hypothermia enhances spinal cord protection against ischemic injury in rabbits. J Thorac Cardiovasc Surg. 146:696–701. 2013. View Article : Google Scholar : PubMed/NCBI | |
Saito T, Saito S, Yamamoto H and Tsuchida M: Neuroprotection following mild hypothermia after spinal cord ischemia in rats. J Vasc Surg. 57:173–181. 2013. View Article : Google Scholar : PubMed/NCBI | |
Fay T: Early experiences with local and generalized refrigeration of the human brain. J Neurosurg. 16:239–260. 1959. View Article : Google Scholar : PubMed/NCBI | |
Tuzgen S, Kaynar MY, Güner A, Gümüştaş K, Belce A, Etuş V and Ozyurt E: The effect of epidural cooling on lipid peroxidation after experimental spinal cord injury. Spinal Cord. 36:654–657. 1998. View Article : Google Scholar : PubMed/NCBI | |
Kalayci M, Coskun O, Cagavi F, Kanter M, Armutcu F, Gul S and Acikgoz B: Neuroprotective effects of ebselen on experimental spinal cord injury in rats. Neurochem Res. 30:403–410. 2005. View Article : Google Scholar : PubMed/NCBI | |
Ji X, Luo Y, Ling F, Stetler RA, Lan J, Cao G and Chen J: Mild hypothermia diminishes oxidative DNA damage and pro-death signaling events after cerebral ischemia: A mechanism for neuroprotection. Front Biosci. 12:1737–1747. 2007. View Article : Google Scholar : PubMed/NCBI | |
Duz B, Kaplan M, Bilgic S, Korkmaz A and Kahraman S: Does hypothermic treatment provide an advantage after spinal cord injury until surgery? An experimental study. Neurochem Res. 34:407–410. 2009. View Article : Google Scholar : PubMed/NCBI | |
Topuz K, Colak A, Cemil B, Kutlay M, Demircan MN, Simsek H, Ipcioglu O, Kucukodaci Z and Uzun G: Combined hyperbaric oxygen and hypothermia treatment on oxidative stress parameters after spinal cord injury: An experimental study. Arch Med Res. 41:506–512. 2010. View Article : Google Scholar : PubMed/NCBI | |
Karamouzian S, Akhtarshomar S, Saied A and Gholamhoseinian A: Effects of methylprednisolone on neuroprotective effects of delay hypothermia on spinal cord injury in rat. Asian Spine J. 9:1–6. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wang D and Zhang J: Effects of hypothermia combined with neural stem cell transplantation on recovery of neurological function in rats with spinal cord injury. Mol Med Rep. 11:1759–1767. 2015. View Article : Google Scholar : PubMed/NCBI | |
Xu X, Li N, Zhu L, Zhou Y and Cheng H: Beneficial effects of local profound hypothermia and the possible mechanism after experimental spinal cord injury in rats. J Spinal Cord Med. 39:220–228. 2015. View Article : Google Scholar : PubMed/NCBI | |
Morino T, Ogata T, Takeba J and Yamamoto H: Microglia inhibition is a target of mild hypothermic treatment after the spinal cord injury. Spinal Cord. 46:425–431. 2008. View Article : Google Scholar : PubMed/NCBI | |
Horiuchi T, Kawaguchi M, Kurita N, Inoue S, Nakamura M, Konishi N and Furuya H: The long-term effects of mild to moderate hypothermia on gray and white matter injury after spinal cord ischemia in rats. Anesth Analg. 109:559–566. 2009. View Article : Google Scholar : PubMed/NCBI | |
Levi AD, Green BA, Wang MY, Dietrich WD, Brindle T, Vanni S, Casella G, Elhammady G and Jagid J: Clinical application of modest hypothermia after spinal cord injury. J Neurotrauma. 26:407–415. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ahmad FU, Wang MY and Levi AD: Hypothermia for acute spinal cord injury-a review. World Neurosurg. 82:207–214. 2014. View Article : Google Scholar : PubMed/NCBI | |
Casas CE, Herrera LP, Prusmack C, Ruenes G, Marcillo A and Guest JD: Effects of epidural hypothermic saline infusion on locomotor outcome and tissue preservation after moderate thoracic spinal cord contusion in rats. J Neurosurg Spine. 2:308–318. 2005. View Article : Google Scholar : PubMed/NCBI | |
