Delayed neurological deterioration after surgery for intraspinal meningiomas: Ischemia-reperfusion injury in a rat model

Wu,Liang; Yang,Tao; Yang,Chenlong; Yao,Ning; Wang,Huiliang; Fang,Jingyi; Xu,Yulun

doi:10.3892/ol.2015.3626

Delayed neurological deterioration after surgery for intraspinal meningiomas: Ischemia-reperfusion injury in a rat model

Authors:
- Liang Wu
- Tao Yang
- Chenlong Yang
- Ning Yao
- Huiliang Wang
- Jingyi Fang
- Yulun Xu
View Affiliations

Affiliations: Department of Neurosurgery, China National Clinical Research Center for Neurological Diseases, Beijing Tiantan Hospital, Capital Medical University, Beijing 100050, P.R. China, Department of Physiology and Pharmacology, Karolinska Institute, Stockholm 11251, Sweden, College of Chemistry, Beijing Normal University, Beijing 100875, P.R. China, Department of Neuropathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100050, P.R. China
Published online on: August 19, 2015 https://doi.org/10.3892/ol.2015.3626
Pages: 2087-2094
Copyright: © Wu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Delayed neurological deterioration in the absence of direct cord insult following surgical removal and cord decompression is a rare but severe postoperative complication in a small subset of patients with intraspinal meningiomas. To date, the underlying pathophysiology of such a finding remains unclear and ischemia‑reperfusion injury (IRI) is considered as the potential etiology in the literature. However, no experimental research has been reported to prove this hypothesis. The present study investigated whether IRI occurs following decompression surgery using an experimental rat model of chronic compressive spinal cord injury (SCI). A chronic spinal cord compression model was developed with various sizes of polymer sheets (mild and severe compression) that were microsurgically implanted underneath the T8‑9 laminae, and occurrence of IRI in the spinal cord following decompression was determined by measuring superoxide dismutase (SOD) level and malondialdehyde (MDA) concentration. In the mild compression groups, after decompression SOD activities significantly increased along with a reduction in MDA content compared with the non‑decompression group (P<0.05), which exhibited diminishment of lipid peroxidation and relief of the secondary injury. These findings indicated that decompression is effective to improve neurological recovery and may deliver improved outcomes for chronic mild compression of the spinal cord. However, in severe compression groups, after decompression, SOD activities markedly reduced further along with a significant increase in MDA content compared with non‑decompression group (P<0.05). The results indicated that lipid peroxidation increased immediately after decompression surgery which resulted from reperfusion of the spinal cord. These findings demonstrated IRI may occur as a result of chronic severe compression of the spinal cord. In clinical practice, sudden cord expansion and reperfusion may have lead to disruption in the blood spinal cord barrier, and triggered a cascade of IRI resulting in postoperative neurologic deterioration. Recognition of this neurological deterioration following removal for intraspinal meningiomas may improve preoperative patient counseling and merits further study for determination of the precise pathophysiology.

