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Hiroshi Ozawa, Takeo Matsumoto, Toshiro Ohashi, Masaaki Sato and Shoichi Kokubun

Object. Although the gray matter of the spinal cord has been thought to be softer than the white matter, there is no evidence to support this belief. Because the spinal cord is extremely soft, it has been difficult to measure the mechanical properties of the gray and white matter. The modulis of elasticity of the gray and white matter were measured in situ by using a pipette aspiration method.

Method. The spinal cord specimens were excised from Japanese white rabbits. Specimens were cut to display the surfaces of axial, frontal, and sagittal sections. The surfaces of the gray and white matter were aspirated using a 0.8-mm-inner-diameter glass pipette while monitoring with a video microscope, and the deformed length in the pipette was measured on a monitor. In each case the modulus of elasticity was calculated by comparing the relationship between the aspiration pressure and aspirated volume of the specimen with that determined by finite element analysis.

The moduli of elasticity of the gray and white matter were 3.4 ± 1.4 kPa (mean ± standard deviation) and 3.4 ± 0.9 kPa in the axial section, 3 ± 0.3 kPa and 3.5 ± 0.5 kPa in the frontal section, and 3.5 ± 0.9 kPa and 2.8 ± 0.4 kPa in the sagittal section, respectively.

Conclusions. No significant difference in modulus of elasticity was shown between the gray and white matter of the spinal in sections made in various directions.

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Hiroshi Kanno, Yukihiko Ozawa, Katsumi Sakata, Hidemitsu Sato, Yutaka Tanabe, Nobuyuki Shimizu and Isao Yamamoto

Object. The goal of this study was to evaluate intraoperative power Doppler ultrasonography when used with a contrast-enhancing agent for operations on intracranial tumors.

Methods. Forty intracranial tumors were examined using power Doppler ultrasonography with a galactose micro-particle—based ultrasonographic contrast-enhancing agent during operations on the brain. The tumors included 37 intracranial neoplasms (14 gliomas, six meningiomas, three hemangioblastomas, two malignant lymphomas, three other primary neoplasms, nine metastatic tumors, and three nonneoplastic lesions). All patients also underwent computerized tomography and magnetic resonance imaging, and all but three of the patients underwent digital subtraction (DS) angiography. Before injection of the ultrasonographic contrast agent, intra- and peritumoral power Doppler flow signals were detected in 32 of the intracranial tumors. After the injection, the signals were enhanced in blood vessels around the tumors and in the tumor parenchyma in 36 tumors. The duration of contrast enhancement continued for 70 to 365 seconds (mean 251.8 ± 69 seconds) after the injection. Among the tumors, hemangioblastomas displayed particularly strong contrast enhancement. In these intracranial tumors, the echo signals obtained using contrast-enhanced power Doppler ultrasonography correlated with DS angiographic staining. Power Doppler ultrasonograms with the appropriate contrast agent provided better data on the precise real-time position of the tumors and their relationship to adjacent vessels than ultrasonograms obtained before the injection of the contrast agent.

Conclusions. Intraoperative power Doppler ultrasonography performed using a contrast-enhancing agent can facilitate intraoperative real-time navigation and assessment of the intratumoral vasculature and peritumoral vessels, particularly for tumors having abundant vessels such as hemangioblastomas.

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Hiroshi Ozawa, Takeo Matsumoto, Toshiro Ohashi, Masaaki Sato and Shoichi Kokubun

Object. The pia mater has received little attention regarding its function in the deformation of the spinal cord under compression. In this study the mechanical properties and function of the spinal pia mater were investigated using three methods.

Methods. Spinal cord segments were excised from rabbits. The elastic modulus of the pia mater was measured by performing a tensile test using specimens with the pia mater intact and ones with the pia mater stripped off. The stiffness of the spinal cord was examined by performing a compression test with specimens containing an intact pia mater and ones with a pia mater that was incised at both sides. The cross-sectional area and circumference of the spinal cord were measured on axial views of magnetic resonance images in patients with cervical disc herniations before and after surgery.

The pia mater had an elastic modulus of 2300 kPa, which was 460 times higher than that of spinal cord parenchyma. By covering the parenchyma, it tripled the overall elastic modulus of the spinal cord. The pia mater increased the stiffness of the spinal cord and enhanced its shape recovery after removal of the compression. The cross-sectional area of the spinal cord increased after surgery, whereas the circumference of the spinal cord changed little.

Conclusions. The pia mater firmly covers the spinal cord and has a high elastic modulus; it therefore provides a constraint on the spinal cord surface. It prevents elongation of the circumference and produces a large strain energy that is responsible for shape restoration following decompression.

