The effects of intrathecal hypotension on tissue perfusion and pathophysiological outcome after acute spinal cord injury

Laboratory investigation

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Object

Venous stasis and intrathecal hypertension are believed to play a significant role in the hypoperfusion present in the spinal cord following injury. Lowering the intrathecal pressure via cerebrospinal fluid (CSF) drainage has been effective in treating spinal cord ischemia during aorta surgery. The purpose of the present study was to determine whether CSF drainage increases spinal cord perfusion and improves outcome after spinal injury in an animal model.

Methods

Anesthetized adult rabbits were subjected to a severe contusion spinal cord injury (SCI). Cerebrospinal fluid was then drained via a catheter to lower the intrathecal pressure by 10 mm Hg. Tissue perfusion was assessed at the site of injury, and values obtained before and after CSF drainage were compared. Two other cohorts of animals were subjected to SCI: 1 group subsequently underwent CSF drainage and the other did not. Results of histological analysis, motor evoked potential and motor function testing were compared between the 2 cohorts at 4 weeks postinjury.

Results

Cerebrospinal fluid drainage led to no significant improvement in spinal cord tissue perfusion. Four weeks after injury, the animals that underwent CSF drainage demonstrated significantly smaller areas of tissue damage at the injury site. There were no differences in motor evoked potentials or motor score outcomes at 4 weeks postinjury.

Conclusions

Cerebrospinal fluid drainage effectively lowers intrathecal pressure and decreases the amount of tissue damage in an animal model of spinal cord injury. Further studies are needed to determine whether different draining regimens can improve motor or electrophysiological outcomes.

Abbreviations used in this paper: BPU = blood perfusion unit; CSF = cerebrospinal fluid; MEP = motor evoked potential; SCI = spinal cord injury.

Abstract

Object

Venous stasis and intrathecal hypertension are believed to play a significant role in the hypoperfusion present in the spinal cord following injury. Lowering the intrathecal pressure via cerebrospinal fluid (CSF) drainage has been effective in treating spinal cord ischemia during aorta surgery. The purpose of the present study was to determine whether CSF drainage increases spinal cord perfusion and improves outcome after spinal injury in an animal model.

Methods

Anesthetized adult rabbits were subjected to a severe contusion spinal cord injury (SCI). Cerebrospinal fluid was then drained via a catheter to lower the intrathecal pressure by 10 mm Hg. Tissue perfusion was assessed at the site of injury, and values obtained before and after CSF drainage were compared. Two other cohorts of animals were subjected to SCI: 1 group subsequently underwent CSF drainage and the other did not. Results of histological analysis, motor evoked potential and motor function testing were compared between the 2 cohorts at 4 weeks postinjury.

Results

Cerebrospinal fluid drainage led to no significant improvement in spinal cord tissue perfusion. Four weeks after injury, the animals that underwent CSF drainage demonstrated significantly smaller areas of tissue damage at the injury site. There were no differences in motor evoked potentials or motor score outcomes at 4 weeks postinjury.

Conclusions

Cerebrospinal fluid drainage effectively lowers intrathecal pressure and decreases the amount of tissue damage in an animal model of spinal cord injury. Further studies are needed to determine whether different draining regimens can improve motor or electrophysiological outcomes.

Acute SCI affects 10,000–14,000 persons per year in the United States.11 Because the average age at injury is 37 years, there are 150,000–300,000 people living with significant disabilities from SCI at any given time. Estimates of the lifetime costs to care for someone with an SCI range from $325,000 to $1.35 million, and the yearly cost to society reach $8 billion.13 With better long-term care technologies, these costs are expected to continue to rise.

At present, no therapies exist that have had a significant impact on recovery of neurological function in injured persons.2 One of the causes of cell injury and decreased functioning in the postinjury period is the secondary injury cascade, consisting of tissue ischemia, release of cytotoxic mediators, and cell death.12 To overcome the secondary injury cascade, much work has focused on limiting the amount of tissue ischemia and increasing tissue perfusion.