Morochovic R, Chudá M, Talánová J, Cibur P, Kitka M and Vanický I: Local transcutaneous cooling of the spinal cord in the rat: Effects on long-term outcomes after compression spinal cord injury. Int J Neurosci. 118:555–568. 2008. View Article : Google Scholar : PubMed/NCBI | |
Morizane K, Ogata T, Morino T, Horiuchi H, Yamaoka G, Hino M and Miura H: A novel thermoelectric cooling device using Peltier modules for inducing local hypothermia of the spinal cord: The effect of local electrically controlled cooling for the treatment of spinal cord injuries in conscious rats. Neurosci Res. 72:279–282. 2012. View Article : Google Scholar : PubMed/NCBI | |
Barbosa MO, Cristante AF, Santos GB, Ferreira R, Marcon RM and Barros Filho TE: Neuroprotective effect of epidural hypothermia after spinal cord lesion in rats. Clinics (Sao Paulo). 69:559–564. 2014. View Article : Google Scholar : PubMed/NCBI | |
Albin MS, White RJ, Locke GS, Massopust LC Jr and Kretchmer HE: Localized spinal cord hypthermia-anesthetic effects and application to spinal cord injury. Anesth Analg. 46:8–16. 1967.PubMed/NCBI | |
Negrin J Jr: Spinal cord hypothermia in the neurosurgical management of the acute and chronic post-traumatic paraplegic patient. Paraplegia. 10:336–343. 1973. View Article : Google Scholar : PubMed/NCBI | |
Yashon D, Vise WM, Dewey RC and Hunt WE: Temperature of the spinal cord during local hypothermia in dogs. J Neurosurg. 39:742–745. 1973. View Article : Google Scholar : PubMed/NCBI | |
Dimar JR, Shields CB, Zhang YP, Burke DA, Raque GH and Glassman SD: The role of directly applied hypothermia in spinal cord injury. Spine (Phila Pa 1976). 25:2294–2302. 2000. View Article : Google Scholar : PubMed/NCBI | |
Chatzipanteli K, Yanagawa Y, Marcillo AE, Kraydieh S, Yezierski RP and Dietrich WD: Posstraumatic hypothermia reduced polymorphonuclear leukocyte accumulation following spinal cord injury in rats. J Neurotrauma. 17:321–332. 2000. View Article : Google Scholar : PubMed/NCBI | |
Cappuccino A, Bisson LJ, Carpenter B, Marzo J, Dietrich WD and Cappuccino H: The use of systemic hypothermia for the treatment of an acute cervical spinal cord injury in a professional football player. Spine (Phila Pa 1976). 35:E57–E62. 2010. View Article : Google Scholar : PubMed/NCBI | |
Levi AD, Casella G, Green BA, Dietrich WD, Vanni S, Jagid J and Wang MY: Clinical outcomes using modest intravascular hypothermia after acute cervical spinal cord injury. Neurosurgery. 66:670–677. 2010. View Article : Google Scholar : PubMed/NCBI | |
Albin MS, White RJ, Yashon D and Harris LS: Effects of localized cooling on spinal cord trauma. J Trauma. 9:1000–1008. 1969. View Article : Google Scholar : PubMed/NCBI | |
Black P and Markowitz RS: Experimental spinal cord injury in monkeys: Comparison of steroids and local hypothermia. Surg Forum. 22:409–411. 1971.PubMed/NCBI | |
Dididze M, Green BA, Dietrich WD, Vanni S, Wang MY and Levi AD: Systemic hypothermia in acute cervical spinal cord injury: A case-controlled study. Spinal Cord. 51:395–400. 2013. View Article : Google Scholar : PubMed/NCBI | |
MacLaren R, Gallagher J, Shin J, Varnado S and Nguyen L: Assessment of adverse events and predictors of neurological recovery after therapeutic hypothermia. Ann Pharmacother. 48:17–25. 2014. View Article : Google Scholar : PubMed/NCBI | |
Hansebout RR and Hansebout CR: Local cooling for traumatic spinal cord injury: Outcomes in 20 patients and review of the literature. J Neurosurg Spine. 20:550–561. 2014. View Article : Google Scholar : PubMed/NCBI | |
Navarro R, Juhas S, Keshavarzi S, Juhasova J, Motlik J, Johe K, Marsala S, Scadeng M, Lazar P, Tomori Z, et al: Chronic spinal compression model in minipigs: A systematic behavioral, qualitative, and quantitative neuropathological study. J Neurotrauma. 29:499–513. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gedrova S, Galik J, Marsala M, Zavodska M, Pavel J, Sulla I, Gajdos M, Lukac I, Kafka J, Ledecky V, et al: Neuroprotective effect of local hypothermia in a computer-controlled compression model in minipig: Correlation of tissue sparing along the rostro-caudal axis with neurological outcome. Exp Ther Med. 15:254–270. 2018.PubMed/NCBI | |
