The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 93, Issue 19

Scientific Articles | October 05, 2011

The Effects of Spinal Cord Injury Induced by Shortening on Motor Evoked Potentials and Spinal Cord Blood Flow: An Experimental Study in Swine

Hitesh N. Modi, MS, PhD¹; Seung-Woo Suh, MD, PhD²; Jae-Young Hong, MD²; Jae-Hyuk Yang, MD²

¹ 602 Sath Sangath Apartment, Satellite, Ahmedabad, Guj 380015, India. E-mail address: hnm7678@yahoo.co.in
² Scoliosis Research Institute, Department of Orthopedics, Korea University Guro Hospital, 80 Guro-Dong, Guro-Gu, Seoul, South Korea. E-mail address for S.-W. Suh: spine@korea.ac.kr.

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Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

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Investigation performed at the Scoliosis Research Institute, Department of Orthopedics, Korea University Guro Hospital, Seoul, South Korea

J Bone Joint Surg Am, 2011 Oct 05;93(19):1781-1789. doi: 10.2106/JBJS.I.01794

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Abstract

Background:

Spinal cord injury due to spinal shortening is disastrous, but the amount that the spine can be shortened without injury is unknown. We assessed spinal cord injury and changes in spinal cord blood flow after spinal shortening in swine.

Methods:

Ten pigs underwent pedicle screw instrumentation between T10 and T13 followed by a T11 and T12 vertebrectomy resulting in spinal shortening. Spinal cord function and spinal cord blood flow were monitored simultaneously with use of transcranial motor evoked potentials and laser Doppler flowmetry, respectively. A staged shortening procedure was performed: phase 1 resulted in no morphological change in the spinal cord, phase 2 resulted in buckling of the spinal cord, and phase 3 resulted in kinking of the spinal cord. After loss of motor evoked potential signals, which was considered to indicate spinal cord injury, the spinal instrumentation was tightened. The motor evoked potentials and spinal cord blood flow were monitored for an additional thirty minutes, and a wake-up test was then performed. Finally, a spinal cord specimen was obtained and evaluated histologically.

Results:

The motor evoked potential data demonstrated no evidence of spinal cord injury during phases 1 and 2. However, the signals were lost during phase 3, indicating spinal cord injury. The mean shortening was 35 ± 2.7 mm, which was similar to the mean vertebral body height at the thoracolumbar level (33.6 ± 1.9 mm), indicating that spinal cord injury resulted from shortening equivalent to the height of one vertebra. Spinal shortening did not cause injury if the amount of shortening was less than the mean segmental height of the entire spinal column (27.7 ± 1.6 mm for T1-L6). The spinal cord blood flow increased slightly (by 11.6% ± 20.6%) during phase 2, but decreased by 43.1% ± 11.4% during phase 3. The wake-up test performed after thirty minutes revealed no movement in the lower limbs.

Conclusions:

Spinal shortening of ≥104.2% of one vertebral body height at the thoracolumbar level caused spinal cord injury, but shortening of ≤73.8% did not result in injury.

Clinical Relevance:

This study provides guidelines for the mean amount of spinal shortening that will result in spinal cord injury in swine.

Figures in this Article

Introduction

Correction of rigid, severe scoliosis is difficult due to the severe rotation of the vertebrae and the altered anatomy of the spinal column^1,2. Spinal column shortening is one of the most popular techniques for correcting severe, rigid scoliosis^3,4, but patients undergoing corrective surgery for significant kyphoscoliosis are at risk of developing intraoperative neurological deficits^5,6 and postoperative neurological complications^7-10. Although spinal cord injury is disastrous, the amount that the spine can be shortened without injury is unknown. Intraoperative techniques used to detect, and ideally to prevent, spinal cord injury include somatosensory evoked potentials and transcranial motor evoked potentials¹¹. Loss of an evoked potential signal may indicate either structural injury to the spinal cord or spinal cord ischemia due to compromised blood flow¹². Motor evoked potentials can identify spinal cord injury at an early stage, and catastrophic complications can be minimized if the shortening procedure is reversed promptly¹¹.