One way to increase tissue perfusion in the intrathecal compartment is to lower the venous outflow pressure. This can easily be accomplished by draining CSF intrathecally. Recent reports have demonstrated the efficacy of lumbar CSF drainage in decreasing the amount of spinal cord ischemia both in animal models of spinal cord ischemia and in patients undergoing thoracic aorta cross-clamping for aneurysm surgery.5,6,9 Based on these background studies, the objectives of the present study were first to determine the effects of CSF drainage on spinal cord tissue perfusion, and then test whether this treatment led to improvements in the electrophysiological, histological, and physiological outcomes in an animal model of acute SCI.

Methods

All methodologies concerning the use of animals for scientific study were approved by the Institutional Animal Care and Use Committee at Barrow Neurological Institute and St. Joseph's Hospital and Medical Center. The animals were kept in individual quarters in a room with a 12-hour light/dark cycle and free access to food and water. Full-time veterinary staff were available daily.

Cerebrospinal Fluid Drainage and Tissue Perfusion

Adult New Zealand white rabbits (Charles River) were anesthetized with intramuscular injections of ketamine (40 mg/kg) and xylazine (10 mg/kg). The rabbits then underwent intubation and were maintained under general anesthesia with 2–3% isofluorane and morphine (0.1–0.5 mg intravenous boluses). A femoral artery and vein were canalized for blood pressure recordings and administration of drugs, respectively.

A midline laminectomy was then performed from T-8 to T-10 to expose the dura mater at those levels. The spinal column was stabilized with surgical clamps to eliminate motion from the ventilator, and a motorized impactor (Benchmark) was placed over the dura at the T-9 level. Each animal received an identical impact of 4 m/second velocity with a 3-mm-diameter probe to a 1-mm depth to produce a complete SCI.4

Immediately after impaction, the spinal subarachnoid space was accessed via a 22-gauge catheter inserted at the lumbrosacral junction in animals undergoing CSF drainage. Control animals did not undergo needle insertion. After impaction, a laser Doppler tissue perfusion probe (LDF100C, Biopac) was centered over the site of impaction and the perfusion value was recorded.

The generic value scale of BPU (0–1000) is used by the device software to determine the blood perfusion based on capillary blood flow, and is detected by the light backscatter from the emitted laser beam. Baseline BPU was recorded for 1 hour after impaction and then the CSF drain was opened and CSF was drained for 10 minutes. During the drainage, the CSF pressure dropped 10 mm Hg and was recorded. The amount of CSF drained to obtain the desired 10 mm Hg drop ranged between 0.5 and 1 ml. The BPU values were continuously recorded during drainage using a pressure transducer (Fig. 1). After the 10-minute drainage period, the pressure was restored to the predrainage level and the baseline BPU was recorded. Drainage was repeated at 2 and 3 hours postinjury. During perfusion analysis, arterial blood pressure was continuously monitored to ensure that any perfusion changes were not caused by changes in blood pressure. After the perfusion recording sessions, the animals were killed with an intravenous injection of pentobarbital. An identical protocol was used in the animals not subjected to spinal cord impaction to assess the baseline affect of CSF drainage on spinal cord tissue perfusion.

Fig. 1.
Fig. 1.

Graph showing the changes in mean arterial blood pressure (MAP), CSF pressure, and perfusion during CSF drainage 1 hour after acute SCI in a rabbit.

Physiological and Histological Analysis With CSF Drainage

A second group of adult New Zealand white rabbits was used in the functional analyses. The animals were anesthetized and invasively monitored as described above. Motor evoked potentials were elicited by transcranial stimulation and recorded unilaterally from the contralateral gastrocnemius muscle.15,16 Briefly, a train of 3 stimulating currents (333 Hz, 10–100 mA, 0.3 msec duration) was applied to the scalp overlying the sensorimotor cortex, and bipolar recording electrodes inserted into the contralateral gastrocnemius muscle were used to record the evoked potentials. A grounding electrode was placed in the skin just rostral to the recording electrodes. The average response from 20 sets of stimulations was used to analyze the peak amplitude and latency from the first potential in each animal.

