Restricted accessResearch articleFirst published online 2021-11
Duraplasty in Traumatic Thoracic Spinal Cord Injury: Impact on Spinal Cord Hemodynamics,Tissue Metabolism,Histology,and Behavioral Recovery Using a Porcine Model
After acute traumatic spinal cord injury (SCI), the spinal cord can swell to fill the subarachnoid space and become compressed by the surrounding dura. In a porcine model of SCI, we performed a duraplasty to expand the subarachnoid space around the injured spinal cord and evaluated how this influenced acute intraparenchymal hemodynamic and metabolic responses, in addition to histological and behavioral recovery. Female Yucatan pigs underwent a T10 SCI, with or without duraplasty. Using microsensors implanted into the spinal cord parenchyma, changes in blood flow (ΔSCBF), oxygenation (ΔPO2), and spinal cord pressure (ΔSCP) during and after SCI were monitored, alongside metabolic responses. Behavioral recovery was tested weekly using the Porcine Injury Behavior Scale (PTIBS). Thereafter, spinal cords were harvested for tissue sparing analyses. In both duraplasty and non-animals, the ΔSCP increased ∼5 mm Hg in the first 6 h post-injury. After this, the SCP appeared to be slightly reduced in the duraplasty animals, although the group differences were not statistically significant after controlling for injury severity in terms of impact force. During the first seven days post-SCI, the ΔSCBF or ΔPO2 values were not different between the duraplasty and control animals. Over 12 weeks, there was no improvement in hindlimb locomotion as assessed by PTIBS scores and no reduction in tissue damage at the injury site in the duraplasty animals. In our porcine model of SCI, duraplasty did not provide any clear evidence of long-term behavioral or tissue sparing benefit after SCI.
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References
1.
FurlanJ.C., NoonanV., CadotteD.W., and FehlingsM.G. (2011). Timing of decompressive surgery of spinal cord after traumatic spinal cord injury: an evidence-based examination of pre-clinical and clinical studies. J. Neurotrauma, 28, 1371–1399.
2.
BadhiwalaJ.H., WilsonJ.R., WitiwC.D., HarropJ.S., VaccaroA.R., AarabiB., GrossmanR.G., GeislerF.H., and FehlingsM.G. (2021). The influence of timing of surgical decompression for acute spinal cord injury: a pooled analysis of individual patient data. Lancet Neurol. 20, 117–126.
3.
FehlingsM.G., VaccaroA., WilsonJ.R., SinghA., CadotteD.W., HarropJ.S., AarabiB., ShaffreyC., DvorakM., FisherC., ArnoldP., MassicotteE.M., LewisS., and RampersaudR. (2012). Early versus delayed decompression for traumatic cervical spinal cord injury: Results of the Surgical Timing in Acute Spinal Cord Injury Study (STASCIS). PLoS One, 7, e32037.
4.
SaadounS., WerndleM.C., Lopez de HerediaL., and PapadopoulosM.C. (2016). The dura causes spinal cord compression after spinal cord injury. Br. J. Neurosurg. 30, 582–584.
5.
JonesC.F., CriptonP.A., and KwonB.K. (2012). 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.
6.
WerndleM.C., SaadounS., PhangI., CzosnykaM., VarsosG. V., CzosnykaZ.H., SmielewskiP., JamousA., BellB.A., ZoumprouliA., and PapadopoulosM.C. (2014). Monitoring of spinal cord perfusion pressure in acute spinal cord injury: initial findings of the injured spinal cord pressure evaluation study*. Crit. Care Med. 42, 646–655.
7.
PhangI., and PapadopoulosM.C. (2015). Intraspinal pressure monitoring in a patient with spinal cord injury reveals different intradural compartments: Injured Spinal Cord Pressure Evaluation (ISCoPE) Study. Neurocrit. Care, 23, 414–418.
8.
SaadounS., and PapadopoulosM.C. (2016). Spinal cord injury: is monitoring from the injury site the future?. Crit. Care, 20, 308.
9.
PhangI., WerndleM.C., SaadounS., VarsosG., CzosnykaM., ZoumprouliA., and PapadopoulosM.C. (2015). 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.
10.
