Spinal cord hemangioblastomas: significance of intraoperative neurophysiological monitoring for resection and long-term outcome

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  • Neurosurgical Clinic, Clinic of the University of Munich (LMU), Campus Grosshadern, Munich, Germany
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OBJECTIVE

Spinal cord hemangioblastomas are rare benign tumors developing either sporadically or as part of von Hippel-Lindau (VHL) disease. Generally, resection is the treatment of choice. However, the significance of intraoperative neurophysiological monitoring (IONM) for resection and postoperative outcome is still controversial. The authors analyzed the surgical and clinical courses of patients who had undergone resection of spinal cord hemangioblastoma, with special attention to preoperative imaging, the use of IONM, and short- and long-term outcomes.

METHODS

A series of 24 patients (male/female 1:1, lesion sporadic/associated with VHL 2.4:1) who had undergone 26 operations for the resection of 27 spinal cord hemangioblastomas was analyzed. All patients had undergone pre- and postoperative contrast-enhanced MRI. In all cases, microsurgical tumor removal had been performed under continuous IONM of both somatosensory and transcranial motor evoked potentials as well as electromyographic recording. Clinical characteristics, imaging findings, and operative records were retrospectively analyzed. Outcome parameters included short- and long-term status as regards sensorimotor deficits and a questionnaire on general performance, patient satisfaction, and Oswestry Disability Index (ODI) at the end of the follow-up period. The impact of IONM findings on postoperative deficits and outcome parameters as well as risk factors affecting functional prognosis was statistically assessed.

RESULTS

Preoperative symptoms (mean duration 16.2 ± 22.0 months) included sensory changes (100.0%), pain (66.7%), spinal ataxia (66.7%), motor deficit (41.7%), and bladder/bowel dysfunction (12.5%). Average age at the first operation was 36.8 ± 12.8 years. Most tumors (21 intramedullary, 6 intra- and/or extramedullary) were located dorsally (92.6%) and cervically (77.8%) and were accompanied by peritumoral edema and/or syringomyelia (81.5%). Tumor resection was achieved via laminectomy for 15 tumors, hemilaminectomy for 5, laminoplasty for 6, and interlaminar approach for 1. Gross-total resection was accomplished for 26 tumors (96.3%) with no local tumor recurrence during follow-up. Intraoperative neurophysiological monitoring was nonpathological in 11 operations (42.3%) and pathological in 15 (57.7%). Patients with nonpathological IONM had significantly fewer new sensorimotor deficits (p = 0.005). Long-term follow-up evaluation (mean 7.9 ± 4.0 years postoperatively, 7 patients lost to follow-up) revealed a stable or improved McCormick myelopathy grade in 88.2% of the patients, and 88.2% reported a stable or improved overall outcome according to Odom's criteria. Long-term general performance was excellent with 88.2% having a WHO/Eastern Cooperative Oncology Group (ECOG) Performance Status grade ≤ 1, 76.5% a Karnofsky Performance Scale score ≥ 80, and 70.6% a Barthel Index (BI) of 100. The mean ODI (11.4% ± 12.5%) indicated only minimal disability. There was a significant correlation between pathological IONM findings and a worse long-term status according to the BI and ODI (p = 0.011 and 0.024, respectively). Additionally, VHL disease was a risk factor affecting functional prognosis (p = 0.044).

CONCLUSIONS

Microsurgical removal of spinal cord hemangioblastomas with IONM facilitates a satisfying long-term outcome for patients. Nonpathological IONM findings are associated with a lower risk of new sensorimotor deficits and correlate with a better overall long-term outcome. von Hippel–Lindau disease is a risk factor for a worse long-term prognosis.

ABBREVIATIONS

BI = Barthel Index; ECOG = Eastern Cooperative Oncology Group; EMG = electromyography; IMSCT = intramedullary spinal cord tumor; IONM = intraoperative neurophysiological monitoring; KPS = Karnofsky Performance Scale; NPV = negative predictive value; ODI = Oswestry Disability Index; PPV = positive predictive value; PSI = Patient Satisfaction Index; SSEP = somatosensory evoked potential; TcMEP = transcranial motor evoked potential; VHL = von Hippel-Lindau.

OBJECTIVE

Spinal cord hemangioblastomas are rare benign tumors developing either sporadically or as part of von Hippel-Lindau (VHL) disease. Generally, resection is the treatment of choice. However, the significance of intraoperative neurophysiological monitoring (IONM) for resection and postoperative outcome is still controversial. The authors analyzed the surgical and clinical courses of patients who had undergone resection of spinal cord hemangioblastoma, with special attention to preoperative imaging, the use of IONM, and short- and long-term outcomes.

METHODS

A series of 24 patients (male/female 1:1, lesion sporadic/associated with VHL 2.4:1) who had undergone 26 operations for the resection of 27 spinal cord hemangioblastomas was analyzed. All patients had undergone pre- and postoperative contrast-enhanced MRI. In all cases, microsurgical tumor removal had been performed under continuous IONM of both somatosensory and transcranial motor evoked potentials as well as electromyographic recording. Clinical characteristics, imaging findings, and operative records were retrospectively analyzed. Outcome parameters included short- and long-term status as regards sensorimotor deficits and a questionnaire on general performance, patient satisfaction, and Oswestry Disability Index (ODI) at the end of the follow-up period. The impact of IONM findings on postoperative deficits and outcome parameters as well as risk factors affecting functional prognosis was statistically assessed.

RESULTS

Preoperative symptoms (mean duration 16.2 ± 22.0 months) included sensory changes (100.0%), pain (66.7%), spinal ataxia (66.7%), motor deficit (41.7%), and bladder/bowel dysfunction (12.5%). Average age at the first operation was 36.8 ± 12.8 years. Most tumors (21 intramedullary, 6 intra- and/or extramedullary) were located dorsally (92.6%) and cervically (77.8%) and were accompanied by peritumoral edema and/or syringomyelia (81.5%). Tumor resection was achieved via laminectomy for 15 tumors, hemilaminectomy for 5, laminoplasty for 6, and interlaminar approach for 1. Gross-total resection was accomplished for 26 tumors (96.3%) with no local tumor recurrence during follow-up. Intraoperative neurophysiological monitoring was nonpathological in 11 operations (42.3%) and pathological in 15 (57.7%). Patients with nonpathological IONM had significantly fewer new sensorimotor deficits (p = 0.005). Long-term follow-up evaluation (mean 7.9 ± 4.0 years postoperatively, 7 patients lost to follow-up) revealed a stable or improved McCormick myelopathy grade in 88.2% of the patients, and 88.2% reported a stable or improved overall outcome according to Odom's criteria. Long-term general performance was excellent with 88.2% having a WHO/Eastern Cooperative Oncology Group (ECOG) Performance Status grade ≤ 1, 76.5% a Karnofsky Performance Scale score ≥ 80, and 70.6% a Barthel Index (BI) of 100. The mean ODI (11.4% ± 12.5%) indicated only minimal disability. There was a significant correlation between pathological IONM findings and a worse long-term status according to the BI and ODI (p = 0.011 and 0.024, respectively). Additionally, VHL disease was a risk factor affecting functional prognosis (p = 0.044).

CONCLUSIONS

Microsurgical removal of spinal cord hemangioblastomas with IONM facilitates a satisfying long-term outcome for patients. Nonpathological IONM findings are associated with a lower risk of new sensorimotor deficits and correlate with a better overall long-term outcome. von Hippel–Lindau disease is a risk factor for a worse long-term prognosis.

ABBREVIATIONS

BI = Barthel Index; ECOG = Eastern Cooperative Oncology Group; EMG = electromyography; IMSCT = intramedullary spinal cord tumor; IONM = intraoperative neurophysiological monitoring; KPS = Karnofsky Performance Scale; NPV = negative predictive value; ODI = Oswestry Disability Index; PPV = positive predictive value; PSI = Patient Satisfaction Index; SSEP = somatosensory evoked potential; TcMEP = transcranial motor evoked potential; VHL = von Hippel-Lindau.