After the MEP recordings, the T8–10 levels were exposed under sterile conditions and the impaction was performed as described above. Spinal subarachnoid catheters were not placed in control animals, while in rabbits in the study group a catheter was placed under sterile conditions and 1 ml of CSF was withdrawn 1 hour after impaction. The surgical site was then sutured and the animals were allowed to recover on a heating pad in an intensive care setting. Just prior to surgery and for the first 24 hours afterwards, the animals were given cefazolin (5 mg/kg) to prevent infection. The animals had their bladders manually expressed every 12 hours until spontaneous urination was observed, which was typically within 3 days.

Starting on the day of surgery (preimpaction), each animal underwent a weekly motor examination using the Tarlov scale: 0, no movement; 1, some minor movement of the joints; 2, major movements of the joints but cannot stand; 3, impaired, but can stand and possibly walk; and 4, normal motor function.17 After 4 weeks, each animal was anesthetized with ketamine/xylazine and a final set of MEPs performed. The animals were then given a lethal dose of pentobarbital and the spinal cord was harvested where the impaction had been performed. At least 1 cm of unaffected spinal cord above and below the impaction site was included in the specimen and fixed in 4% paraformaldehyde for histological analysis.

Histological Analysis

In each animal, a block of spinal cord containing the injured site was embedded in paraffin and sectioned axially at 30-μm increments. Eight sections from each block, including 4 from the middle, 2 from the rostral, and 2 from the caudal extent of the impaction site, were retained and mounted on chrome-gelatin coated slides. Sections were stained with H & E. Low-power magnification (× 4) images of the spinal cord sections were taken with a digital camera (Spot RT-SE) attached to a microscope (Nikon Optiphot-2). Next, the surface area of the contusion and the total surface area in each section were measured using Image-J software (National Institutes of of Health). The measurements were performed in a blinded manner by a single observer, and the ratio of contused area to total area was calculated for each slice.

Data Analysis

For tissue perfusion recordings, the percentage change in BPU during CSF drainage was calculated from baseline. This change was then averaged at each time point (1, 2, and 3 hours) postinjury. The same calculations were determined for the animals that did not undergo impaction and the time points were delineated from the starting time of BPU recordings following the surgical exposure.

In the functional analyses, weekly Tarlov scores, ratios of histological injury area to total area, and MEP amplitudes were averaged for each group (CSF drainage and control rabbits). These averages were then compared with the unpaired Student t-test and the analysis of variance test using commercially available statistical software (SigmaStat, SPSS Inc.) with statistical significance set at p = 0.05.

Results

Tissue Perfusion and CSF Drainage

Four animals subjected to SCI and 4 animals who did not (control group) were used in perfusion analyses during CSF drainage. An example of the effect of CSF drainage on spinal cord perfusion following contusion injury is shown in Fig. 1. The changes in mean arterial blood pressure and CSF pressure during drainage at each time point in the 2 groups are shown in Table 1. In the animals that did not undergo SCI, tissue perfusion dropped 25% during 1 hour of CSF drainage. This drop in perfusion was not seen at the 2- and 3-hour time points when small increases of 10 and 4% were seen, respectively. Likewise in the animals subjected to SCI a drop in perfusion of 47% was observed after 1 hour. This drop was diminished, but still present, at the 2- and 3-hour time points to 17 and 12%, respectively. None of these perfusion changes were significantly different at any point between the control and injured animals (Fig. 2).