Bor-Seng-ShuE., TeixeiraM.J., HirschR., de AndradeA.F., and MarinoR. (2004). Transcranial doppler sonography in two patients who underwent decompressive craniectomy for traumatic brain swelling: report of two cases. Arq. Neuropsiquiatr. 62, 715–721.
11.
FigajiA.A., FieggenA.G., SandlerS.J.I., ArgentA.C., Le RouxP.D., and PeterJ.C. (2007). Intracranial pressure and cerebral oxygenation changes after decompressive craniectomy in a child with traumatic brain swelling. Childs Nerv. Syst. 23, 1331–1335.
12.
LeeJ.H., JonesC.F., OkonE.B., AndersonL., TigchelaarS., KoonerP., GodbeyT., ChuaB., GrayG., HildebrandtR., CriptonP., TetzlaffW., and KwonB.K. (2013). A novel porcine model of traumatic thoracic spinal cord injury. J. Neurotrauma, 30, 142–159.
13.
KimK.T., StreijgerF., ManouchehriN., SoK., ShorttK., OkonE.B., TigchelaarS., CriptonP., and KwonB.K. (2018). Review of the UBC porcine model of traumatic spinal cord injury. J. Korean Neurosurg. Soc. 61, 539–547.
14.
StrauchJ.T., LautenA., ZhangN., WahlersT., and GrieppR.B. (2007). Anatomy of spinal cord blood supply in the pig. Ann. Thorac. Surg. 83, 2130–2134.
15.
StrauchJ.T., SpielvogelD., LautenA., ZhangN., ShiangH., WeiszD., BodianC.A., and GrieppR.B. (2003). Importance of extrasegmental vessels for spinal cord blood supply in a chronic porcine model. Eur. J. Cardiothorac. Surg. 24, 817–824.
16.
EtzC.D., KariF.A., MuellerC.S., SilovitzD., BrennerR.M., LinH.M., and GrieppR.B. (2011). The collateral network concept: a reassessment of the anatomy of spinal cord perfusion. J. Thorac. Cardiovasc. Surg. 141, 1020–1028.
17.
StreijgerF., SoK., ManouchehriN., TigchelaarS., LeeJ.H., OkonE.B., ShorttK., KimS.E., McInnesK., McInnesK., CriptonP., and KwonB.K. (2017). Changes in pressure, hemodynamics, and metabolism within the spinal cord during the first 7 days after injury using a porcine model. J. Neurotrauma, 34, 3336–3350.
18.
KimK.T., StreijgerF., SoK., ManouchehriN., ShorttK., OkonE.B., TigchelaarS., FongA., MorrisonC., KeungM., SunJ., LiuE., CriptonP.A., and KwonB.K. (2019). Differences in morphometric measures of the uninjured porcine spinal cord and dural sac predict histological and behavioral outcomes after traumatic spinal cord injury. J. Neurotrauma, 36, 3005–30017.
19.
JonesC.F., KwonB.K., and CriptonP.A. (2012). Mechanical indicators of injury severity are decreased with increased thecal sac dimension in a bench-top model of contusion type spinal cord injury. J. Biomech. 45, 1003–1010.
20.
TimofeevI., CarpenterK.L., NortjeJ., Al-RawiP.G., O'ConnellM.T., CzosnykaM., SmielewskiP., PickardJ.D., MenonD.K., KirkpatrickP.J., GuptaA.K., and HutchinsonP.J. (2011). Cerebral extracellular chemistry and outcome following traumatic brain injury: a microdialysis study of 223 patients. Brain, 134, 484–494.
21.
CheungA., TuL., ManouchehriN., KimK.T., SoK., WebsterM., FiskS., TigchelaarS., DalkilicS.S., SayreE.C., StreijgerF., MacNabA., KwonB.K., and ShadganB. (2020). Continuous optical monitoring of spinal cord oxygenation and hemodynamics during the first seven days post-injury in a porcine model of acute spinal cord injury. J. Neurotrauma, 37, 2292–2301.
22.
WerndleM.C., ZoumprouliA., SedgwickP., and PapadopoulosM.C. (2012). Variability in the treatment of acute spinal cord injury in the United Kingdom: results of a national survey. J. Neurotrauma, 29, 880–888.
23.