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Hiroshi Ozawa, Shoichi Kokubun, Toshimi Aizawa, Takeshi Hoshikawa and Chikashi Kawahara

Object

The authors analyzed a series of 118 cases of spinal dumbbell tumors to elucidate the feature of the tumors.

Methods

Of 674 cases of spinal cord tumors, the incidence of dumbbell tumors was studied. The tumors were analyzed, and the authors focus on the distribution of age and sex, the pathological diagnoses, their locations, Eden classification, and the surgical methods used.

Results

The incidence of dumbbell tumors was 18%. The mean patient age was 43 years, which was younger than that for all spinal cord tumors (mean 50 years). There were 11 patients younger than 10 years of age. The rate of dumbbell tumors in the cervical spine was significantly higher than that of all spinal cord tumors. Fifteen (18%) of the 81 schwannomas were observed in the C-2 nerve root, thus having a higher incidence than those in the other nerve roots. In 99 cases (84%), the tumors were removed through a hemilaminectomy with or without a facetectomy and posterior fusion. Of 118 cases, 69% of the tumors were schwannomas, and malignant tumors were found in 10 cases (8.5%). Seven (64%) of 11 patients younger than 10 years of age had malignant tumors. Three patients older than 10 years of age had malignant tumors, thus accounting for 2.8% of the 107 older patients.

Conclusions

The incidence of dumbbell tumors was 18%, and they are not uncommon. Malignant dumbbell tumors were more common in children younger than 10 years of age than in older patients.

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Kenichiro Yahata, Haruo Kanno, Hiroshi Ozawa, Seiji Yamaya, Satoshi Tateda, Kenta Ito, Hiroaki Shimokawa and Eiji Itoi

OBJECTIVE

Extracorporeal shock wave therapy (ESWT) is widely used to treat various human diseases. Low-energy ESWT increases expression of vascular endothelial growth factor (VEGF) in cultured endothelial cells. The VEGF stimulates not only endothelial cells to promote angiogenesis but also neural cells to induce neuroprotective effects. A previous study by these authors demonstrated that low-energy ESWT promoted expression of VEGF in damaged neural tissue and improved locomotor function after spinal cord injury (SCI). However, the neuroprotective mechanisms in the injured spinal cord produced by low-energy ESWT are still unknown. In the present study, the authors investigated the cell specificity of VEGF expression in injured spinal cords and angiogenesis induced by low-energy ESWT. They also examined the neuroprotective effects of low-energy ESWT on cell death, axonal damage, and white matter sparing as well as the therapeutic effect for improvement of sensory function following SCI.

METHODS

Adult female Sprague-Dawley rats were divided into the SCI group (SCI only) and SCI-SW group (low-energy ESWT applied after SCI). Thoracic SCI was produced using a New York University Impactor. Low-energy ESWT was applied to the injured spinal cord 3 times a week for 3 weeks after SCI. Locomotor function was evaluated using the Basso, Beattie, and Bresnahan open-field locomotor score for 42 days after SCI. Mechanical and thermal allodynia in the hindpaw were evaluated for 42 days. Double staining for VEGF and various cell-type markers (NeuN, GFAP, and Olig2) was performed at Day 7; TUNEL staining was also performed at Day 7. Immunohistochemical staining for CD31, α-SMA, and 5-HT was performed on spinal cord sections taken 42 days after SCI. Luxol fast blue staining was performed at Day 42.

RESULTS

Low-energy ESWT significantly improved not only locomotion but also mechanical and thermal allodynia following SCI. In the double staining, expression of VEGF was observed in NeuN-, GFAP-, and Olig2-labeled cells. Low-energy ESWT significantly promoted CD31 and α-SMA expressions in the injured spinal cords. In addition, low-energy ESWT significantly reduced the TUNEL-positive cells in the injured spinal cords. Furthermore, the immunodensity of 5-HT–positive axons was significantly higher in the animals treated by low-energy ESWT. The areas of spared white matter were obviously larger in the SCI-SW group than in the SCI group, as indicated by Luxol fast blue staining.

CONCLUSIONS

The results of this study suggested that low-energy ESWT promotes VEGF expression in various neural cells and enhances angiogenesis in damaged neural tissue after SCI. Furthermore, the neuroprotective effect of VEGF induced by low-energy ESWT can suppress cell death and axonal damage and consequently improve locomotor and sensory functions after SCI. Thus, low-energy ESWT can be a novel therapeutic strategy for treatment of SCI.