TABLE 1

Summary of intrathecal hypotension effects on various physiological measures*

Parameter1 Hr Postinjury/Sham2 Hrs Postinjury/Sham3 Hrs Postinjury/Sham
SCI group
 change in MABP (mm Hg)1.1 ± 1.1−2.6 ± 0.7−0.6 ± 1.4
 change in CSF pressure (mm Hg)9.4 ± 1.210.0 ± 2.19.8 ± 2.0
 CSF vol drained (ml)0.7 ± 0.10.7 ± 0.10.6 ± 0.1
 change in perfusion (%)−47.4 ± 11.1−16.8 ± 13.9−11.7 ± 18.9
control group (no SCI)
 change in MABP (%)−3.6 ± 4.50.9 ± 1.32.1 ± 1.4
 change in CSF pressure (mm Hg)8.2 ± 0.49.3 ± 0.79.2 ± 0.7
 CSF vol drained (ml)0.8 ± 0.10.9 ± 0.21.0 ± 0.2
 change in perfusion (%)−25.5 ± 10.09.7 ± 26.14.3 ± 22.2

* All values are given as means ± standard error of the means. MABP = mean arterial blood pressure; vol = volume.

Fig. 2.
Fig. 2.

Graph of average change in perfusion over time during CSF drainage in uninjured control animals and animals that underwent SCI at 1, 2, and 3 hours after injury.

Cerebrospinal Fluid Drainage and Functional Analyses

Twelve animals were subjected to SCI. Six of these 12 underwent CSF drainage and 6 did not. Three animals died during the postoperative period of sepsis-related complications, leaving 5 animals in the control group and 4 animals in the CSF drainage group. The preinjury MEP amplitudes averaged 12.2 μV in the control group and 7.6 μV in the CSF drainage group. This difference was not significantly different. Four weeks after the injury, there was no significant recovery of MEP amplitudes in either group (Table 2). No animals recovered the ability to ambulate after impaction (Tarlov score = 3). There was no significant difference in the Tarlov scores between the groups at any time point for the full 4 weeks (Fig. 3).

TABLE 2

Motor evoked potential amplitude comparisons between control and CSF drainage animals*

GroupPreimpaction (μV)Immediately Postimpaction (μV)4 Wks Postimpaction (μV)
control12.2 ± 3.900.2 ± 0.1
CSFLD7.6 ± 0.700

* Values are given as means ± standard error of the means. CSFLD = CSF lumbar drainage.

Fig. 3.
Fig. 3.

Graph showing average weekly Tarlov scores for control and CSF drainage animals (CSFLD) during the 4-week period following SCI. CSFLD = CSF drainage.

Examples of axial spinal cord histological slices through the impaction site for both groups of animals are shown in Fig. 4. When compiled, the average ratio of injured tissue to total cross-sectional area at the level of injury was significantly lower in the CSF drainage group (56%) compared with the control group (44%; Fig. 5).

Fig. 4.
Fig. 4.

Photomicrographs of cross-sections of spinal cord at the level of injury in a control rabbit that underwent SCI but not drainage (A), and an animal that underwent CSF drainage and SCI (B). Notice the decrease in injury area for the animal that underwent CSF drainage. H & E, original magnification × 4.

Fig. 5.
Fig. 5.

Graph of the average ratio of injured/total cross-sectional area of the injury level of the spinal cord in control animals that underwent SCI but no drainage and in animals that underwent SCI and CSF drainage. Data are means and standard error of the means. *p < 0.05.

Discussion

We have demonstrated that drainage of CSF after acute SCI in an animal model reduces the area of tissue damage at the injury site. We found no improvement in the electrophysiological or motor outcomes in animals that underwent CSF drainage. Based on these data, we conclude that decreasing intrathecal pressure after an injury severe enough to cause a complete neurological deficit does not lead to significant functional improvement in this model.

Our most interesting finding was the fact that the spinal cord perfusion decreased during periods of intrathecal hypotension. This was a paradoxical result given the fact that decreasing venous outflow pressure leads to an increase in tissue perfusion. Earlier studies analyzing spinal cord blood flow during CSF drainage have shown mixed results. Authors of studies using radiolabeled tracers to analyze blood flow in a dog model demonstrated increases in spinal cord blood flow during CSF drainage.3,7 The authors of a separate study in a dog model demonstrated no change in blood flow in the spinal cord after CSF drainage.14 These authors used direct measurements of tissue perfusion in the spinal cord using the hydrogen clearance method with a platinum electrode, as described previously.10 Our data correlate with the latter finding because there was essentially no change in perfusion in either the SCI or control animals at 2 hours after the injury. Although we saw no change in perfusion, the data are limited by the amount of tissue analyzed by the probe. It is possible that the perfusion was enhanced in other areas of the spinal cord near the injury which led to the histological improvement. Because the perfusion probe was on the surface of the spinal cord, an increase in perfusion in the deeper parenchyma may be responsible for the histological findings. As a more invasive probe would have prevented us from controlling CSF drainage, it was not possible to test the perfusion in the deeper tissue, and further studies are needed of the perfusion changes surrounding the injury site.