View Figures

View References

1	Setzer M, Vatter H, Marquardt G, Seifert V and Vrionis FD: Management of spinal meningiomas: Surgical results and a review of the literature. Neurosurg Focus. 23:E142007. View Article : Google Scholar : PubMed/NCBI
2	Sandalcioglu IE, Hunold A, Müller O, Bassiouni H, Stolke D and Asgari S: Spinal meningiomas: Critical review of 131 surgically treated patients. Eur Spine J. 17:1035–1041. 2008. View Article : Google Scholar : PubMed/NCBI
3	Ambekar S, Sharma M, Kukreja S and Nanda A: Complications and outcomes of surgery for spinal meningioma: A nationwide inpatient sample analysis from 2003 to 2010. Clin Neurol Neurosurg. 118:65–68. 2014. View Article : Google Scholar : PubMed/NCBI
4	Taher F, Lebl DR, Cammisa FP, Pinter DW, Sun DY and Girardi FP: Transient neurological deficit following midthoracic decompression for severe stenosis: A series of three cases. Eur Spine J. 22:2057–2061. 2013. View Article : Google Scholar : PubMed/NCBI
5	Uematsu Y, Tokuhashi Y and Matsuzaki H: Radiculopathy after laminoplasty of the cervical spine. Spine (Phila Pa 1976). 23:2057–2062. 1998. View Article : Google Scholar : PubMed/NCBI
6	Chin KR, Seale J and Cumming V: ‘White cord syndrome’ of acute tetraplegia after anterior cervical decompression and fusion for chronic spinal cord compression: A case report. Case Rep Orthop. 2013:6979182013.PubMed/NCBI
7	Orchowski J, Bridwell KH and Lenke LG: Neurological deficit from a purely vascular etiology after unilateral vessel ligation during anterior thoracolumbar fusion of the spine. Spine (Phila Pa 1976). 30:406–410. 2005. View Article : Google Scholar : PubMed/NCBI
8	Lee KS, Shim JJ, Doh JW, Yoon SM, Bae HG and Yun IG: Transient paraparesis after laminectomy in a patient with multi-level ossification of the spinal ligament. J Korean Med Sci. 19:624–626. 2004. View Article : Google Scholar : PubMed/NCBI
9	Yang T, Wu L, Deng X, Yang C, Zhang Y, Zhang D and Xu Y: Delayed neurological deterioration with an unknown cause subsequent to surgery for intraspinal meningiomas. Oncol Lett. 9:2325–2330. 2015.PubMed/NCBI
10	Wisselink W, Money SR, Crockett DE, Nguyen JH, Becker MO, Farr GH and Hollier LH: Ischemia-reperfusion injury of the spinal cord: Protective effect of the hydroxyl radical scavenger dimethylthiourea. J Vasc Surg. 20:444–491. 1994. View Article : Google Scholar : PubMed/NCBI
11	Shan LQ, Ma S, Qiu XC, Zhou Y, Zhang Y, Zheng LH, Ren PC, Wang YC, Fan QY and Ma BA: Hydroxysafflor Yellow A protects spinal cords from ischemia/reperfusion injury in rabbits. BMC Neurosci. 11:982010. View Article : Google Scholar : PubMed/NCBI
12	Chan PH: Role of oxidants in ischemic brain damage. Stroke. 27:1124–1129. 1996. View Article : Google Scholar : PubMed/NCBI
13	Wilson JX and Gelb AW: Free radicals, antioxidants and neurologic injury: Possible relationship to cerebral protection by anesthetics. J Neurosurg Anesthesiol. 14:66–79. 2002. View Article : Google Scholar : PubMed/NCBI
14	Kim P, Haisa T, Kawamoto T, Kirino T and Wakai S: Delayed myelopathy induced by chronic compression in the rat spinal cord. Ann Neurol. 55:503–511. 2004. View Article : Google Scholar : PubMed/NCBI
15	Wang J, Rong W, Hu X, Liu X, Jiang L, Ma Y, Dang G, Liu Z and Wei F: Hyaluronan tetrasaccharide in the cerebrospinal fluid is associated with self-repair of rats after chronic spinal cord compression. Neuroscience. 210:467–480. 2012. View Article : Google Scholar : PubMed/NCBI
16	Basso DM, Beattie MS, Bresnahan JC, Anderson DK, Faden AI, Gruner JA, Holford TR, Hsu CY, Noble LJ, Nockels R, et al: MASCIS evaluation of open field locomotor scores: Effects of experience and teamwork on reliability multicenter animal spinal cord injury study. J. Neurotrauma. 13:343–359. 1996. View Article : Google Scholar : PubMed/NCBI
17	Kou J, Fischgrund J, Biddinger A and Herkowitz H: Risk factors for spinal epidural hematoma after spinal surgery. Spine (Phila Pa 1976). 27:1670–1673. 2002. View Article : Google Scholar : PubMed/NCBI
18	Cramer DE, Maher PC, Pettigrew DB and Kuntz C IV: Major neurologic deficit immediately after adult spinal surgery: Incidence and etiology over 10 years at a single training institution. J Spinal Disord Tech. 22:565–570. 2009. View Article : Google Scholar : PubMed/NCBI
19	Ahn JS, Lee JK and Kim BK: Prognostic factors that affect the surgical outcome of the laminoplasty in cervical spondylotic myelopathy. Clin Orthop Surg. 2:98–104. 2010. View Article : Google Scholar : PubMed/NCBI
20	Young WF and Baron E: Acute neurologic deterioration after surgical treatment for thoracic spinal stenosis. J Clin Neurosci. 8:129–132. 2001. View Article : Google Scholar : PubMed/NCBI