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Hiroshi Ozawa, Takashi Kusakabe, Toshimi Aizawa, Takeshi Nakamura, Yushin Ishii and Eiji Itoi

The authors describe 2 patients with C-2 nerve root tumors in whom the lesions were located bilaterally in the lateral portions of the C1–2 interlaminar space and compressed the spinal cord when the atlantoaxial joint was rotated.

The patients were adult men with neurofibromatosis. Each presented with clumsiness of both hands and motor weakness of the extremities accompanied by spastic gait. Magnetic resonance imaging of the cervical spine performed with the neck in the neutral position showed tumors at the bilateral lateral portion of the C1–2 interlaminar space without direct compression of the spinal cord. The spinal cord exhibited an I-shaped deformity at the same level as the tumors in one case and a trapezoidal deformity at the same level as the tumors in the other case. Computed tomography myelography and MRI on rotation of the cervical spine revealed bilateral intracanal protrusion of the tumors compressing the spinal cord from the lateral side. The tumors were successfully excised and occipitocervical fusion was performed.

The tumors were pushed out into the spinal canal from the bilateral lateral portion of the interlaminar spaces due to rotation of the atlantoaxial joint. This was caused by a combination of posteromedial displacement of the lateral mass on the rotational side of the atlas and narrowing of the lateral portion of the interlaminar space on the contralateral side due to the coupling motion of the lateral bending and extension of the atlas. The spinal cord underwent compression from both lateral sides in a one-way rotation. Without sustained spinal cord compression, intermittent long-term dynamic spinal cord compression from both lateral sides should induce a pathognomonic spinal cord deformity and the onset of paralysis. To the authors' knowledge, there have been no reports of the present conditions—that is, the bilateral protrusion of tumors from the bilateral lateral portion of the C1–2 interlaminar spaces into the spinal canal due to atlantoaxial rotation.

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Shoichi Kokubun, Hiroshi Ozawa, Toshimi Aizawa, Ngo Minh Ly and Yasuhisa Tanaka

Object

Tethered cord syndrome (TCS) is a disorder involving an abnormal stretching of the tethered spinal cord caused by several pathological conditions and presents with a variety of neurological symptoms. Untethering (tethered cord release) is the gold standard treatment for TCS. However, untethering carries risks of spinal cord injury and postoperative retethering. To avoid these potential risks, the authors applied spine-shortening osteotomy to adult patients with TCS, and report on the surgical procedure and treatment outcomes.

Methods

Eight patients with TCS caused by a lipomyelomeningocele were surgically treated by the authors' original procedure of spine-shortening osteotomy. Six patients were male and 2 were females; average age at the time of surgery was 31 years old. Spine-shortening osteotomy was performed at the level of L-1 in all but 2 patients, in whom it was performed at T-12, with spinal fusion between T-12 and L-2 or T-11 and L-1 using a pedicle screw–rod system. The average follow-up period was 6.2 years and the patients' pre- and postoperative conditions were evaluated clinically and radiologically.

Results

Preoperatively, all patients displayed severe neurological deficits such as motor disturbance, muscle atrophy, and bladder dysfunction. Several months before surgery, all showed progressive symptoms. Those symptoms showed initial improvement in 6 patients and stabilized in 2 postoperatively, but the improved symptoms worsened again in 4 of the 6 patients. The osteotomized vertebrae were shortened by 21 mm on average, and all spines showed complete bone union without loss of correction. At the final follow-up evaluations, 6 patients showed stabilization as per the modified Japanese Orthopaedic Association score for thoracic myelopathy.

Conclusions

Spine-shortening osteotomy successfully helps reduce the spinal cord tension without causing direct neural damage. At minimum, it stabilized the patients' symptoms and/or helped delay neurological deterioration for a period of time. Spine-shortening osteotomy might be a feasible mode of treatment for adult TCS caused by a spinal lipoma.

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Haruo Kanno, Toshimi Aizawa, Hiroshi Ozawa, Takeshi Hoshikawa, Eiji Itoi and Shoichi Kokubun

The authors report a rare case of tethered cord syndrome with low-placed conus medullaris complicated by a vertebral fracture that was successfully treated by a spine-shortening vertebral osteotomy. The patient was a 57-year-old woman whose neurological condition worsened after a T-12 vertebral fracture because a fracture fragment and the associated local kyphotic deformity directly compressed the tethered spinal cord. An osteotomy of the T-12 vertebra was performed in order to correct the kyphosis, remove the fracture fragment, and reduce the tension on the spinal cord. Postoperative radiographs showed the spine to be shortened by 22 mm, and the kyphosis between T-11 and L-1 improved from 23° to 0°. Two years after the surgery, the patient's neurological symptoms were resolved. The bone union was complete with no loss of correction.