Spinal cord injury occurs in 2 phases. The first phase is the primary physical damage due to the impact energy of the compressive nature of the injury. The damage can be very complex with shearing of the axons, destruction of the cell bodies, and disruption of the microvasculature at the site of injury. The extent of the damage is determined by the initial force of impact, the duration of the compression, and the amount of preexisting tension or compression on the spinal cord from spondylosis or stenosis.18

The secondary phase of the injury begins soon after the primary injury has occurred and can be influenced by many factors such as hypoxia, hypotension, and the extent of the primary injury. The initial insult causes a disruption of the microvasculature which leads to tissue hypoperfusion.8 This can be severely accentuated by systemic variables such as pulmonary and cardiovascular dysfunction due to the inability of the spinal cord tissue to autoregulate perfusion after a traumatic injury.19 Overall this leads to profound tissue ischemia that persists for hours to days after the insult. The ischemia, in addition to the initial injury, initiates a cascade of cellular destruction due to cell membrane breakdown and the release of multiple factors such as calcium and glutamate.1 These factors further potentiate the breakdown of cellular membranes through the activation of proteases and phospholipases in a positive feedback manner.

The role that ischemia plays in the secondary injury cascade has been well studied in animal models.8 To date, the most effective way to limit the amount of spinal cord ischemia following injury is by limiting systemic hypoxia and hypotension. Several pharmacological agents have been tested that have shown mixed results in limiting spinal cord hypoperfusion such as glucocorticoids and glutamate receptor antagonists.1 However, the primary issue with cord ischemia is the disruption of the vasculature itself, which creates a physical barrier to tissue perfusion. This barrier limits the ability to deliver pharmacological agents to the site of injury, which is a possible reason why so many of these agents are unsuccessful in treating SCI.

Several models of spinal cord ischemia have been developed to determine ways to limit the chance of cord infarction following aortic occlusion during aortic aneurysm surgery. One of the most encouraging treatments shown to decrease neurological dysfunction in these models is CSF drainage.9 This treatment has also been recently shown to decrease the incidence of paraplegia in patients after thoracic aneurysm repair in a randomized, prospective study.6 Although drainage of CSF has been successful in treating isolated incidents of spinal cord ischemia, the current study is the first to analyze its effect on the secondary ischemia that develops after traumatic SCI.

Conclusions

Draining CSF after acute SCI causes a significant drop in intrathecal pressure. This drop in intrathecal pressure paradoxically led to an early decrease in tissue perfusion that was less pronounced at longer postinjury intervals. Although intrathecal hypotension led to this early decrease in tissue perfusion, it did lead to a significant reduction in the size of the tissue injury following acute SCI. However, the improved histological outcome did not translate into improvements in either the motor or electrophysiological outcome, and more studies are warranted in less severely injured animals to determine the role that intrathecal hypotension plays in the treatment of acute SCI.