FehlingsM.G., RabinD., SearsW., CadotteD.W., and AarabiB. (2010). Current practice in the timing of surgical intervention in spinal cord injury. Spine (Phila. Pa. 1976). 35, S166–S173.
24.
KhaingZ.Z., CatesL.N., FischedickA.E., McclinticA.M., MouradP.D., and HofstetterC.P. (2017). Temporal and spatial evolution of raised intraspinal pressure after traumatic spinal cord injury. J. Neurotrauma, 34, 645–651.
25.
HarwellD.M., GibsonJ.L., FesslerR.D., HoltzJ., PettigrewD.B., and KuntzC. (2016). Pia mater significantly contributes to spinal cord intraparenchymal pressure in a simulated model of edema. Spine (Phila. Pa. 1976). 41, E524–E529.
26.
LindsbergP.J., O'NeillJ.T., PaakkariI.A., HallenbeckJ.M., and FeuersteinG. (1989). Validation of laser-Doppler flowmetry in measurement of spinal cord blood flow. Am. J. Physiol. - Hear. Circ. Physiol. 257, H674–H680.
27.
HamamotoY., OgataT., MorinoT., HinoM., and YamamotoH. (2007). Real-time direct measurement of spinal cord blood flow at the site of compression: relationship between blood flow recovery and motor deficiency in spinal cord injury. Spine (Phila. Pa. 1976). 32, 1955–1962.
28.
SoubeyrandM., LaemmelE., CourtC., DuboryA., VicautE., and DuranteauJ. (2013). Rat model of spinal cord injury preserving dura mater integrity and allowing measurements of cerebrospinal fluid pressure and spinal cord blood flow. Eur. Spine J. 22, 1810–1819.
29.
PhillipsJ.P., Cibert-GotonV., LangfordR.M., and ShortlandP.J. (2013). Perfusion assessment in rat spinal cord tissue using photoplethysmography and laser Doppler flux measurements. J. Biomed. Opt. 18, 037005.
30.
KramerM.S., VinallP.E., KatolikL.I., and SimeoneF.A. (1996). Comparison of cerebral blood flow measured by laser-Doppler flowmetry and hydrogen clearance in cats after cerebral insult and hypervolemic hemodilution. Neurosurgery, 38, 355–361.
31.
SkarphedinssonJ.O., HårdingH., and ThorénP. (1988). Repeated measurements of cerebral blood flow in rats. Comparisons between the hydrogen clearance method and laser Doppler flowmetry. Acta Physiol. Scand. 134, 133–142.
32.
LindsbergP.J., JacobsT.P., FrerichsK.U., HallenbeckJ.M., and FeuersteinG.Z. (1992). Laser-Doppler flowmetry in monitoring regulation of rapid microcirculatory changes in spinal cord. Am. J. Physiol. 263, H285–H292.
33.
YamadaT., MorimotoT., NakaseH., HirabayashiH., HiramatsuK.I., and SakakiT. (1998). Spinal cord blood flow and pathophysiological changes after transient spinal cord ischemia in cats. Neurosurgery, 42, 626–634.
34.
WestergrenH., FarooqueM., OlssonY., and HoltzA. (2001). Spinal cord blood flow changes following systemic hypothermia and spinal cord compression injury: an experimental study in the rat using Laser-Doppler flowmetry. Spinal Cord, 39, 74–84.
35.
MartirosyanN.L., KalaniM.Y.S., BichardW.D., BaajA.A., Fernando GonzalezL., PreulM.C., and TheodoreN. (2015). Cerebrospinal fluid drainage and induced hypertension improve spinal cord perfusion after acute spinal cord injury in pigs. Neurosurgery, 76, 461–468.
36.
MarsalaM., SorkinL.S., and YakshT.L. (1994). Transient spinal ischemia in rat: characterization of spinal cord blood flow, extracellular amino acid release, and concurrent histopathological damage. J. Cereb. Blood Flow Metab. 14, 604–614.
37.
JiaZ.Q., LiG., ZhangZ.Y., LiH.T., WangJ.Q., FanZ.K., and LvG. (2016). Time representation of mitochondrial morphology and function after acute spinal cord injury. Neural Regen. Res. 11, 137–143.
38.
McEwenM.L., SullivanP.G., RabchevskyA.G., and SpringerJ.E. (2011). Targeting mitochondrial function for the treatment of acute spinal cord injury. Neurotherapeutics, 8, 168–179.