Experimental models and clinical observations of spinal cord injury support the concepts of primary and secondary injury¹³. The most widely used experimental spinal cord injury model is the weight-drop method introduced by Allen¹⁴ and later modified by other researchers^15-17. Other traumatic spinal cord injury models include the use of extradural balloons¹⁸, the use of aneurysm clips¹⁹, and photochemical induction of spinal cord injury²⁰. Models of traumatic spinal cord injury in rodents^21,22 produce very limited information regarding the biological processes involved in human spinal cord injury because of the neurobiological differences between rodents and humans. Therefore, many researchers have attempted to develop models using various animals to study acute spinal cord injury²³. The majority of the research has involved direct impact of a specific weight on the spinal cord after laminectomy, translation of the vertebral bodies, or direct transection of the cord in order to create the spinal cord injury. The effects of spinal cord injury and the therapeutic effects of various medications intended to aid recovery after spinal cord injury have been studied^24-26. Such studies are helpful in determining the therapeutic effects of drug treatment in cases of acute traumatic spinal cord injury, in highlighting the relationship between the severity of neurological injury and the duration of compression, and in demonstrating that it is possible to produce consistent injuries in rats, mice, or similar small animals. In our pilot study, a spinal cord injury model was developed in swine treated with a spinal shortening procedure. The aims of our study were to assess spinal cord injury with use of motor evoked potentials and changes in spinal cord blood flow with use of laser Doppler flowmetry, and to determine the relationship between spinal cord injury and the amount of shortening of the spinal column.

Materials and Methods

Animal Selection

An experimental study involving thirteen farm pigs was approved by our university's animal care and use committee. The mean age (and standard deviation) of the study animals was 3.3 ± 0.3 months (range, three to four months), and the mean weight was 51.9 ± 1.0 kg (range, 50 to 53 kg). The first two experimental animals were used to identify the requirements of the procedure and the difficulties encountered during it. One of the remaining pigs showed changes in the amplitude of the motor evoked potentials before the final shortening. Thus, after exclusion of these three animals, the study cohort in our pilot study included ten animals.

Preoperative Preparation and Anesthesia

All experiments were performed at the Biomedical Animal Research Center at Konkuk University under care of a veterinary team. Study animals underwent fasting for twenty-four hours prior to anesthesia. Ketamine (10-20 mg/kg) was administered intramuscularly, then a venous line was inserted and the animal was intubated with an endotracheal tube²⁷. Anesthesia was induced with short-acting intravenous thiopentol (10-15 mg/kg)²⁸ and maintained with intravenous propofol (20-25 mg/kg)^27,29.

Positioning and Preparation for Neuromonitoring

After induction of anesthesia, the pig was placed prone on a radiolucent table. The upper end plates of the first thoracic and the first sacral vertebra were identified and marked with the use of a C-arm, and the approximate length of the spinal column (T1 to L6) was measured. The desired level of the surgery at T11-12 was also marked. The transcranial motor evoked potential system (NIM Spine; Sofamor Danek [Medtronic], Memphis, Tennessee) used for the neuromonitoring was then applied. A technician operated the motor evoked potential system and assisted in reading and analyzing the neuromonitoring data throughout the experiment. Baseline motor evoked potential amplitudes and continuous electromyographic signals were measured before the experiment.

Monitoring of Spinal Cord Blood Flow

Spinal cord blood flow monitoring with use of laser Doppler flowmetry was initiated before beginning the osteotomy in order to provide baseline values and was continued during and after the spinal shortening procedure in order to observe any changes.