Hemangioblastomas are rare spinal cord neoplasms accounting for 2%–6% of all spinal cord tumors.2,7,28 They are histologically benign but highly vascularized tumors that can develop either sporadically or as part of von Hippel-Lindau (VHL) disease, a multicentric disorder caused by an autosomal dominant tumor suppressor gene mutation on chromosome 3p25.3. The association between VHL disease and CNS hemangioblastoma is well known and the two occur together in 23%–38% of cases.2,4,7,29 Generally, resection is the treatment of choice for spinal cord hemangioblastomas.5,7,16,22,28,36 However, because of the rarity of spinal cord hemangioblastomas, the surgical management strategies, short- and especially long-term functional outcomes, and risk factors affecting prognosis are still matters of controversy. To better define these aspects, we evaluated a series of patients who had undergone microsurgical resection of spinal cord hemangioblastomas at a single institution, devoting special attention to preoperative imaging, surgical management including the use of intraoperative neurophysiological monitoring (IONM), and functional outcome on short- and long-term follow-up evaluation.

Methods

All patients included in our analysis had been referred to our department (Neurosurgical Clinic, Clinic of the University of Munich [LMU], Germany) in the period from January 2000 to December 2013 for the resection of spinal cord hemangioblastoma. After obtaining study approval from the IRB of the Clinic of the University of Munich (LMU), Germany, we identified and retrospectively reviewed medical records and radiological studies for 24 patients from our clinic database. We analyzed epidemiological aspects, clinical characteristics, imaging findings, management strategies, operative records, complications, and individual outcomes. Of the 24 identified patients, 17 (70.8%) were available for long-term follow-up interviews and questionnaires concerning quality of life and general performance evaluations. Informed consent had been obtained previously.

Clinical Evaluation

Neurological examinations were performed and functional grades according to the classification of McCormick (Table 1)26 were assigned for all patients before and shortly (mean 9.6 ± 4.4 days, range 5–19 days) after surgery. Each patient's postoperative general clinical outcome was graded using Odom's criteria.30 Postoperatively, new or worsened sensorimotor deficits and bladder/bowel dysfunction were recorded. Long-term follow-up was assessed in a standardized telephone interview. Altogether, 17 patients were available for telephone and/or outpatient interviews regarding their symptoms and functional outcome as well as for questionnaires including the Patient Satisfaction Index (PSI),40 World Health Organization/Eastern Cooperative Oncology Group (ECOG) Performance Status Scale,31 Karnofsky Index (also known as the Karnofsky Performance Scale [KPS]),17 Barthel Index (BI),24 Oswestry Disability Index (ODI),9 and SF-36v2 Health Survey. Mean follow-up among those patients was 7.9 ± 4.0 years (range 1.1–14.1 years).

TABLE 1.

McCormick clinical grading scale for neurological function*

GradeDefinition
INeurologically normal; mild focal deficit not significantly affecting function of involved limb; mild spasticity or reflex abnormality; normal gait
IIPresence of sensorimotor deficit affecting function of involved limb; mild to moderate gait difficulty; severe pain or dysesthetic syndrome impairing patient's quality of life; still functions and ambulates independently
IIIMore severe neurological deficit; requires cane/brace for ambulation or has significant bilateral upper extremity impairment; may or may not function independently
IVSevere deficit; requires wheelchair or cane/brace with bilateral upper extremity impairment; usually not independent

Reproduced from McCormick et al: J Neurosurg 72:523–532, 1990. Published with permission.

Imaging Evaluation

Evaluation of tumor location and distribution was based on preoperative contrast-enhanced MRI. On the basis of radiological and intraoperative observations, we characterized tumors as either dorsal or ventral of the coronary spinal cord midline and as completely intramedullary, intramedullary-extramedullary (≤ 50% of tumor was extramedullary), or primarily extramedullary (< 50% of tumor was intramedullary). Gross-total resection was defined as complete tumor removal according to intraoperative microscopic findings and postoperative contrast-enhanced T1-weighted MRI. The presence and extent of edema and syringomyelia were assessed using T2-weighted and/or FLAIR MRI sequences.

Surgical Procedures

No patient underwent preoperative embolization, external beam radiation therapy, or radiosurgery; 1 of the 24 patients had undergone biopsy of the spinal cord hemangioblastoma for histopathological confirmation in advance of resection. Total intravenous anesthesia was induced, carefully avoiding the application of muscle relaxants except for intubation purposes. For tumor resection, patients were placed prone. Via a posterior midline approach, the lamina and spinous processes overlying the tumor were exposed, and laminotomy, hemilaminectomy, laminoplasty, or interlaminar fenestration was performed to expose the tumor margins. In all cases intraoperative ultrasonography was used before dural opening to ensure precise exposure of the tumor. Feeding arteries located at the pial surface were coagulated, and tumor was exposed by circumferential dissection at the tumorpia margin and by application of gentle traction to the tumor via a micro-dissector or suction tip. Bleeding from the tumor was controlled with circumferential coagulation, and tumor was usually removed en bloc with the major draining veins left intact until the end of tumor removal. For dorsolateral tumors, the dorsal root fascicles were mobilized and divided to facilitate an appropriate view of the tumor surface for removal. After confirming complete resection by intraoperative ultrasonography, the dura was closed in a watertight manner. For patients with VHL disease and multiple lesions, we removed the symptomatic lesions; adjacent tumors were resected only if possible without further injury. Moreover, surgery was recommended if symptomatic tumor growth was observed on MR images. Altogether, 26 operations for the resection of 27 spinal cord hemangioblastomas were performed until the last follow-up evaluation.

Intraoperative Neurophysiological Monitoring

In all cases, microsurgical tumor removal was performed under continuous IONM of both somatosensory and transcranial motor evoked potentials (SSEPs and TcMEPs) as well as electromyography (EMG). For stimulation and recording, we used an integrated IONM system (ISIS, Inomed). To elicit TcMEPs for recording, we positioned stimulating electrodes over C3 and C4, according to the international 10–20 system. Transcranial electric stimulation was delivered with constant current stimuli (train-of-five pulses in a biphasic fashion with an individual pulse width of 1.2–1.6 msec, an interstimulus interval of 4 msec, and a maximum intensity of 150 mA at 300 V). For recording, electrodes were placed bilaterally and intramuscularly in thenar and tibialis anterior muscles, as well as in the biceps, brachioradialis, triceps, hypothenar, iliopsoas, adductor, quadriceps femoris, tibialis anterior, foot flexor, extensor hallucis longus, and/or sphincter muscle groups according to the spinal level of interest. Somatosensory evoked potentials (individual pulse width 400 msec, repetition rate 3.7 Hz, maximum 40 mA, at least 200 averages) were elicited in the median and posterior tibial nerve, as well as at the lumbar levels and the pudendal nerve. For technical reasons, D-wave monitoring was not performed in all cases and thus was not included in our analysis.

After patient positioning, baseline recordings of SSEPs and MEPs were obtained. The SSEPs were continuously recorded throughout surgery, while MEPs were obtained every 30 minutes prior to dural opening and on the surgeon's request during tumor removal especially after manipulation of the tumor or spinal cord. Electrophysiological data were continuously analyzed by a technician trained in IONM.

A significant reduction in SSEP amplitude ≥ 50% and/or an increase in SSEP latency ≥ 2 msec, a significant decrement in TcMEP amplitude ≥ 80% (according to Langeloo et al.19), and significant spontaneous EMG activity (for example, neurotonic discharges) especially during or immediately after surgical manipulation were defined as “warning criteria of IONM” and—excluding technical reasons (for example, dislocation of electrodes), anesthesiological reasons (for example, lowering of blood pressure or body temperature, change of intravenous anesthesia management, or addition of volatile anesthetics), and temporary surgical reasons (for example, irrigation with cold saline solution)—were classified as pathological IONM findings. No significant deterioration in SSEPs, TcMEPs, and EMG monitoring during surgery was classified as nonpathological IONM findings.

In circumstances of critical IONM changes, the most recent anesthesiological and surgical steps were reconsidered, and immediate corrective actions were initiated, for example, control of electrode position, cessation of additional volatile anesthetics, correction of blood pressure, or modification of surgical technique.