39.
ØstergaardL., EngedalT.S., AamandR., MikkelsenR., IversenN.K., AnzabiM., Næss-SchmidtE.T., DrasbekK.R., BayV., BlicherJ.U., TietzeA., MikkelsenI.K., HansenB., JespersenS.N., JuulN., SørensenJ.C.H., and RasmussenM. (2014). Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury. J. Cereb. Blood Flow Metab. 34, 1585–1598.
40.
SoustielJ.F., SviriG.E., MahamidE., ShikV., AbeshausS., and ZaaroorM. (2010). Cerebral blood flow and metabolism following decompressive craniectomy for control of increased intracranial pressure. Neurosurgery, 67, 65–72.
41.
TichauerK.M., BrownD.W., HadwayJ., LeeT.Y., and St. LawrenceK. (2006). Near-infrared spectroscopy measurements of cerebral blood flow and oxygen consumption following hypoxia-ischemia in newborn piglets. J. Appl. Physiol. 100, 850–857.
42.
DellazizzoL., DemersS.P., CharbonneyE., WilliamsV., SerriK., AlbertM., GiguèreJ.F., LarocheM., WilliamsonD., and BernardF. (2018). Minimal PaO2 threshold after traumatic brain injury and clinical utility of a novel brain oxygenation ratio. J. Neurosurg. Online ahead of. print.
43.
RaganD.K., McKinstryR., BenzingerT., LeonardJ., and PinedaJ.A. (2012). Depression of whole-brain oxygen extraction fraction is associated with poor outcome in pediatric traumatic brain injury. Pediatr. Res. 71, 199–204.
WilcoxR.K., BoergerT.O., HallR.M., BartonD.C., LimbD., and DicksonR.A. (2002). Measurement of canal occlusion during the thoracolumbar burst fracture process. J. Biomech. 35, 381–384.
46.
PanjabiM.M., KifuneM., WenL., ArandM., OxlandT.R., LinR.M., Steve YoonW.S., and VasavadaA. (1995). Dynamic canal encroachment during thoracolumbar burst fractures. J. Spinal Disord. 8, 39–48.
47.
SmithJ.S., AndersonR., PhamT., BhatiaN., StewardO., and GuptaR. (2010). Role of early surgical decompression of the intradural space after cervical spinal cord injury in an animal model. J. Bone Jt. Surg. Am. 92, 1206–1214.
48.
ZhangJ., WangH., ZhangC., and LiW. (2016). Intrathecal decompression versus epidural decompression in the treatment of severe spinal cord injury in rat model: a randomized, controlled preclinical research. J. Orthop. Surg. Res. 11, 11–34.
49.
RollsA., ShechterR., and SchwartzM. (2009). The bright side of the glial scar in CNS repair. Nat. Rev. Neurosci. 10, 235–241.
50.
YiuG., and HeZ. (2006). Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617–627.
51.
IannottiC., ZhangY.P., ShieldsL.B.E., HanY., BurkeD.A., XuX.M., and ShieldsC.B. (2006). 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.
52.
JalanD., SainiN., ZaidiM., PallottieA., ElkabesS., and HearyR.F. (2017). Effects of early surgical decompression on functional and histological outcomes after severe experimental thoracic spinal cord injury. J. Neurosurg. Spine, 26, 62–75.
53.
CamlarM., Turk, Ç., BuhurA., OltuluF., OrenM., SenogluM., and OzerF. (2019). Does decompressive duraplasty have a neuroprotective effect on spinal trauma?: an experimental study. World Neurosurg. 126, e288–e294.
54.
AarabiB., OlexaJ., ChryssikosT., GalvagnoS.M., HershD.S., WessellA., SansurC., SchwartzbauerG., CrandallK., ShanmuganathanK., SimardJ.M., MushlinH., KoleM., LeE., PrattN., CannarsaG., LomanginoC.D., ScarboroM., ArescoC., and CurryB. (2019). Extent of spinal cord decompression in motor complete (American Spinal Injury Association Impairment Scale grades A and B) traumatic spinal cord injury patients: post-operative magnetic resonance imaging analysis of standard operative approaches. J. Neurotrauma, 36, 862–876.
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