Surgical Procedure

After skin preparation, a 15 to 18-cm incision was made along the midline of the dorsum from T9 to L1. The spine was exposed subperiosteally from T10 to T13. Once dissection was complete, the motor evoked potentials were recorded. The positions of the T10 and T13 pedicles were again confirmed with use of the C-arm, and entry into each pedicle was achieved with use of an awl. The passage within the pedicle was extended to a depth of 30 mm with use of a pedicle probe. A 5 × 30-mm pedicle screw was inserted into each T10 and T13 pedicle, with continuous electromyographic monitoring, and the motor evoked potential signals were checked immediately after inserting the pedicle screws. The T10 and T13 levels were then stabilized bilaterally with use of a pair of 90-mm rods in order to prevent translation^21,30,31. A total laminectomy was performed from T10 through T13. The facet joints were also removed in order to facilitate movement and create space for the osteotomy. The spinal cord was protected with a dural protector, and a bilateral osteotomy of the vertebral body was performed just caudal to the pedicle of T11 and just cephalad to the pedicle of T13 with use of a 10-mm osteotome. The osteotomy was completed on one side after fixing the segments with the rod on the contralateral side, and vice versa. The distance between T10 and T13 was measured in order to assess the total height of the T11 and T12 vertebrae. Once the osteotomy was complete, a two-level vertebral column resection was performed, and the motor evoked potentials were compared with the baseline amplitude. Motor evoked potential monitoring continued as gradual compression was applied bilaterally to the rods in order to initiate spinal shortening. Spinal shortening was achieved gradually in three phases, as described by Kawahara et al.³² (Fig. 1). In phase 1, the spinal cord appeared morphologically normal; in phase 2, the spinal cord began to buckle; and in phase 3, the spinal cord kinked (Fig. 2). The motor evoked potentials were checked and compared with the baseline value during each phase. Spinal cord injury was identified when the motor evoked potential disappeared in all leads. In addition, spinal cord blood flow was monitored with use of laser Doppler flowmetry during each phase. The rod-screw construct was tightened once the motor evoked potential signals were lost. The amount of compression was measured with use of vernier calipers throughout each phase of the procedure. The amount of shortening was calculated by subtracting the final distance between T10 and T13 from the baseline distance (corresponding to the T11 and T12 vertebral levels). At the time of final shortening, when the motor evoked potential signals were lost (Fig. 2), the motor evoked potentials and spinal cord blood flow were checked every five minutes for the next thirty minutes in order to observe any further changes. At the end of the thirty minutes, motor function was checked in both hindlimbs with use of the Stagnara wake-up test³³. The pig was then anesthetized again, and compression was released in order to observe whether there was any recovery of the motor evoked potentials. The pig was killed at the conclusion of the experiment, and a spinal cord sample was obtained for histopathological examination, which was performed with hematoxylin and eosin staining.

Fig. 1

Illustrations depicting the spinal shortening procedure at baseline immediately before the shortening procedure (a); during phase 1, in which the spinal cord appears morphologically normal (b); during phase 2, in which the spinal cord begins to buckle (c); and during phase 3, in which the spinal cord begins to kink (d). Loss of the motor evoked potentials, indicating spinal cord injury, occurred during phase 3, as the spinal cord kinked. (The shaded area denotes the area of vertebral resection prior to the shortening.)

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Fig. 2

Photograph showing spinal cord kinking during phase 3 of the spinal shortening procedure.

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Data Analysis

The mean shortening that resulted in spinal cord injury (indicated by a drop in the motor evoked potential to <50% of the baseline value in both limbs) was calculated, and this value was compared with the mean vertebral height of the excised single vertebral segment. The mean spinal shortening that resulted in spinal cord injury was also compared with the mean segmental height of the entire spinal column. In addition, the spinal cord blood flow after the spinal cord injury was also compared with the baseline value. Comparisons were performed with use of paired t tests, and a p value of <0.05 was considered significant.

Source of Funding

There was no external funding for this study.

Results

Mean Morphological and Intraoperative Data

The mean body weight, spinal column length, thoracolumbar vertebral body height, and estimated intraoperative blood loss during the procedure were 51.9 ± 1.0 kg (range, 50 to 53 kg; 95% confidence interval [CI], ± 2 kg), 526.0 ± 24.6 mm (range, 490 to 570 mm; 95% CI, ± 49 mm), 27.7 ± 1.3 mm (range, 25.8 to 30.0 mm; 95% CI, ± 3 mm), and 1240 ± 279.7 mL (range, 800 to 1600 mL; 95% CI, ± 555 mL), respectively. The mean segmental height of the entire spinal column (27.7 ± 1.3 mm) was less than the mean thoracolumbar (T11-12) vertebral body height (33.6 ± 1.9 mm, p < 0.0001) because of the smaller size of the thoracic vertebrae (Table I and Appendix).