Statistical Analysis

All statistical analyses were performed using Sigma-Plot for Windows version 11.0 (Systat Software Inc.). The patient population was described with summary statistics. Mean values are reported as the mean ± standard deviation. Clinical outcomes were graded based on functional status according to the McCormick classification at the short-and long-term follow-up evaluations and were categorized as 1) improved or stable or 2) worse in comparison with the preoperative status. Intraoperative neurophysiological monitoring findings were dichotomized as either 1) nonpathological or 2) pathological. Postoperative neurological status was classified as 1) no postoperative change in sensorimotor deficits or 2) new or worsened transient (< 3 months) or permanent (> 3 months) postoperative sensory changes and/or motor deficits. Fisher's exact test, Spearman rank-order correlation, and Pearson product-moment correlation were used to determine the influence of IONM findings on postoperative neurological status and on outcome parameters. To investigate other risk factors associated with clinical outcome, including patient sex, age at first clinical signs, duration of symptoms, age at first operation, presence of syrinx, VHL disease, ventral tumor location, complete intramedullary tumor, and subtotal resection, logistic regression analyses (polytomous variables) and Fisher's exact tests (dichotomous variables) were performed. Statistical significance was determined by a p < 0.05.

Results

Patient Population and Clinical Characteristics

A total of 24 patients, 12 males and 12 females (ratio 1:1), underwent microsurgical treatment for intraspinal hemangioblastomas. Mean age at first surgery was 36.8 ± 12.8 years (range 15–62 years). At the most recent followup, a total of 26 operations for the resection of 27 spinal cord hemangioblastomas had been performed with a mean of 1.1 ± 0.3 operations per patient (range 1–2 operations).

The main presenting symptoms were sensory changes in 24 patients (100%), pain and spinal ataxia in 16 patients each (66.7%), motor deficit in 10 (41.7%), and bladder/bowel dysfunction in 3 (12.5%; Table 2). Mean age at the first clinical sign was 35.4 ± 13.1 years (range 14–62 years), and the mean duration of symptoms was 16.2 ± 22.0 months (range 1.1–85.2 months). Preoperative neurological status is shown in Table 3. Overall, the median preoperative McCormick grade was II (range I–IV). Seven patients (29.2%) met the criteria for VHL disease, including 6 patients with multiple CNS hemangioblastomas, 1 patient with a family history of VHL disease, 1 with pancreas cysts, 1 with multiple kidney cysts, and 1 with both pheochromocytoma and renal cell carcinoma; some patients met more than 1 criterion.

TABLE 2.

Clinical and imaging characteristics of 24 patients with 27 resected spinal cord hemangioblastomas

CharacteristicNo. (%)
M/F12 (50.0)/12 (50.0)
Mean age at 1st clinical sign in yrs35.4 ± 13.1
Mean duration of symptoms in mos16.2 ± 22.0
Clinical symptoms
Sensory changes24 (100.0)
  Pain16 (66.7)
  Spinal ataxia16 (66.7)
  Motor deficit10 (41.7)
  Bladder/bowel dysfunction3 (12.5)
VHL disease7 (29.2)
Tumor location
  Ventral2 (7.4)
  Dorsal25 (92.6)
Tumor relation to spinal cord
  Completely intramedullary21 (77.8)
  Intramedullary-extramedullary4 (14.8)
  Primarily extramedullary2 (7.4)
No. of syringes22 (81.5)

Mean values expressed ± standard deviation.

TABLE 3.

Preoperative and postoperative neurological status according to McCormick grade

ParameterNo. of Patients (%)
Before SurgeryShort-Term Outcome (1–4 wks postop)Long-Term Outcome (1–14 yrs postop)
No. of patients242417
Grade
  I8 (33.3)7 (29.2)6 (35.3)
  II11 (45.8)10 (41.7)9 (52.9)
  III4 (16.7)4 (16.7)0 (0.0)
  IV1 (4.2)3 (12.5)2 (11.8)

There was no significant difference in epidemiological and clinical characteristics between patients with sporadic and those with VHL-associated spinal cord hemangioblastomas.

Radiological and Surgical Tumor Features

The most common tumor location was the upper (15 tumors [55.6%]) and lower (6 [22.2%]) cervical spine, followed by the thoracic spine (5 [18.5%]) and lumbar spine (1 [3.7%]). Most of the tumors were located dorsally (25 [92.6%]; Table 2 and Fig. 1). Of the 27 resected tumors, 21 (77.8%) were completely intramedullary, 4 (14.8%) were intramedullary-extramedullary, and 2 (7.4%) were primarily extramedullary. Twenty-two tumors (81.5%) were accompanied by peritumoral edema and/or syringomyelia, both clearly visible on T2-weighted and FLAIR MRI sequences.

FIG. 1.
FIG. 1.

Schematic demonstrating the distribution of spinal cord hemangioblastomas in this study. White and black circles and x's represent the 27 resected tumors and illustrate the vertebral level and relation to the dentate ligament. Adapted from Mehta et al: J Neurosurg Spine 72:233–242, 2010. Published with permission.

As with the epidemiological and clinical findings, there were no significant differences in the imaging findings between patients with sporadic and VHL-associated spinal cord hemangioblastomas; therefore, all patients were analyzed as a single group.

Intraoperative Findings and Extent of Resection

The surgical details and results of the 26 operations performed are summarized in Table 4. For the microsurgical tumor resection, laminectomy was performed for 15 tumors (55.6%), hemilaminectomy for 5 (18.5%), laminoplasty for 6 (22.2%), and an interlaminar approach for 1 (3.7%), with each of the surgical approaches enabling adequate exposure of the tumor margins.

TABLE 4.

Surgical details and results in 24 patients who underwent 26 operations

CharacteristicNo. (%)
Mean age at 1st op in yrs ± SD36.8 ± 12.8
Preop DSA2 (7.7)
Surgical approach
  Interlaminar approach1 (3.7)
  Hemilaminectomy5 (18.5)
  Laminectomy15 (55.6)
  Laminoplasty6 (22.2)
Resection status
  Gross-total resection26 (96.3)
  Subtotal resection1 (3.7)
Intraop ultrasound18 (69.2)
IONM26 (100.0)
Local tumor recurrence0 (0.0)

DSA = digital subtraction angiography.

All 17 patients with sporadic spinal cord hemangioblastoma and long-term follow-up data each underwent a single operation, and gross-total resection was achieved in all cases. In the 7 patients with VHL disease, 8 tumors were removed at the first surgery. A second operation for resection of a growing spinal cord hemangioblastoma was performed in 2 of the patients; the times between the operations were 2 months and 3 years, and both tumors had been seen in an asymptomatic state on MRI before the first operation. Thus, 9 operations were performed in the 7 VHL patients to remove 10 tumors; gross-total resection of 9 tumors and subtotal resection of 1 tumor (because surgery was terminated after severe IONM deterioration) were achieved. Altogether, a total of 26 operations were performed in 24 patients to resect 27 spinal cord hemangioblastomas. Gross-total resection was accomplished for 26 tumors (96.3%) with no local tumor recurrence during follow-up (Fig. 2); resection was subtotal for 1 tumor without further growth during follow-up. Histologically, all resected tumors were consistent with hemangioblastoma WHO Grade I.

FIG. 2.
FIG. 2.

Preoperative sagittal T2-weighted (A) and contrast-enhanced T1-weighted (B) MR images showing a hemangioblastoma at C7–T1 with associated syrinx and spinal cord edema. Postoperative sagittal T2-weighted (C) and contrast-enhanced T1-weighted (D) MR images obtained after complete tumor resection.

Clinical Outcome and IONM

Intraoperative neurophysiological monitoring data are summarized in Table 5, and the neurological and functional recovery data are summarized in Tables 3 and 6.

TABLE 5.

Intraoperative neurophysiological monitoring findings and postoperative sensorimotor deficits

IONM FindingsTotalNew or Worsened Postop Sensory Changes and/or Motor Deficits (no. of cases/total no. of cases [% of total])
NoneTransientPermanent
Pathological*15/26 (57.7)5/15 (33.3)7/15 (46.7)3/15 (20.0)
Nonpathological11/26 (42.3)10/11 (90.9)1/11 (9.1)0/11 (0.0)

Significant reduction in SSEP amplitude (≥ 50%) and/or increase in SSEP latency (≥ 2 msec) and/or significant decrement in TcMEP amplitude (≥ 80%) and/or significant spontaneous EMG activity especially during or after surgical manipulation.

Transient deficits: complete relief to the preoperative sensorimotor status within < 3 months after surgery; permanent deficits: persistent deterioration of sensorimotor status > 3 months after surgery.

TABLE 6.