Sulla I, Boldizar M, Racekova E and Balik V: Experience with a thoracic laminectomy in minipigs. Folia Veterinaria. 56:35–39. 2012. | |
Lim SN, Gladman SJ, Dyall SC, Patel U, Virani N, Kang JX, Priestley JV and Michael-Titus AT: Transgenic mice with high endogenous omega-3 fatty acids are protected from spinal cord injury. Neurobiol Dis. 51:104–112. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tator CH and Fehlings MG: Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg. 75:15–26. 1991. View Article : Google Scholar : PubMed/NCBI | |
Rosenfeld JF, Vaccaro AR, Albert TJ, Klein GR and Cotler JM: The benefits of early decompression in cervical spinal cord injury. Am J Orthop (Belle Mead NJ). 27:23–28. 1998.PubMed/NCBI | |
Fehlings MG and Perrin RG: The timing of surgical intervention in the treatment of spinal cord injury: A systematic review of recent clinical evidence. Spine (Phila Pa 1976). 31 (11 Suppl):S28–S36. 2006. View Article : Google Scholar : PubMed/NCBI | |
Smith JS, Anderson R, Pham T, Bhatia N, Steward O and Gupta R: Role of early surgical decompression of the intradural space after cervical spinal cord injury in an animal model. J Bone Joint Surg Am. 92:1206–1214. 2010. View Article : Google Scholar : PubMed/NCBI | |
Perkins PG and Deane RH: Long-term follow-up of six patients with acute spinal injury following dural decompression. Injury. 19:397–401. 1988. View Article : Google Scholar : PubMed/NCBI | |
Phang I, Werndle MC, Saadoun S, Varsos G, Czosnyka M, Zoumprouli A and Papadopoulos MC: Expansion duroplasty improves intraspinal pressure, spinal cord perfusion pressure, and vascular pressure reactivity index in patients with traumatic spinal cord injury: Injured spinal cord pressure evaluation study. J Neurotrauma. 32:865–874. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kong CY, Hosseini AM, Belanger LM, Ronco JJ, Paquette SJ, Boyd MC, Dea N, Street J, Fisher CG, Dvorak MF and Kwon BK: A prospective evaluation of hemodynamic management in acute spinal cord injury patients. Spinal Cord. 51:466–471. 2013. View Article : Google Scholar : PubMed/NCBI | |
Iannotti C, Zhang YP, Shields LB, Han Y, Burke DA, Xu XM and Shields CB: Dural repair reduces connective tissue scar invasion and cystic cavity formation after acute spinal cord laceration injury in adult rats. J Neurotrauma. 23:853–865. 2006. View Article : Google Scholar : PubMed/NCBI | |
Desai A, Ball PA, Bekelis K, Lurie J, Mirza SK, Tosteson TD and Weinstein JN: SPORT: Does incidental durotomy affect long-term outcomes in cases of spinal stenosis? Neurosurgery. 69:38–44. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jones CF, Cripton PA and Kwon BK: Gross morphological changes of the spinal cord immediately after surgical decompression in a large animal model of traumatic spinal cord injury. Spine (Phila Pa 1976). 37:E890–E899. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jones CF, Newell RS, Lee JH, Cripton PA and Kwon BK: The pressure distribution of cerebrospinal fluid responds to residual compression and decompression in an animal model of acute spinal cord injury. Spine (Phila Pa 1976). 37:E1422–E1431. 2012. View Article : Google Scholar : PubMed/NCBI | |
Schumacher PA, Siman RG and Fehlings MG: Pretreatment with calpain inhibitor CEP-4143 inhibits calpain I activation and cytoskeletal degradation, improves neurological function, and enhances axonal survival after traumatic spinal cord injury. J Neurochem. 74:E1646–E1655. 2000. View Article : Google Scholar | |