Disclaimer

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

References

  • 1

    Amar APLevy ML: Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery 44:102710401999

  • 2

    Baptiste DCFehlings MG: Update on the treatment of spinal cord injury. Prog Brain Res 161:2172332007

  • 3

    Bower TCMurray MJGloviczki PYaksh TLHollier LHPairolero PC: Effects of thoracic aortic occlusion and cerebrospinal fluid drainage on regional spinal cord blood flow in dogs: correlation with neurologic outcome. J Vasc Surg 9:1351441989

  • 4

    Brody DLMacDonald CKessens CCYuede CParsadanian MSpinner M: Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injury. J Neurotrauma 24:6576732007

  • 5

    Cina CSAbouzahr LArena GOLagana ADevereaux PJFarrokhyar F: Cerebrospinal fluid drainage to prevent paraplegia during thoracic and thoracoabdominal aortic aneurysm surgery: a systematic review and meta-analysis. J Vasc Surg 40:36442004

  • 6

    Coselli JSLemaire SAKoksoy CSchmittling ZCCurling PE: Cerebrospinal fluid drainage reduces paraplegia after thoracoabdominal aortic aneurysm repair: results of a randomized clinical trial. J Vasc Surg 35:6316392002

  • 7

    Elmore JRGloviczki PHarper CM JrMurray MJWu QHBower TC: Spinal cord injury in experimental thoracic aortic occlusion: investigation of combined methods of protection. J Vasc Surg 15:7897991992

  • 8

    Fehlings MGTator CHLinden RD: The relationships among the severity of spinal cord injury, motor and somatosensory evoked potentials and spinal cord blood flow. Electroencephalogr Clin Neurophysiol 74:2412591989

  • 9

    Francel PCLong BAMalik JMTribble CJane JAKron IL: Limiting ischemic spinal cord injury using a free radical scavenger 21-aminosteroid and/or cerebrospinal fluid drainage. J Neurosurg 79:7427511993

  • 10

    Griffiths IRRowan JOCrawford RA: Spinal cord blood flow measured by a hydrogen clearance technique. J Neurol Sci 26:5295441975

  • 11

    Horn EMForage JSonntag VKHAcute treatment of patients with spinal cord injury. Herkowitz HNGarfin SNEismont FJBell GRBalderston RA: Rothman-Simeone: The Spine ed 5New YorkSaunders2006

  • 12

    Horn EMPruel MCSonntag VKHBambakidis NC: Multimodality treatment of spinal cord injury: endogenous stem cells and other magic bullets. Barrow Quarterly 23:9142007

  • 13

    Jackson ABDijkers MDevivo MJPoczatek RB: A demographic profile of new traumatic spinal cord injuries: change and stability over 30 years. Arch Phys Med Rehabil 85:174017482004

  • 14

    Kazama SMasaki YMaruyama SIshihara A: Effect of altering cerebrospinal fluid pressure on spinal cord blood flow. Ann Thorac Surg 58:1121151994

  • 15

    Nashmi RImamura HTator CHFehlings MG: Serial recording of somatosensory and myoelectric motor evoked potentials: role in assessing functional recovery after graded spinal cord injury in the rat. J Neurotrauma 14:1511591997

  • 16

    Oro JJGibbs SRHaghighi SS: Balloon device for experimental graded spinal cord compression in the rat. J Spinal Disord 12:2572611999

  • 17

    Tarlov IMKlinger H: Spinal cord compression studies. II. Time limits for recovery after acute compression in dogs. Arch Neurol Psychiatry 71:2712901954

  • 18

    Tator CH: Spine-spinal cord relationships in spinal cord trauma. Clin Neurosurg 30:4794941983

  • 19

    Tator CHFehlings MG: Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15261991

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Article Information

Address correspondence to: Eric M. Horn, M.D., Ph.D., Department of Neurological Surgery, Indiana University College of Medicine, 545 Barnhill Drive 139 Emerson Hall, Indianapolis, Indiana 46202-5124. email: emhorn@iupui.edu

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Graph showing the changes in mean arterial blood pressure (MAP), CSF pressure, and perfusion during CSF drainage 1 hour after acute SCI in a rabbit.

  • View in gallery

    Graph of average change in perfusion over time during CSF drainage in uninjured control animals and animals that underwent SCI at 1, 2, and 3 hours after injury.

  • View in gallery

    Graph showing average weekly Tarlov scores for control and CSF drainage animals (CSFLD) during the 4-week period following SCI. CSFLD = CSF drainage.