Clinical outcome at different follow-up periods, according to Odom's criteria30

Outcome*No. of Patients (%)
Short-Term Outcome (1–4 wks postop, n = 24)Long-Term Outcome (1–14 yrs postop, n = 17)
Excellent0 (0.0)0 (0.0)
Good3 (12.5)7 (41.2)
Fair12 (50.0)8 (47.1)
Poor9 (37.5)2 (11.8)

Excellent: all preoperative symptoms relieved, abnormal findings improved; good: minimal persistence of preoperative symptoms, abnormal findings unchanged or improved; fair: definite relief of some preoperative symptoms, other symptoms unchanged or slightly improved; and poor: symptoms and signs unchanged or worse.

Short-Term Outcome

During the short-term follow-up period (5–19 days after surgery, all 24 patients), new or worsened sensory changes occurred after 11 operations (42.3%) and resolved within 3 months in 8 cases while remaining permanent in 3 cases. New or worsened motor deficits after surgery were present after 6 operations (23.1%) and consisted of 4 cases of a transient (< 3 months) new or worsened hemiparesis and 2 cases of a permanent new or worsened tetraparesis. Further new or worsened symptoms in the immediate postoperative period included bowel/bladder dysfunction after resection of an L-1 hemangioblastoma (3.8%) as well as internuclear ophthalmoplegia and cranial nerve disorders in a case of brainstem venous thrombosis after resection of a C-3 hemangioblastoma (3.8%). However, all short-term neurological changes were mild in the majority of cases, and neurological status according to the McCormick grading scale was maintained in most patients (79.2%). One patient (4.2%) improved by 1 McCormick grade immediately after surgery, whereas the status of 3 patients (12.5%) deteriorated by 1 grade and the status of 1 patient (4.2%) deteriorated by 3 grades, including those patients with the permanent new or worsened postoperative tetraparesis and brainstem venous thrombosis. According to Odom's criteria, most patients experienced an improved immediate clinical outcome with 3 patients (12.5%) having a “good” outcome and 12 patients (50.0%) having a “fair” outcome. Nevertheless, in 9 patients (37.5%), the Odom's criteria for a “poor” result indicated a deteriorated immediate clinical outcome.

Intraoperative Neurophysiological Monitoring

Intraoperative neurophysiological monitoring was nonpathological in 11 operations (42.3%) and pathological in 15 operations (57.7%) in which there were 10 pathological SSEPs, 8 pathological MEPs, and 9 pathological EMG events. Most pathological IONM events occurred during preparation and resection of tumors. Somatosensory evoked potentials had a sensitivity of 60% and a specificity of 75% in detecting new postoperative sensory deficits, whereas TcMEPs showed a sensitivity of 50% and a specificity of 60% in detecting new postoperative motor deficits. The negative predictive value (NPV) and positive predictive value (PPV) of SSEPs for new postoperative sensory deficits were 75% and 60%, respectively, and those of TcMEPs for new postoperative motor deficits were 83% and 38%, respectively. The corresponding sensitivity (50%), specificity (65%), NPV (76%), and PPV (33%) of EMG findings for new postoperative motor deficits were slightly lower than the MEP values. The combination of SSEPs, TcMEPs, and EMG findings provided an overall sensitivity of 91% with a specificity of 67%, a NPV of 91%, and a PPV of 67% for new postoperative sensorimotor deterioration. Particularly, in 10 of the 15 cases with pathological IONM findings, new or worsened transient or permanent sensorimotor deficits were found postoperatively, whereas only 1 of the 11 cases with nonpathological IONM findings was affected by a postoperatively deteriorated sensorimotor status. Statistically, pathological SSEP findings were significantly associated with more new or worsened transient or permanent sensory deficits postoperatively (p = 0.043, Fisher's exact test). In contrast, there was no statistically significant correlation between pathological TcMEPs or EMG findings and postoperative motor function deterioration. Taken together, patients with nonpathological IONM during tumor resection had significantly fewer new or worsened transient or permanent sensorimotor deficits after surgery (p = 0.005, Fisher's exact test) and were significantly more likely to have an improved immediate clinical outcome in terms of functional status as expressed by the change between pre- and postoperative McCormick grading (p = 0.046, r = 0.411, Spearman rank-order correlation). During resection of completely intramedullary tumors, significantly more pathological findings were detected on multimodal IONM than during resection of intramedullary-extramedullary or primarily extramedullary tumors (p = 0.021, Mann-Whitney rank-sum test). Additionally, pathological TcMEP findings were significantly more frequent during resection of ventral tumors than during removal of dorsal tumors (p = 0.035, Mann-Whitney rank-sum test), whereas there were no significant differences regarding pathological SSEP findings. There was no significant correlation between the frequency of pathological IONM findings and the vertebral level of the tumor or the surgical approach to the spinal cord for tumor resection.

Long-Term Outcome

According to the McCormick grade at the most recent follow-up, functional outcome had improved in 3 (17.6%) of 17 patients, remained stable in 12 (70.6%), and deteriorated in 2 (11.8%). Changes of only 1 grade occurred in all cases. Overall, the median McCormick grade at the long-term follow-up (mean 7.9 ± 4.0 years after surgery) was II (range I–IV), the same as the median grade preoperatively. At the latest follow-up examinations, most patients presented with an improvement in general clinical outcome according to Odom's criteria, with 7 patients (41.2%) having a good outcome, 8 (47.1%) having a fair outcome, and only 2 (11.8%) having deteriorated with a poor outcome. Questionnaire evaluation at the most recent follow-up interview revealed a high rate of satisfaction regarding surgical outcome, with 12 patients (70.6%) reporting a PSI score of 1 and 1 patient (5.9%) reporting a PSI score of 2. However, 1 patient with a PSI score of 3 and 3 patients with a score of 4 would not undergo surgery again. Long-term performance in everyday life was excellent in 12 patients (70.6%) with a BI of 100, indicating no disability. Furthermore, 15 patients (88.2%) showed a WHO/ECOG Performance Status grade ≤ 1, and 13 patients (76.5%) had a KPS score ≥ 80, indicating an ability to carry on normal activities and to work with no need of special care during the long-term follow-up. In line with these results, the mean ODI score on the long-term questionnaire was 11.4% ± 12.5% (range 0%–32%), showing only minimal disability. However, 3 patients (17.6%) reported moderate disability (BI 60–95) and 2 patients (11.8%) reported severe disability (BI < 60) in activities of daily living at the most recent examination. At the same time, 2 patients (11.8%) had a WHO/ECOG Performance Status Grade 4 and 1 patient (5.9%) had a KPS score < 50, indicating severe disability and the need for institutional or hospital care. According to the SF-36v2 Health Survey, the mean physical health composite score (PCS) on the long-term questionnaire evaluation was 49.1 ± 9.1 (range 30.3–61.7) and the mean mental health composite score (MCS) was 45.5 ± 10.9 (range 32.5–68.6), indicating slightly worse physical and mental health than the average population.

Surgical Complications

Cerebrospinal fluid leakage occurred in 1 patient and was successfully treated with lumbar drainage. Increased intraoperative blood loss requiring intra- and/or postoperative blood transfusion was seen in 2 patients (estimated intraoperative blood loss for each patient was approximately 2000 ml). An epidural abscess developed in 1 patient, requiring revision surgery and antibiotic therapy. Spinal instability was seen in 2 patients after tumor resection via a single-level cervical approach, with 1 of the patients requiring fusion surgery during follow-up. Altogether, the rate of surgical complications was 26.9%, with impairments remaining in 2 of the 6 affected patients (Table 7). In combination with the postoperative appearance of new or worsened permanent sensorimotor deficits in 3 patients, the total rate of lasting long-term impairments after surgery was 19.2%.

TABLE 7.