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Muneyoshi Yasuda, Hiroshi Nakagawa, Hiroaki Ozawa, Chikage Inukai, Takeya Watabe, Junichi Mizuno and Masakazu Takayasu

This case report presents the unusual holospinal dissemination of a neurenteric cyst, which was successfully treated by fenestration and placement of a subarachnoid-peritoneal (SP) shunt. The patient was a 46-year-old Japanese woman with a history of fourth ventricle neurenteric cysts, which were managed with cyst fenestration in 1996 and 2005. She had been doing well until January 2006, when she developed dizziness and an unsteady gait. A neurological examination revealed a disturbance in the deep sensation of the feet. A neuroimaging evaluation demonstrated multiple cystic lesions in the whole spinal canal, which significantly distorted the spinal cord. Because the spinal cord distortion was the most severe in the lower cervical to upper thoracic areas, a unilateral osteoplastic laminotomy with an endoscopic cyst fenestration was performed in these areas, followed by placement of an SP shunt. The pathological diagnosis was a disseminated neurenteric cyst. There was no malignancy, and the patient has been well, with an improved gait and no signs of peritoneal dissemination, for > 1 year.

The present case showed a unique extent of dissemination, which was most likely a secondary characteristic. Neurenteric cysts are well known for their tendency to recur, and total removal is usually difficult because of adhesion of the cyst membrane to important structures. The lesion also compromises cerebrospinal fluid circulation. Cyst fenestration combined with SP shunt placement might be a treatment option in such a case.

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Seiji Yamaya, Hiroshi Ozawa, Haruo Kanno, Koshi N. Kishimoto, Akira Sekiguchi, Satoshi Tateda, Kenichiro Yahata, Kenta Ito, Hiroaki Shimokawa and Eiji Itoi

Object

Extracorporeal shock wave therapy (ESWT) is widely used for the clinical treatment of various human diseases. Recent studies have demonstrated that low-energy ESWT upregulates the expression of vascular endothelial growth factor (VEGF) and promotes angiogenesis and functional recovery in myocardial infarction and peripheral artery disease. Many previous reports suggested that VEGF produces a neuroprotective effect to reduce secondary neural tissue damage after spinal cord injury (SCI). The purpose of the present study was to investigate whether lowenergy ESWT promotes VEGF expression and neuroprotection and improves locomotor recovery after SCI.

Methods

Sixty adult female Sprague-Dawley rats were randomly divided into 4 groups: sham group (laminectomy only), sham-SW group (low-energy ESWT applied after laminectomy), SCI group (SCI only), and SCI-SW group (low-energy ESWT applied after SCI). Thoracic spinal cord contusion injury was inflicted using an impactor. Low-energy ESWT was applied to the injured spinal cord 3 times a week for 3 weeks. Locomotor function was evaluated using the Basso, Beattie, and Bresnahan (BBB) Scale (open field locomotor score) at different time points over 42 days after SCI. Hematoxylin and eosin staining was performed to assess neural tissue damage in the spinal cord. Neuronal loss was investigated by immunostaining for NeuN. The mRNA expressions of VEGF and its receptor, Flt-1, in the spinal cord were assessed using real-time polymerase chain reaction. Immunostaining for VEGF was performed to evaluate VEGF protein expression in the spinal cord.

Results

In both the sham and sham-SW groups, no animals showed locomotor impairment on BBB scoring. Histological analysis of H & E and NeuN stainings in the sham-SW group confirmed that no neural tissue damage was induced by the low-energy ESWT. Importantly, animals in the SCI-SW group demonstrated significantly better locomotor improvement than those in the SCI group at 7, 35, and 42 days after injury (p < 0.05). The number of NeuN-positive cells in the SCI-SW group was significantly higher than that in the SCI group at 42 days after injury (p < 0.05). In addition, mRNA expressions of VEGF and Flt-1 were significantly increased in the SCI-SW group compared with the SCI group at 7 days after injury (p < 0.05). The expression of VEGF protein in the SCI-SW group was significantly higher than that in the SCI group at 7 days (p < 0.01).

Conclusions

The present study showed that low-energy ESWT significantly increased expressions of VEGF and Flt-1 in the spinal cord without any detrimental effect. Furthermore, it significantly reduced neuronal loss in damaged neural tissue and improved locomotor function after SCI. These results suggested that low-energy ESWT enhances the neuroprotective effect of VEGF in reducing secondary injury and leads to better locomotor recovery following SCI. This study provides the first evidence that low-energy ESWT can be a safe and promising therapeutic strategy for SCI.