  • View in gallery

    Photomicrographs of cross-sections of spinal cord at the level of injury in a control rabbit that underwent SCI but not drainage (A), and an animal that underwent CSF drainage and SCI (B). Notice the decrease in injury area for the animal that underwent CSF drainage. H & E, original magnification × 4.

  • View in gallery

    Graph of the average ratio of injured/total cross-sectional area of the injury level of the spinal cord in control animals that underwent SCI but no drainage and in animals that underwent SCI and CSF drainage. Data are means and standard error of the means. *p < 0.05.

References

1

Amar APLevy ML: Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery 44:102710401999

2

Baptiste DCFehlings MG: Update on the treatment of spinal cord injury. Prog Brain Res 161:2172332007

3

Bower TCMurray MJGloviczki PYaksh TLHollier LHPairolero PC: Effects of thoracic aortic occlusion and cerebrospinal fluid drainage on regional spinal cord blood flow in dogs: correlation with neurologic outcome. J Vasc Surg 9:1351441989

4

Brody DLMacDonald CKessens CCYuede CParsadanian MSpinner M: Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injury. J Neurotrauma 24:6576732007

5

Cina CSAbouzahr LArena GOLagana ADevereaux PJFarrokhyar F: Cerebrospinal fluid drainage to prevent paraplegia during thoracic and thoracoabdominal aortic aneurysm surgery: a systematic review and meta-analysis. J Vasc Surg 40:36442004

6

Coselli JSLemaire SAKoksoy CSchmittling ZCCurling PE: Cerebrospinal fluid drainage reduces paraplegia after thoracoabdominal aortic aneurysm repair: results of a randomized clinical trial. J Vasc Surg 35:6316392002

7

Elmore JRGloviczki PHarper CM JrMurray MJWu QHBower TC: Spinal cord injury in experimental thoracic aortic occlusion: investigation of combined methods of protection. J Vasc Surg 15:7897991992

8

Fehlings MGTator CHLinden RD: The relationships among the severity of spinal cord injury, motor and somatosensory evoked potentials and spinal cord blood flow. Electroencephalogr Clin Neurophysiol 74:2412591989

9

Francel PCLong BAMalik JMTribble CJane JAKron IL: Limiting ischemic spinal cord injury using a free radical scavenger 21-aminosteroid and/or cerebrospinal fluid drainage. J Neurosurg 79:7427511993

10

Griffiths IRRowan JOCrawford RA: Spinal cord blood flow measured by a hydrogen clearance technique. J Neurol Sci 26:5295441975

11

Horn EMForage JSonntag VKHAcute treatment of patients with spinal cord injury. Herkowitz HNGarfin SNEismont FJBell GRBalderston RA: Rothman-Simeone: The Spine ed 5New YorkSaunders2006

12

Horn EMPruel MCSonntag VKHBambakidis NC: Multimodality treatment of spinal cord injury: endogenous stem cells and other magic bullets. Barrow Quarterly 23:9142007

13

Jackson ABDijkers MDevivo MJPoczatek RB: A demographic profile of new traumatic spinal cord injuries: change and stability over 30 years. Arch Phys Med Rehabil 85:174017482004

14

Kazama SMasaki YMaruyama SIshihara A: Effect of altering cerebrospinal fluid pressure on spinal cord blood flow. Ann Thorac Surg 58:1121151994

15

Nashmi RImamura HTator CHFehlings MG: Serial recording of somatosensory and myoelectric motor evoked potentials: role in assessing functional recovery after graded spinal cord injury in the rat. J Neurotrauma 14:1511591997

16

Oro JJGibbs SRHaghighi SS: Balloon device for experimental graded spinal cord compression in the rat. J Spinal Disord 12:2572611999

17

Tarlov IMKlinger H: Spinal cord compression studies. II. Time limits for recovery after acute compression in dogs. Arch Neurol Psychiatry 71:2712901954

18

Tator CH: Spine-spinal cord relationships in spinal cord trauma. Clin Neurosurg 30:4794941983

19

Tator CHFehlings MG: Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15261991

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