Surgical outcomes

OutcomeNo. of Cases (%)
Intraop/postop complications
  Extensive bleeding2 (7.7)
  Epidural abscess1 (3.8)
  CSF effusion1 (3.8)
  Brainstem venous thrombosis1 (3.8)
Revision surgery1 (3.8)
Transient sensorimotor changes (<3 mos)8 (30.8)
  Transient sensory changes8 (30.8)
  Transient motor deficits4 (15.4)
Permanent sensorimotor changes (>3 mos)3 (11.5)
  Permanent sensory changes3 (11.5)
  Permanent motor deficits2 (7.7)
Long-term spinal instability2 (7.7)
Fusion surgery during follow-up1 (3.8)

Risk Factors Affecting Long-Term Prognosis

Long-term functional outcome was significantly diminished in patients suffering from VHL disease (p = 0.044, Fisher's exact test; Table 8). All other investigated factors (patient sex, age at first clinical signs, duration of symptoms, age at first operation, presence of syrinx, ventral or complete intramedullary tumor location, and subtotal resection) were not significantly associated with long-term functional outcome according to logistic regression analyses (polytomous variables) and Fisher's exact test (dichotomous variables). Furthermore, there was a significant correlation between pathological IONM findings and a worse long-term BI (p = 0.011, r = 0.542, Spearman rank-order correlation) and ODI score (p = 0.024, r = 0.598, Spearman rank-order correlation), whereas pathological intraoperative changes in SSEPs were correlated with a diminished long-term ODI score (p = 0.025, r = 0.540, Spearman rank-order correlation).

TABLE 8.

Probability of factors affecting clinical outcomes

Factorp Value
Patient sex1.000
Age at 1st clinical signs0.996
Age at 1st op0.996
Duration of symptoms0.996
Presence of syrinx0.426
VHL0.044*
Ventral tumor1.000
Complete intramedullary tumor0.331
Subtotal resectionNA

NA = not applicable.

Categorized functional outcome according to McCormick score: 0 = improved or stable; 1 = deteriorated.

Discussion

Epidemiology, Tumor Location, and Clinical Findings

The clinical manifestation of spinal cord hemangioblastomas is known to peak within the 4th decade of life with a wide range of dynamics in clinical progression (2–204 months).7,20,22,28 A slight predominance in males has been reported.4,7,28 In our study, both patient age at presentation (mean 35.4 years) and duration of symptoms (range 1.1–85.2 months) were consistent with data reported in the literature, whereas the sex ratio of our population was balanced. Furthermore, in accordance with data indicating that 23%–38% of CNS hemangioblastomas occur in association with VHL disease,2,4,7,29 we found that 29.2% of our population met the criteria for VHL disease. Although hemangioblastomas can arise throughout the entire spinal cord, in our study they were predominantly localized in the cervical (77.8%) and thoracic (18.5%) spine (Fig. 1), findings comparable to data in prior studies.7,28 In line with published results,7,8,20,22,28 most tumors in our study were intramedullary and dorsal to the dentate ligament (92.6% of the cases) as well as accompanied by peritumoral edema and/or syringomyelia (81.5% of the cases). Clinically, preoperative sensory changes (100%), pain (66.7%), and spinal ataxia (66.7%) predominated, corresponding with the mostly dorsal location of tumors, whereas motor deficits (41.7%) and bladder/bowel complaints (12.5%) were less frequent. All clinical findings were comparable to those of previous studies.7,8,28,36

Surgical Procedures and Tumor Control

Surgical removal of spinal cord hemangioblastoma is considered to be the treatment of choice, while only sporadic attempts at stereotactic radiosurgery have been published.37 Given our experience, we recommend integrating 2 procedures into the surgical process to enhance procedural safety and efficacy: 1) coagulation and transection of feeding arteries before tumor resection and occlusion of the draining veins, and 2) en bloc removal after stepwise dissection and circumferential coagulation and shrinking because piecemeal resection carries a higher risk for extensive bleeding. Gross-total resection should be the goal as well since hemangioblastoma recurrence is almost certainly a consequence of subtotal resection;28 overall, a tumor recurrence rate of about 20% has been described after CNS hemangioblastoma resection, especially in younger patients and in cases of VHL disease.4,6 In our study, circumferential dissection as described anteriorly allowed complete tumor resection in 96.3% of the cases without local tumor recurrence during the mean followup of about 8 years, showing that complete tumor resection is durable and attainable in most cases. None of our patients underwent preoperative embolization, which is a matter of debate in the literature. Some authors emphasize embolization of feeding arteries for the reduction of tumor blood supply to facilitate tumor resection.2,20 However, Deng et al. underlined the complicated superselective catheterization needed for embolization of spinal cord hemangioblastomas and suggested that it is mostly unnecessary for complete tumor resection.7 In our series, the rate of gross-total resection was high despite omitting preoperative embolization, while intra- or postoperative blood transfusion due to increased intraoperative loss of blood was seen in only 2 patients; no severe cardiocirculatory event was observed. Considering the reported 3.1% overall complication rate during preoperative embolization of spinal tumors,11 we concluded that for most tumors a safe and effective resection can be conducted using microsurgical techniques without preoperative embolization. Nevertheless, we think that preoperative embolization should be taken into account in cases of large-volume tumors, especially if MRI indicates larger tumor vessels, suggesting high local perfusion.

Intraoperative Neurophysiological Monitoring and Clinical Outcome

In our series, patients with nonpathological IONM during tumor resection had significantly fewer new or worsened transient or permanent sensorimotor deficits after surgery.

Generally, IONM modalities that specifically assess the structures most at risk are chosen in spine surgery. In cervical and thoracic procedures the integrity of the spinal cord with its sensory and motor pathways is of the utmost importance, and the combined monitoring of SSEPs and MEPs provides a global assessment of spinal cord function. In lumbosacral procedures preservation of neurological function depends mainly on nerve root integrity, and EMG monitoring is the focus of IONM.10 In our study, most spinal cord hemangioblastomas were located at the cervical and thoracic levels. Accordingly, pathological IONM findings for SSEPs and TcMEPs were significantly associated with new or worsened transient or permanent sensorimotor deficits after surgery (p = 0.043 and p = 0.038, Fisher's exact test), whereas there was no significant correlation between pathological EMG findings and postoperative sensorimotor deterioration. Additionally, the corresponding sensitivity, specificity, NPV, and PPV of the EMG findings were lower than the SSEP and MEP values. However, the highest overall sensitivity was provided by the combination of SSEPs, TcMEPs, and EMG findings, underlining the importance of multimodal monitoring during resection of spinal cord hemangioblastoma. Furthermore, we also found that tumor location in relation to the spinal cord influenced IONM findings during surgery: during resection of completely intramedullary tumors, the frequency of pathological IONM findings was significantly greater than during resection of at least partly extramedullary tumors. Additionally, pathological TcMEP findings were significantly more frequent during resection of ventral tumors than resection of dorsal tumors. However, since both ventral and dorsal tumors were resected via a posterior approach, the dorsal columns of the spinal cord were at risk during microsurgical removal of all tumors. Accordingly, we recorded no significant difference in the frequency of pathological SSEP findings during resection of tumors, whether located more dorsally or ventrally.

We also proved that multimodal IONM during tumor resection is a strong surrogate marker for both short- and long-term postoperative outcomes. Pathological IONM findings during surgery implied new or worsened transient sensorimotor deficits in about 50% of the cases and permanent sensorimotor deficits in 20% of the cases, whereas none of the patients with nonpathological IONM results showed a permanent deficit. Moreover, patients with nonpathological IONM findings were significantly more likely to have a better short-term clinical course in terms of functional outcome according to the McCormick grading system, and this resulted in a slightly shorter median in-patient stay. Furthermore, our study is the first to show that IONM findings correlate with important parameters of general performance in everyday life and disability at the long-term follow-up evaluation. Pathological IONM findings were significantly associated with a diminished long-term status according to the BI, a widely used scoring system for assessing general performance in activities of daily living. Additionally, pathological IONM findings during tumor resection were significantly correlated with a worse long-term ODI score, underlining the prognostic potential of IONM for both immediate functional outcome and long-term overall outcome.