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TABLE I Shortening and Motor Evoked Potential Signals at Each Stage of the Spinal Column Shortening

	Preop. Height of T11 + T12 (mm)	Mean Thoracolumbar Vertebral Height (mm)	Phase 1, Normal Morphology		Phase 2, Start of Buckling		Phase 3, Spinal Cord Injury on Kinking		Compression Causing Spinal Cord Injury (mm)	Movement During Wake-Up After 30 Min
Pig No.	T10-13 Gap*	MEP†	T10-13 Gap*	MEP†	T10-13 Gap*	MEP†
1	66	33	50 (48.5)	M	40 (78.8)	M	32 (103.0)	L	34	N
2	60	30	48 (40.0)	M	35 (83.3)	D	28 (106.7)	L	32	N
3	66	33	52 (42.4)	M	42 (72.7)	M	30 (109.1)	L	36	N
4	70	35	54 (45.7)	M	44 (74.3)	M	34 (102.9)	L	36	N
5	65	32.5	50 (46.2)	M	40 (76.9)	M	30 (107.7)	L	35	N
6	65	32.5	50 (46.2)	M	31 (104.6)	D	26 (120.0)	L	39	N
7	72	36	55 (47.2)	M	40 (88.9)	M	34 (105.6)	L	38	N
8	66	33	60 (18.2)	M	52 (42.4)	M	36 (90.9)	L	30	N
9	72	36	60 (33.3)	M	50 (61.1)	M	36 (100.0)	L	36	N
10	70	35	65 (14.3)	M	50 (57.1)	M	36 (97.1)	L	34	N
Mean	67.2	33.6	54.4 (38.1)		42.4 (73.8)		32.2 (104.2)		35.0
Std. Dev.	3.8	1.9	5.6		6.8		3.6		2.7

*Values are given as the remaining distance in mm, with the corresponding shortening expressed as a percentage of the mean thoracolumbar vertebral height in parentheses.
†MEP = motor evoked potentials, M = maintained, D = decreased, and L = lost.

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TABLE I Shortening and Motor Evoked Potential Signals at Each Stage of the Spinal Column Shortening

	Preop. Height of T11 + T12 (mm)	Mean Thoracolumbar Vertebral Height (mm)	Phase 1, Normal Morphology		Phase 2, Start of Buckling		Phase 3, Spinal Cord Injury on Kinking		Compression Causing Spinal Cord Injury (mm)	Movement During Wake-Up After 30 Min
Pig No.	T10-13 Gap*	MEP†	T10-13 Gap*	MEP†	T10-13 Gap*	MEP†
1	66	33	50 (48.5)	M	40 (78.8)	M	32 (103.0)	L	34	N
2	60	30	48 (40.0)	M	35 (83.3)	D	28 (106.7)	L	32	N
3	66	33	52 (42.4)	M	42 (72.7)	M	30 (109.1)	L	36	N
4	70	35	54 (45.7)	M	44 (74.3)	M	34 (102.9)	L	36	N
5	65	32.5	50 (46.2)	M	40 (76.9)	M	30 (107.7)	L	35	N
6	65	32.5	50 (46.2)	M	31 (104.6)	D	26 (120.0)	L	39	N
7	72	36	55 (47.2)	M	40 (88.9)	M	34 (105.6)	L	38	N
8	66	33	60 (18.2)	M	52 (42.4)	M	36 (90.9)	L	30	N
9	72	36	60 (33.3)	M	50 (61.1)	M	36 (100.0)	L	36	N
10	70	35	65 (14.3)	M	50 (57.1)	M	36 (97.1)	L	34	N
Mean	67.2	33.6	54.4 (38.1)		42.4 (73.8)		32.2 (104.2)		35.0
Std. Dev.	3.8	1.9	5.6		6.8		3.6		2.7