21	Sakaura H, Hosono N, Mukai Y, Ishii T and Yoshikawa H: C5 palsy after decompression surgery for cervical myelopathy: Review of the literature. Spine (Phila Pa 1976). 28:2447–2451. 2003. View Article : Google Scholar : PubMed/NCBI
22	Delattre JY, Arbit E, Thaler HT, Rosenblum MK and Posner JB: A dose-response study of dexamethasone in a model of spinal cord compression caused by epidural tumor. J Neurosurg. 70:920–925. 1989. View Article : Google Scholar : PubMed/NCBI
23	Manabe S, Tanaka H, Higo Y, Park P, Ohno T and Tateishi A: Experimental analysis of the spinal cord compressed by spinal metastasis. Spine (Phila Pa 1976). 14:1308–1315. 1989. View Article : Google Scholar : PubMed/NCBI
24	Ushio Y, Posner R, Posner JB and Shapiro WR: Experimental spinal cord compression by epidural neoplasm. Neurology. 27:422–429. 1977. View Article : Google Scholar : PubMed/NCBI
25	Ikeda H, Ushio Y, Hayakawa T and Mogami H: Edema and circulatory disturbance in the spinal cord compressed by epidural neoplasms in rabbits. J Neurosurg. 52:203–209. 1980. View Article : Google Scholar : PubMed/NCBI
26	Delattre JY, Arbit E, Rosenblum MK, Thaler HT, Lau N, Galicich JH and Posner JB: High dose versus low dose dexamethasone in experimental epidural spinal cord compression. Neurosurgery. 22:1005–1007. 1988. View Article : Google Scholar : PubMed/NCBI
27	Harkey HL, al-Mefty O, Marawi I, Peeler DF, Haines DE and Alexander LF: Experimental chronic compressive cervical myelopathy: Effects of decompression. J Neurosurg. 83:336–341. 1995. View Article : Google Scholar : PubMed/NCBI
28	Schramm J, Hashizume K, Fukushima T and Takahashi H: Experimental spinal cord injury produced by slow, graded compression: Alterations of cortical and spinal evoked potentials. J Neurosurg. 50:48–57. 1979. View Article : Google Scholar : PubMed/NCBI
29	Baba H, Maezawa Y, Uchida K, Imura S, Kawahara N, Tomita K and Kudo M: Three-dimensional topographic analysis of spinal accessory motoneurons under chronic mechanical compression: An experimental study in the mouse. J Neurol. 244:222–229. 1997. View Article : Google Scholar : PubMed/NCBI
30	Baba H, Furusawa N, Fukuda M, Maezawa Y, Imura S, Kawahara N, Nakahashi K and Tomita K: Potential role of streptozotocin in enhancing ossification of the posterior longitudinal ligament of the cervical spine in the hereditary spinal hyperostotic mouse (twy/twy). Eur J Histochem. 41:191–202. 1997.PubMed/NCBI
31	Furusawa N, Baba H, Imura S and Fukuda M: Characteristics and mechanism of the ossification of posterior longitudinal ligament in the tip-toe walking Yoshimura (twy) mouse. Eur J Histochem. 40:199–210. 1996.PubMed/NCBI
32	Okawa A, Nakamura I, Goto S, Moriya H, Nakamura Y and Ikegawa S: Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat Genet. 19:271–273. 1998. View Article : Google Scholar : PubMed/NCBI
33	Tator CH and Koyanagi L: Vascular mechanisms in the pathophysiology of human spinal cord injury. J Neurosurg. 86:483–492. 1997. View Article : Google Scholar : PubMed/NCBI
34	Gupta R, Singh M and Sharma A: Neuroprotective effect of antioxidants on ischaemia and reperfusion-induced cerebral in jury. Pharmacol Res. 48:209–215. 2003. View Article : Google Scholar : PubMed/NCBI
35	Ilhan A, Koltuksuz U, Ozen S, Uz E, Ciralik H and Akyol O: The effects of caffeic acid phenethyl ester (CAPE) on spinal cord ischemia/reperfusion injury in rabbits. Eur J Cardiothorac Surg. 16:458–463. 1999. View Article : Google Scholar : PubMed/NCBI
36	Golding JD, Rigley MacDonald ST, Juurlink BH and Rosser BW: The effect of glutamine on locomotor performance and skeletal muscle myosins following spinal cord injury in rats. J Appl Physiol (1985). 101:1045–1052. 2006. View Article : Google Scholar : PubMed/NCBI
37	Cemil B, Topuz K, Demircan MN, Kurt G, Tun K, Kutlay M, Ipcioglu O and Kucukodaci Z: Curcumin improves early functional results after experimental spinal cord injury. Acta Neurochir (Wien). 152:1583–1590. 2010. View Article : Google Scholar : PubMed/NCBI
38	Ferrari R, Ceconi C, Curello S, Cargnoni A, Alfiri O, Pardini A, Marzollo P and Visioli O: Oxygen free radicals and myocardial damage: Protective role of thiol-containing agents. Am J Med. 91:95S–105S. 1991. View Article : Google Scholar : PubMed/NCBI
39	Emmez H, Börcek AÖ, Kaymaz M, Kaymaz F, Durdağ E, Civi S, Gülbahar O, Aykol S and Paşaoğlu A: Neuroprotective effects of gabapentin in experimental spinal cord injury. World Neurosurg. 73:729–734. 2010. View Article : Google Scholar : PubMed/NCBI
40	Christie SD, Comeau B, Myers T, Sadi D, Purdy M and Mendez I: Duration of lipid peroxidation after acute spinal cord injury in rats and the effect of methylprednisolone. Neurosurg Focus. 25:E52008. View Article : Google Scholar : PubMed/NCBI