The amount of published data on IONM for the resection of intramedullary spinal cord tumors (IMSCTs) is small so far; therefore, the specific prognostic potential of SSEPs, MEPs, or EMG is mostly not determined. Although SSEP signals are generally believed to be good basic indicators of spinal cord function, MEPs are more significant in monitoring function of the corticospinal tract; congruously, changes in MEPs have appeared to be more sensitive in the detection of postoperative motor deficits.10,13 Hyun and Rhim14 showed that combined SSEP and MEP monitoring provides higher sensitivity, PPV, and NPV than single-modality techniques. Jin et al.15 emphasized the importance of the additional integration of EMG recording because of an observed association between EMG events and upcoming MEP changes during tumor removal, suggesting that the addition of EMG recordings can improve safety by acting as an early predictor of evoked potential changes. The current literature recommends multimodal IONM with the recording of SEPs and MEPs for global surveillance of spinal cord function during IMSCT surgery, even though the total number of investigated patients is still very limited.1,3,14,15 The most frequently assessed variables are sensitivity, specificity, NPV, and PPV of IONM for the immediate neurological outcome after surgery, with results similar to our findings in multimodal IONM.15 Studies of the prognostic significance of IONM findings, especially for long-term outcome, are scarce. In 2005, Quiñones-Hinojosa et al.35 published their results on correlating changes in IONM during IMSCT resection with postoperative motor function in the immediate and long-term follow-ups, showing a significant relation between reductions in the complexity and/or loss of the TcMEP waveform and motor grade loss up to 15 months postoperatively. In 2006, Sala et al.38 published a historical case control study focused on MEP monitoring in IMSCT, showing significant improvement in long-term motor outcome in the IONM group compared with a non-IONM group. Since only intraoperative MEP recordings were analyzed in the studies by Quiñones-Hinojosa et al. and Sala et al., ours is the first study to assess state-of-the-art multimodal IONM with TcMEPs, SSEPs, and EMG, providing a statistical correlation with postoperative sensorimotor and functional outcome as well as long-term general performance. For future studies, additional D-wave monitoring and dorsal column mapping procedures may offer the potential to further improve the accuracy of IONM for the preservation of dorsal column and motor tract integrity18,38 and decrease the morbidity associated with the surgical approach,27 especially in the resection of intramedullary and cervically located tumors.

Circumstances of Changes in IONM and Corrective Actions

The circumstances of critical changes in evoked potentials according to the criteria mentioned in Methods are diverse: 1) technical reasons such as dislocation of electrodes; 2) anesthesiological reasons such as lowering of blood pressure or body temperature, change in intravenous anesthesia management, or addition of volatile anesthetics;25 or 3) surgical reasons such as tumor preparation and resection including coagulation next to the tumor-parenchyma margin, traction to the tumor or parenchyma during dissection, irrigation with cold saline solution, or occlusion of feeding arteries or draining vessels. As a consequence, each critical change in evoked potentials was carefully considered within the context of the most recent anesthesiological and surgical steps. First, vital parameters—especially blood pressure and body temperature—were normalized and anesthesia management was reconsidered, especially the addition of volatile anesthetics, which was stopped. If critical changes in evoked potentials persisted, resection was halted and the surgical site was inspected. Further corrective actions included reducing traction on the tumor or surrounding parenchyma, repositioning the retractors, irrigating with warm saline solution, applying surgical cotton pads or a thrombin-coated collagen sponge for hemostasis instead of coagulation near feeding vessels or spinal cord parenchyma, applying absorbent cotton soaked with nimodipine in cases of visible vasospasm, continuing the resection at distant sites, or increasing blood pressure to establish improved perfusion.

Clinical Outcome

New or worsened sensorimotor deficits during the first days and weeks after surgery occurred after 42.3% of resections. However, these new sensorimotor deficits were transient and less marked in most cases (72.7%). As a consequence, the McCormick grade was maintained or improved in most patients (83.4%) during the early postoperative period, and the status of only a minority of patients (16.7%) deteriorated a median of 1 grade; similar results have been obtained in comparable studies.7,28 Additionally, the majority of patients (62.5%) had an improved immediate clinical outcome according to Odom's criteria.

Since most of the new postoperative sensorimotor deficits appeared to be transient (< 3 months), we concluded that patients with an intramedullary hemangioblastoma should be followed up in a long-term manner before the effects of resection can be entirely determined. A review of the literature reveals that our study is one of the largest on spinal cord hemangioblastomas and is among those with the longest follow-up period as well. Regarding long-term outcome, we found that the majority of patients were stable or improved in their McCormick functional grade and showed an improvement in clinical outcome according to Odom's criteria (88.2% and 94.1%, respectively, after a mean follow-up of almost 8 years); these rates are similar to those reported in the literature.2,7,8 Only the studies by Mehta et al.28 and Lunardi et al.23 had slightly longer mean follow-ups of up to 15 and 12 years, respectively, whereas their rates of long-term stabilization and/or improvement in McCormick functional grade were similar to our long-term results. Overall, in our study, the median McCormick grade at the long-term follow-up, as well as preoperatively, was Grade II (range I–IV), indicating that resection is effective in sustainably stabilizing neurological status over time. In combination with the limited rate of postoperative complications, the satisfying long-term functional outcome led to a high rate of subjective satisfaction regarding surgery (PSI score ≤ 2) in 76.5% of the patients with long-term follow-up.

Most studies on spinal cord hemangioblastoma resections have used only the McCormick classification system for follow-up evaluation. Only Sun et al.41 and Pavesi et al.34 have used the KPS to show that patients' general performance was satisfying, with about 80% of the patients having a KPS score ≥ 80. Note that long-term follow-up in both of these studies was shorter than ours at 4 and 3.2 years, respectively. Our study is the first in which important aspects of overall performance in activities of daily life, disability, quality of life, and satisfaction have been investigated after an average period of approximately 8 years by using various scoring systems such as the PSI, ODI, BI, and WHO/ECOG Performance Status as well as the SF-36v2 Health Survey, providing proof that resection is a powerful tool in obtaining a satisfying long-term outcome. Long-term evaluation revealed excellent performance in everyday life with more than three-quarters of the patients having a BI ≥ 95, WHO/ECOG Performance Status grade ≤ 1, and KPS score ≥ 80, while the mean long-term ODI score (11.4% ± 12.5%) indicated only minimal disability. By the end of the long-term follow-up, only 4 of 17 patients stated that they would not undergo surgery again for the same results.

When comparing our series of spinal cord hemangioblastomas to published series on IMSCTs, we found that a comparable high rate of patients (73%–91.3%) stays functionally stable or improves in McCormick grading during a long-term follow-up after resection.21,39,42,43 However, similar to published series of spinal cord hemangioblastoma resections, most studies of IMSCT resections solely analyzed functional outcome via McCormick grading, while additional aspects of overall patient performance in activities of daily life were rarely assessed. One of the exceptions is the study by Halvorsen et al.,12 in which the authors analyzed patient clinical course after the resection of intraspinal ependymomas, 65% of which were intramedullary. Seventy-five percent of the patients scored 0 or 1 on the ECOG scale, and 83% had minimal or moderate disability according to the ODI at a mean long-term follow-up of 82 months. These results are similar to our long-term results of spinal cord hemangioblastoma resections. Despite the massive vascularization and highly eloquent localization of intramedullary hemangioblastomas, the resection of these lesions seems to have a long-term prognosis similar to that following resection of less-vascularized IMSCTs.

Factors Affecting Prognosis

Predictors of clinical outcome are controversial. Some authors have identified tumor volume, ventral location, and association with peritumoral edema as risk factors for a poor surgical outcome,16,22,28 while others have found none of these correlations and claim that subtotal resection leads to a worse outcome than does gross-total resection.7,8 In long-term follow-up evaluations, Parker et al.33 showed that patients with VHL had a poorer functional outcome than a non-VHL group. Park et al.32 could not find any worse outcome in the VHL group. In our study, statistical assessment of suspected risk factors confirmed that VHL disease evolved as a significant risk factor negatively affecting long-term functional prognosis: 50% of the patients suffering from VHL disease showed a deterioration in McCormick grading, whereas all patients with sporadic spinal cord hemangioblastomas remained stable or improved in their McCormick grade as compared with their preoperative status. Furthermore, pathological IONM findings during resection were significantly correlated with a worse long-term status according to the BI score and ODI score, underlining the significance of IONM in resections. No significant correlation between outcome and the presence of a syrinx as well as tumor distribution, location, or relation to the spinal cord was seen. However, the impact of subtotal resection on outcome could not be statistically assessed since gross-total resection was achieved in all except one tumor.

Study Limitations

First, our study was performed in a retrospective manner with all the limitations inherent to that study design. Second, although we concluded that preoperative embolization is not necessary for safe and effective surgical treatment of most spinal hemangioblastomas, data are insufficient for statistical comparison because there was no control group undergoing preoperative embolization. Furthermore, even though our study of patients who underwent resection of spinal hemangioblastomas is one of the larger ones to date, the total number of investigated patients is still limited. In addition, most of the tumors were located dorsally (92.6%), were completely intramedullary (77.8%), and were located in the cervical spine (77.8%). Because of this imbalance in tumor distribution and the altogether modest patient number, the validity of our statistical correlation analysis between IONM findings and tumor anatomy (for example, location or relation within spinal cord) is limited, and potential effects may not have been statistically revealed.