Nishida F, Sisti MS, Zanuzzi CN, Barbeito CG and Portiansky EL: Neurons of the rat cervical spinal cord express vimentin and neurofilament after intraparenchymal injection of kainic acid. Neurosci Lett. 643:103–110. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lépinoux-Chambaud C and Eyer J: Review on intermediate filaments of the nervous system and their pathological alterations. Histochem Cell Biol. 140:13–22. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang H, Wu M, Zhan C, Ma E, Yang M, Yang X and Li Y: Neurofilament proteins in axonal regeneration and neurodegenerative diseases. Neural Regen Res. 7:620–626. 2012.PubMed/NCBI | |
Greig A, Donevan SD, Mujtaba TJ, Parks TN and Rao MS: Characterization of the AMPA-activated receptors present on motoneurons. J Neurochem. 74:179–191. 2000. View Article : Google Scholar : PubMed/NCBI | |
Vandenberghe W, Ihle EC, Patneau DK, Robberecht W and Brorson JR: AMPA receptor current density, not desensitization, predicts selective motoneuron vulnerability. J Neurosci. 20:7158–7166. 2000. View Article : Google Scholar : PubMed/NCBI | |
Van Den Bosch L and Robberecht W: Different receptors mediate motor neuron death induced by short and long exposures to excitotoxicity. Brain Res Bull. 53:383–388. 2000. View Article : Google Scholar : PubMed/NCBI | |
Lukáčová N, Kisucká A, Pavel J, Hricová L, Kucharíková A, Gálik J, Maršala M, Langfort J and Chalimoniuk M: Spinal cord transection modifies neuronal nitric oxide synthase expression in medullar reticular nuclei and in the spinal cord and increases parvalbumin immunopositivity in motoneurons below the site of injury in experimental rabbits. Acta Histochem. 114:518–524. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gillinov AM, Redmond JM, Zehr KJ, Troncoso JC, Arroyo S, Lesser RP, Lee AW, Stuart RS, Reitz BA and Baumgartner WA: Superior cerebral protection with profound hypothermia during circulatory arrest. Ann Thorac Surg. 55:1432–1439. 1993. View Article : Google Scholar : PubMed/NCBI | |
Mezrow CK, Midulla PS, Sadeghi AM, Gandsas A, Wang W, Dapunt OE, Zappulla R and Griepp RB: Evaluation of cerebral metabolism and quantitative electroencephalography after hypothermic circulatory arrest and low-flow cardiopulmonary bypass at different temperatures. J Thorac Cardiovasc Surg. 107:1006–1019. 1994.PubMed/NCBI | |
Lima B, Williams JB, Bhattacharya SD, Shah AA, Andersen N, Gaca JG and Hughes GC: Results of proximal arch replacement using deep hypothermia for circulatory arrest: Is moderate hypothermia really justifiable? Am Surg. 77:1438–1444. 2011.PubMed/NCBI | |
Vanický I, Marsala M, Gálik J and Marsala J: Epidural perfusion cooling protection against protracted spinal cord ischemia in rabbits. J Neurosurg. 79:736–741. 1993. View Article : Google Scholar : PubMed/NCBI | |
Lucas JH, Wang GF and Gross GW: NMDA antagonists prevent hypothermic injury and death of mammalian spinal neurons. J Neurotrauma. 7:229–236. 1990. View Article : Google Scholar : PubMed/NCBI | |
Romero-Sierra C, Hansebout R, Sierhuis A and Lewin M: A new method for localized spinal cord cooling. Med Biol Enf. 12:188–193. 1974. View Article : Google Scholar | |
Marsala M, Vanicky I, Galik J, Radonak J, Kundrat I and Marsala J: Panmyelic epidural cooling protects against ischemic spinal cord damage. J Surg Res. 55:21–31. 1993. View Article : Google Scholar : PubMed/NCBI | |
Marsala M, Galik J, Ishikawa T and Yaksh TL: Technique of selective spinal cord cooling in rat: Methodology and application. J Neurosci Methods. 74:97–106. 1997. View Article : Google Scholar : PubMed/NCBI | |
Teh DBL, Chua SM, Prasad A, Kakkos I, Jiang W, Yue M, Liu X and All AH: Neuroprotective assessment of prolonged local hypothermia post contusive spinal cord injury in rodent model. Spine J. 18:507–514. 2018. View Article : Google Scholar : PubMed/NCBI | |
Camara AK, Riess ML, Kevin LG, Novalija E and Stowe DF: Hypothermia augments reactive oxygen species detected in the guinea pig isolated perfused heart. Am J Physiol Heart Circ Physiol. 286:H1289–H1299. 2004. View Article : Google Scholar : PubMed/NCBI |