Spinal Cord Functional Assessment with Use of Motor Evoked Potentials

The heights of the T11 and T12 vertebral bodies and the motor evoked potentials at baseline (immediately after vertebrectomy, before compression) and during phases 1, 2, and 3 of the spinal shortening are shown in Table I. The mean heights of the T11 and T12 vertebrae (and standard deviation) totaled 67.2 ± 3.8 mm, corresponding to a mean vertebral body height of 33.6 ± 1.9 mm (range, 30 to 36 mm; 95% CI, ± 4 mm). The motor evoked potentials remained at approximately the baseline level in all of the pigs during phase 1 of the spinal shortening, which resulted in a mean T10-13 distance of 54.4 ± 5.6 mm (95% CI, ± 11 mm). The motor evoked potentials also remained at approximately the baseline level in eight of the ten pigs during phase 2, which resulted in a mean T10-13 distance of 42.4 ± 6.8 mm (95% CI, ± 13 mm). The motor evoked potential signals in the remaining two pigs decreased to <50% of baseline in one of the leads (Table I). However, these cases were considered to represent decreased functionality and not spinal cord injury, as the motor evoked potential signals on the contralateral side remained at >50% of the baseline value. The motor evoked potential signals in all leads were lost in all experimental animals during phase 3 of the spinal shortening, indicating spinal cord injury. The final mean distance between T10 and T13 was 32.2 ± 3.6 mm (95% CI, ± 7 mm), corresponding to a mean shortening of 35.0 ± 2.7 mm (range, 30 to 39 mm; 95% CI, ± 5 mm). Thus, shortening of 104.2% ± 7.8% (95% CI, ± 11.6%) of the mean vertebral height at T11-12 caused spinal cord injury during phase 3, but shortening of 73.8% ± 17.4% (95% CI, ± 11.8%) did not cause spinal cord injury during phase 2 (Table I). The mean amount of spinal shortening that resulted in spinal cord injury was similar to the mean vertebral body height at the T11-12 thoracolumbar levels (p = 0.115), suggesting that spinal cord injury can result from spinal shortening of approximately one vertebral level. However, the amount of spinal shortening required to produce spinal cord injury was significantly greater than the mean segmental height of the entire spinal column (i.e., T1-L6) (p < 0.0001). These findings suggest that spinal shortening does not produce spinal cord injury unless the amount of shortening exceeds the mean segmental height of the spinal column as a whole.

Spinal Cord Blood Flow

The mean spinal cord blood flow during phases 1, 2, and 3 was 24.1 ± 9.0 (95% CI, ± 18), 26.9 ± 11.8 (95% CI, ± 23), and 14.1 ± 6.7 (95% CI, ± 13) mL/100 g/min, respectively (Table II). The spinal cord blood flow increased slightly from baseline to phase 2, by 11.6% ± 20.6% (range, −25% to 33.3%; 95% CI, ± 36%), but the difference from the baseline value was not significant (p = 0.098). The spinal cord blood flow decreased by 43.1% ± 11.4% (range, 30% to 65%; 95% CI, ± 23%) from baseline to phase 3 (p < 0.0001). This showed that spinal shortening can compromise spinal cord blood flow.

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TABLE II Spinal Cord Blood Flow at Each Phase of the Spinal Column Shortening*

	Spinal Cord Blood Flow (mL/100 g/min)			Decrease in Spinal Cord Blood Flow Between Baseline and Spinal Cord Injury (%)
Pig No.	Phases 0 and 1 (Baseline)	Phase 2	Phase 3
1	12	15	5	58.3
2	45	55	28	37.8
3	22	30	15	31.8
4	22	24	12	45.5
5	20	15	7	65.0
6	30	30	16	46.7
7	20	24	13	35.0
8	22	18	14	36.4
9	30	34	21	30.0
10	18	24	10	44.4
Mean	24.1	26.9	14.1	43.1
Std. Dev.	9.0	11.8	6.7	11.4

*Phase 0 = prior to shortening, phase 1 = no morphological change, phase 2 = start of cord buckling, and phase 3 = cord kinking and spinal cord injury.

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TABLE II Spinal Cord Blood Flow at Each Phase of the Spinal Column Shortening*

	Spinal Cord Blood Flow (mL/100 g/min)			Decrease in Spinal Cord Blood Flow Between Baseline and Spinal Cord Injury (%)
Pig No.	Phases 0 and 1 (Baseline)	Phase 2	Phase 3
1	12	15	5	58.3
2	45	55	28	37.8
3	22	30	15	31.8
4	22	24	12	45.5
5	20	15	7	65.0
6	30	30	16	46.7
7	20	24	13	35.0
8	22	18	14	36.4
9	30	34	21	30.0
10	18	24	10	44.4
Mean	24.1	26.9	14.1	43.1
Std. Dev.	9.0	11.8	6.7	11.4

*Phase 0 = prior to shortening, phase 1 = no morphological change, phase 2 = start of cord buckling, and phase 3 = cord kinking and spinal cord injury.

Stagnara Wake-Up Test

A wake-up test was performed thirty minutes after the conclusion of the shortening procedure by discontinuing the anesthetic agents and monitoring movement in the hindlimbs following painful stimuli. However, no movements were observed. Movement in the forelimbs was observed on wake-up, suggesting that reversal of the anesthesia was complete.