Conclusions

Complete microsurgical resection is the treatment of choice for spinal cord hemangioblastomas. Our study, notwithstanding the limitations inherent to retrospective research, suggests that for most patients, gross-total tumor resection can be achieved safely and effectively via surgery under continuous IONM without preoperative embolization. Patients with nonpathological IONM findings during surgery have significantly fewer new transient and no permanent sensorimotor deficits postoperatively. Therefore, nonpathological IONM reassures the surgeon during tumor removal and is important for postoperative patient guidance. Following tumor resection, most patients have a satisfactory functional outcome and overall general performance on short- and long-term postoperative follow-up. However, pathological IONM findings are correlated with a worse immediate functional outcome and a worse long-term overall outcome according to the BI and ODI score. von Hippel-Lindau disease is a risk factor for a poorer long-term functional prognosis.

References

  • 1

    Ando M, Tamaki T, Yoshida M, Kawakami M, Kubota S, Nakagawa Y, et al. : Intraoperative spinal cord monitoring using combined motor and sensory evoked potentials recorded from the spinal cord during surgery for intramedullary spinal cord tumor. Clin Neurol Neurosurg 133:1823, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Boström A, Hans FJ, Reinacher PC, Krings T, Bürgel U, Gilsbach JM, et al. : Intramedullary hemangioblastomas: timing of surgery, microsurgical technique and follow-up in 23 patients. Eur Spine J 17:882886, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Cheng JS, Ivan ME, Stapleton CJ, Quinones-Hinojosa A, Gupta N, Auguste KI: Intraoperative changes in transcranial motor evoked potentials and somatosensory evoked potentials predicting outcome in children with intramedullary spinal cord tumors. J Neurosurg Pediatr 13:591599, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Conway JE, Chou D, Clatterbuck RE, Brem H, Long DM, Rigamonti D: Hemangioblastomas of the central nervous system in von Hippel-Lindau syndrome and sporadic disease. Neurosurgery 48:5563, 2001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Cristante L, Herrmann HD: Surgical management of intramedullary hemangioblastoma of the spinal cord. Acta Neurochir (Wien) 141:333340, 1999

  • 6

    de la Monte SM, Horowitz SA: Hemangioblastomas: clinical and histopathological factors correlated with recurrence. Neurosurgery 25:695698, 1989

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Deng X, Wang K, Wu L, Yang C, Yang T, Zhao L, et al. : Intraspinal hemangioblastomas: analysis of 92 cases in a single institution: clinical article. J Neurosurg Spine 21:260269, 2014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Dwarakanath S, Sharma BS, Mahapatra AK: Intraspinal hemangioblastoma: analysis of 22 cases. J Clin Neurosci 15:13661369, 2008

  • 9

    Fairbank JC, Couper J, Davies JB, O'Brien JP: The Oswestry Low Back Pain Disability Questionnaire. Physiotherapy 66:271273, 1980

  • 10

    Gonzalez AA, Jeyanandarajan D, Hansen C, Zada G, Hsieh PC: Intraoperative neurophysiological monitoring during spine surgery: a review. Neurosurg Focus 27:4 E6, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Griessenauer CJ, Salem M, Hendrix P, Foreman PM, Ogilvy CS, Thomas AJ: Preoperative embolization of spinal tumors: a systematic review and meta-analysis. World Neurosurg 87:362371, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Halvorsen CM, Kolstad F, Hald J, Johannesen TB, Krossnes BK, Langmoen IA, et al. : Long-term outcome after resection of intraspinal ependymomas: report of 86 consecutive cases. Neurosurgery 67:16221631, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Hilibrand AS, Schwartz DM, Sethuraman V, Vaccaro AR, Albert TJ: Comparison of transcranial electric motor and somatosensory evoked potential monitoring during cervical spine surgery. J Bone Joint Surg Am 86-A:12481253, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hyun SJ, Rhim SC: Combined motor and somatosensory evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in 17 consecutive procedures. Br J Neurosurg 23:393400, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Jin SH, Chung CK, Kim CH, Choi YD, Kwak G, Kim BE: Multimodal intraoperative monitoring during intramedullary spinal cord tumor surgery. Acta Neurochir (Wien) 157:21492155, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Kanno H, Yamamoto I, Nishikawa R, Matsutani M, Wakabayashi T, Yoshida J, et al. : Spinal cord hemangioblastomas in von Hippel-Lindau disease. Spinal Cord 47:447452, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Karnofsky DA, Burchenal JH, The clinical evaluation of chemotherapeutic agents in cancer MacLeod CM: Evaluation of Chemotherapeutic Agents New York, Columbia University Press, 1949

    • Search Google Scholar
    • Export Citation
  • 18

    Kothbauer KF, Deletis V, Epstein FJ: Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus 4:5 e1, 1998

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Langeloo DD, Lelivelt A, Louis Journée H, Slappendel R, de Kleuver M: Transcranial electrical motor-evoked potential monitoring during surgery for spinal deformity: a study of 145 patients. Spine (Phila Pa 1976) 28:10431050, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Lee DK, Choe WJ, Chung CK, Kim HJ: Spinal cord hemangioblastoma: surgical strategy and clinical outcome. J Neurooncol 61:2734, 2003

  • 21

    Lee SM, Cho YE, Kwon YM: Neurological outcome after surgical treatment of intramedullary spinal cord tumors. Korean J Spine 11:121126, 2014

  • 22

    Lonser RR, Weil RJ, Wanebo JE, DeVroom HL, Oldfield EH: Surgical management of spinal cord hemangioblastomas in patients with von Hippel-Lindau disease. J Neurosurg 98:106116, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Lunardi P, Cervoni L, Maleci A, Fortuna A: Isolated haemangioblastoma of spinal cord: report of 18 cases and a review of the literature. Acta Neurochir (Wien) 122:236239, 1993

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Mahoney FI, Barthel DW: Functional evaluation: the Barthel Index. Md State Med J 14:6165, 1965

  • 25

    Malcharek MJ, Loeffler S, Schiefer D, Manceur MA, Sablotzki A, Gille J, et al. : Transcranial motor evoked potentials during anesthesia with desflurane versus propofol—a prospective randomized trial. Clin Neurophysiol 126:18251832, 2015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    McCormick PC, Torres R, Post KD, Stein BM: Intramedullary ependymoma of the spinal cord. J Neurosurg 72:523532, 1990

  • 27

    Mehta AI, Mohrhaus CA, Husain AM, Karikari IO, Hughes B, Hodges T, et al. : Dorsal column mapping for intramedullary spinal cord tumor resection decreases dorsal column dysfunction. J Spinal Disord Tech 25:205209, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Mehta GU, Asthagiri AR, Bakhtian KD, Auh S, Oldfield EH, Lonser RR: Functional outcome after resection of spinal cord hemangioblastomas associated with von Hippel-Lindau disease. J Neurosurg Spine 12:233242, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Neumann HP, Eggert HR, Weigel K, Friedburg H, Wiestler OD, Schollmeyer P: Hemangioblastomas of the central nervous system. A 10-year study with special reference to von Hippel-Lindau syndrome. J Neurosurg 70:2430, 1989

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Odom GL, Finney W, Woodhall B: Cervical disk lesions. JAMA 166:2328, 1958

  • 31

    Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. : Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5:649655, 1982

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Park CH, Lee CH, Hyun SJ, Jahng TA, Kim HJ, Kim KJ: Surgical outcome of spinal cord hemangioblastomas. J Korean Neurosurg Soc 52:221227, 2012

  • 33

    Parker F, Aghakhani N, Ducati LG, Yacubian-Fernandes A, Silva MV, David P, et al. : Results of microsurgical treatment of medulla oblongata and spinal cord hemangioblastomas: a comparison of two distinct clinical patient groups. J Neurooncol 93:133137, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Pavesi G, Feletti A, Berlucchi S, Opocher G, Martella M, Murgia A, et al. : Neurosurgical treatment of von Hippel-Lindau-associated hemangioblastomas: benefits, risks and outcome. J Neurosurg Sci 52:2936, 2008