Histopathological Examination

We observed epineural hematoma formation with infiltration of neutrophils, indicative of spinal cord injury and edema. In addition, vertical fissures were observed in the axonal fibers, suggesting cutting and neuronal necrosis resulting from compressive forces and ischemia. Macrophage infiltration was also visible, suggesting edematous changes following the spinal cord injury (Fig. 3). These results suggest that structural changes in the spinal cord caused the spinal cord injury.

Fig. 3

Histopathological slides of spinal cord specimens that demonstrated epineural hematoma (a) and axonal cleavage (arrow) and macrophage infiltration due to the ischemia (b) (hematoxylin and eosin).

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Discussion

Leatherman and Dickson³⁴ stressed that the only method that can correct a rigid deformity without the risk of neurological complications is shortening and straightening the spine. However, several investigators have reported that neurological complications may also result during a spinal shortening procedure^35-40. The spinal column is shortened during vertebral osteotomy, posterior vertebral column resection, or en bloc vertebrectomy, resulting in redundancy of the spinal cord relative to the spine^39,40. Dural buckling can occur if a closing-wedge osteotomy results in >35° of correction at any one level³⁹. The current study examined the effects of spinal column shortening during a posterior vertebral column resection procedure on spinal cord function in ten pigs in order to establish the safe range of spinal shortening in this animal model.

Somatosensory evoked potentials can be used to evaluate sensory neural pathways continuously during surgery, without hindering the surgeon, even if muscle relaxants are applied intraoperatively. However, a number of false-negative findings have been reported^41-44. Monitoring of motor evoked potentials, which allows an assessment of the functional status of motor pathways¹¹, can facilitate more rapid identification of impending spinal cord injury⁴⁵, since changes in motor evoked potentials are detectable earlier than changes in somatosensory evoked potentials are. Schwartz et al.⁴⁵ provided convincing evidence that motor evoked potentials are more sensitive to evolving spinal cord injury than somatosensory evoked potentials are, and other studies have supported this finding^43,46,47. In addition to evoked potential monitoring, all surgical procedures involving multisegment fusion should routinely include intraoperative monitoring of neurological function^33,48. We evaluated the functional status of the spinal cord with use of the wake-up test after establishing the existence of spinal cord injury on the basis of the motor evoked potentials. The functional status, as determined by the motor response to painful stimuli, was consistent with the motor evoked potential data and confirmed the reliability of the motor evoked potential monitoring.

The two preferred methods of monitoring spinal cord blood flow involve the use of laser Doppler flowmetry^49,50 and fluorescent microspheres^51,52. For instance, Kato et al.⁵⁰ used laser Doppler flowmetry to examine the effect of interrupting the bilateral segmental arteries arising from the artery of Adamkiewicz on the spinal cord blood flow. Kawahara et al.³² studied the effects of acute spinal shortening on spinal cord blood flow with the use of spinal cord angiography involving fluorescent microspheres. The aim of the current study was to create an animal model assessing spinal cord injury after acute spinal shortening with use of motor evoked potentials supplemented with a Stagnara wake-up test and assessing spinal cord blood flow with use of laser Doppler flowmetry.

Damage to the spinal cord does not stop immediately after the initial injury, but continues during the subsequent hours. This delayed injury process presents an opportunity for treatments aimed at reducing the extent of the disability resulting from spinal cord injury. Good preclinical data are essential for predicting which treatments would be most useful. Previous spinal cord injury models have involved direct injury to the spinal cord by transection or crushing, resulting in spinal cord damage that is different from the damage caused by spinal shortening^24-26,53,54. Fiford et al.⁵⁵ recently developed a vertebral dislocation model in rats that produces axonal and vascular injury within the spinal cord. However, most spinal surgery, and particularly spinal shortening, can cause spinal cord injury.

We chose swine for our pilot animal model of spinal column shortening because the spinal column is large enough to permit the use of pedicle screw instrumentation^56-58. The spinal cord terminates near the L6 level in pigs. The T11 and T12 levels were used in our spinal shortening experiment because these levels have a precarious blood supply, and a minor injury at these levels could cause spinal cord injury in an area corresponding to the midthoracic spine in humans^56,58. Kawahara et al. reported that shortening by up to one-third of the height of a vertebral segment in dogs resulted in no deformity of the dural sac or the spinal cord (phase 1), shortening by between one-third and two-thirds of the vertebral height resulted in shrinking and buckling of the dural sac but no spinal cord deformity (phase 2), and shortening by more than two-thirds of the vertebral height resulted in spinal cord deformity and compression due to the buckling of the dura (phase 3)³². Spinal shortening within the safe range increased spinal cord blood flow. The same phases of spinal shortening were observed in the current experiment, and spinal shortening of more than one vertebral body height at the vertebrectomy level resulted in spinal cord kinking (phase 3), a loss of motor evoked potential signals, and paralysis. Our current experiment differed from that of Kawahara et al. in the use of pigs rather than dogs as an experimental animal, the monitoring of motor evoked potentials rather than somatosensory evoked potentials (which have a higher likelihood of false-negative and false-positive results^41-44,59-65), and the use of laser Doppler flowmetry rather than spinal angiography to monitor the spinal cord blood flow. The spinal cord blood flow measurements in our current study were easier to perform by applying a 24-mm laser probe over the dura at the spinal shortening level. Furthermore, the slight increase in the spinal cord blood flow noted during phase 2 of the spinal shortening in our study, although not significantly different from the baseline value, was similar to that reported by Kawahara et al.³⁸.

No other previous study has reported the extent of spinal shortening relative to the mean body height of the involved vertebrae and to the mean segmental height of the entire spinal column. Our results showed that spinal cord injury was induced by spinal shortening equivalent to one vertebral level at the thoracolumbar (T11-12) junction, as shortening by 104% of the vertebral height at T11-12 resulted in spinal cord injury during phase 3. However, spinal cord injury was not induced by spinal shortening equivalent to the mean segmental height of the entire spinal column (T1-L6), as shortening by 74% of the vertebral height at T11-12 did not result in spinal cord injury during phase 2. Shortening by a distance that is intermediate between the mean segmental height of the entire spinal column (T1-L6) and the mean thoracolumbar vertebral height (T11-12) represented a zone of uncertainty in which spinal cord injury could not be accurately predicted. Histopathological examination of the spinal cord specimens indicated that spinal shortening caused significant neuronal damage as a result of ischemic and edematous changes in the axon fibers that ultimately led to axonal cutting and intradural and epidural hematoma formation. Our findings demonstrated that spinal cord injury can result from structural changes in the spinal cord resulting from spinal shortening as well as from a vascular insult.

Delamarter et al.⁶⁶ employed a circumferential cable compression model to induce spinal cord injury in dogs and noted that neurological function improved following decompression after one hour. Carlson et al.^67,68 also reported neurological improvement following decompression after one hour in a canine model. Rabinowitz et al.⁶⁹ used a nylon tie to induce spinal cord injury in a canine model, and observed neurological recovery following decompression after six hours. Kobrine et al.⁷⁰ evaluated spinal cord injury in a primate model with use of an extradural balloon and found that early decompression promoted neurological recovery. However, the major shortcoming of our study was that the pigs did not survive long enough to determine whether recovery would have occurred. The mean arterial pressure was maintained above 80 mm Hg throughout the surgical procedure and for thirty minutes thereafter. However, continuous bleeding from the osteotomy sites would eventually have caused the mean blood pressure to drop below 80 mm Hg in the absence of a blood transfusion. If the mean arterial pressure is too low, the spinal cord can be injured because of hypoperfusion. Since it would have been difficult to transfuse blood into the pigs following the vertebral column resection to counteract the continuing blood loss, all functions were monitored for thirty minutes after the resection, and the pigs were then killed after the wake-up test as part of the experimental protocol. Further research on pigs that includes blood transfusion is warranted in order to determine the pattern of recovery. We were also unable to assess the role of decompression because adequate decompression was performed prior to spinal shortening in our study. Therefore, our study examined only the immediate effect of spinal shortening on spinal cord function and blood flow. Further research with this model should provide useful information about the relationship between the amount of spinal shortening and spinal cord injury.

Appendix

A table showing the body weight, spinal column length, and estimated intraoperative blood loss of each pig is available with the online version of this article as a data supplement at jbjs.org.

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Topics

vascular flow ; evoked potentials, motor ; spinal cord injuries ; family suidae ; spinal cord ; intraoperative wake-up test

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Hitesh N. Modi, Seung-Woo Suh, Jae-Young Hong, Jae-Hyuk Yang; The Effects of Spinal Cord Injury Induced by Shortening on Motor Evoked Potentials and Spinal Cord Blood FlowAn Experimental Study in Swine. The Journal of Bone & Joint Surgery. 2011 Oct;93(19):1781-1789.

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