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Quiñones-Hinojosa A, Lyon R, Zada G, Lamborn KR, Gupta N, Parsa AT, et al. : Changes in transcranial motor evoked potentials during intramedullary spinal cord tumor resection correlate with postoperative motor function. Neurosurgery 56:982993, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Roonprapunt C, Silvera VM, Setton A, Freed D, Epstein FJ, Jallo GI: Surgical management of isolated hemangioblastomas of the spinal cord. Neurosurgery 49:321328, 2001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Ryu SI, Kim DH, Chang SD: Stereotactic radiosurgery for hemangiomas and ependymomas of the spinal cord. Neurosurg Focus 15:5 E10, 2003

  • 38

    Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, et al. : Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery 58:11291143, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Shrivastava RK, Epstein FJ, Perin NI, Post KD, Jallo GI: Intramedullary spinal cord tumors in patients older than 50 years of age: management and outcome analysis. J Neurosurg Spine 2:249255, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Slosar PJ, Reynolds JB, Schofferman J, Goldthwaite N, White AH, Keaney D: Patient satisfaction after circumferential fusion. Spine (Phila Pa 1976) 25:722726, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Sun , Özduman K, Usseli , Özgen S, Pamir MN: Sporadic spinal hemangioblastomas can be effectively treated by microsurgery alone. World Neurosurg 82:836847, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Xiao R, Miller JA, Abdullah KG, Lubelski D, Mroz TE, Benzel EC: Quality of life outcomes following resection of adult intramedullary spinal cord tumors. Neurosurgery 78:821828, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Yang S, Yang X, Hong G: Surgical treatment of one hundred seventy-four intramedullary spinal cord tumors. Spine (Phila Pa 1976) 34:27052710, 2009

Disclosures

Dr. Tonn has received support from BrainLab for non–study-related clinical or research effort.

Author Contributions

Conception and design: Siller, Zausinger. Acquisition of data: Siller, Herlitz. Analysis and interpretation of data: Siller, Szelényi. Drafting the article: Siller. Critically revising the article: Siller, Szelényi, Tonn, Zausinger. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Siller. Statistical analysis: Siller. Administrative/technical/material support: Siller. Study supervision: Siller, Zausinger.

Supplemental Information

Previous Presentations

Parts of this paper have been presented orally at the Annual Spine Section Meeting of the German Society of Neurosurgery held in Berlin on October 3, 2015, and at the 10th Annual Meeting of the German Spine Society held in Frankfurt on December 12, 2015.

Contributor Notes

INCLUDE WHEN CITING Published online December 16, 2016; DOI: 10.3171/2016.8.SPINE16595.

Correspondence Sebastian Siller, Neurosurgical Clinic, Clinic of the University of Munich (LMU), Campus Grosshadern, Marchioninistrasse 15, Munich 81377, Germany. email: sebastian.siller@med.uni-muenchen.de.
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    Schematic demonstrating the distribution of spinal cord hemangioblastomas in this study. White and black circles and x's represent the 27 resected tumors and illustrate the vertebral level and relation to the dentate ligament. Adapted from Mehta et al: J Neurosurg Spine 72:233–242, 2010. Published with permission.

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    Preoperative sagittal T2-weighted (A) and contrast-enhanced T1-weighted (B) MR images showing a hemangioblastoma at C7–T1 with associated syrinx and spinal cord edema. Postoperative sagittal T2-weighted (C) and contrast-enhanced T1-weighted (D) MR images obtained after complete tumor resection.

  • 1

    Ando M, Tamaki T, Yoshida M, Kawakami M, Kubota S, Nakagawa Y, et al. : Intraoperative spinal cord monitoring using combined motor and sensory evoked potentials recorded from the spinal cord during surgery for intramedullary spinal cord tumor. Clin Neurol Neurosurg 133:1823, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Boström A, Hans FJ, Reinacher PC, Krings T, Bürgel U, Gilsbach JM, et al. : Intramedullary hemangioblastomas: timing of surgery, microsurgical technique and follow-up in 23 patients. Eur Spine J 17:882886, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Cheng JS, Ivan ME, Stapleton CJ, Quinones-Hinojosa A, Gupta N, Auguste KI: Intraoperative changes in transcranial motor evoked potentials and somatosensory evoked potentials predicting outcome in children with intramedullary spinal cord tumors. J Neurosurg Pediatr 13:591599, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Conway JE, Chou D, Clatterbuck RE, Brem H, Long DM, Rigamonti D: Hemangioblastomas of the central nervous system in von Hippel-Lindau syndrome and sporadic disease. Neurosurgery 48:5563, 2001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Cristante L, Herrmann HD: Surgical management of intramedullary hemangioblastoma of the spinal cord. Acta Neurochir (Wien) 141:333340, 1999

  • 6

    de la Monte SM, Horowitz SA: Hemangioblastomas: clinical and histopathological factors correlated with recurrence. Neurosurgery 25:695698, 1989

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Deng X, Wang K, Wu L, Yang C, Yang T, Zhao L, et al. : Intraspinal hemangioblastomas: analysis of 92 cases in a single institution: clinical article. J Neurosurg Spine 21:260269, 2014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Dwarakanath S, Sharma BS, Mahapatra AK: Intraspinal hemangioblastoma: analysis of 22 cases. J Clin Neurosci 15:13661369, 2008

  • 9

    Fairbank JC, Couper J, Davies JB, O'Brien JP: The Oswestry Low Back Pain Disability Questionnaire. Physiotherapy 66:271273, 1980

  • 10

    Gonzalez AA, Jeyanandarajan D, Hansen C, Zada G, Hsieh PC: Intraoperative neurophysiological monitoring during spine surgery: a review. Neurosurg Focus 27:4 E6, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Griessenauer CJ, Salem M, Hendrix P, Foreman PM, Ogilvy CS, Thomas AJ: Preoperative embolization of spinal tumors: a systematic review and meta-analysis. World Neurosurg 87:362371, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Halvorsen CM, Kolstad F, Hald J, Johannesen TB, Krossnes BK, Langmoen IA, et al. : Long-term outcome after resection of intraspinal ependymomas: report of 86 consecutive cases. Neurosurgery 67:16221631, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Hilibrand AS, Schwartz DM, Sethuraman V, Vaccaro AR, Albert TJ: Comparison of transcranial electric motor and somatosensory evoked potential monitoring during cervical spine surgery. J Bone Joint Surg Am 86-A:12481253, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hyun SJ, Rhim SC: Combined motor and somatosensory evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in 17 consecutive procedures. Br J Neurosurg 23:393400, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Jin SH, Chung CK, Kim CH, Choi YD, Kwak G, Kim BE: Multimodal intraoperative monitoring during intramedullary spinal cord tumor surgery. Acta Neurochir (Wien) 157:21492155, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Kanno H, Yamamoto I, Nishikawa R, Matsutani M, Wakabayashi T, Yoshida J, et al. : Spinal cord hemangioblastomas in von Hippel-Lindau disease. Spinal Cord 47:447452, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Karnofsky DA, Burchenal JH, The clinical evaluation of chemotherapeutic agents in cancer MacLeod CM: Evaluation of Chemotherapeutic Agents New York, Columbia University Press, 1949

    • Search Google Scholar
    • Export Citation
  • 18

    Kothbauer KF, Deletis V, Epstein FJ: Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus 4:5 e1, 1998

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Langeloo DD, Lelivelt A, Louis Journée H, Slappendel R, de Kleuver M: Transcranial electrical motor-evoked potential monitoring during surgery for spinal deformity: a study of 145 patients. Spine (Phila Pa 1976) 28:10431050, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Lee DK, Choe WJ, Chung CK, Kim HJ: Spinal cord hemangioblastoma: surgical strategy and clinical outcome. J Neurooncol 61:2734, 2003

  • 21

    Lee SM, Cho YE, Kwon YM: Neurological outcome after surgical treatment of intramedullary spinal cord tumors. Korean J Spine 11:121126, 2014

  • 22

    Lonser RR, Weil RJ, Wanebo JE, DeVroom HL, Oldfield EH: Surgical management of spinal cord hemangioblastomas in patients with von Hippel-Lindau disease. J Neurosurg 98:106116, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Lunardi P, Cervoni L, Maleci A, Fortuna A: Isolated haemangioblastoma of spinal cord: report of 18 cases and a review of the literature. Acta Neurochir (Wien) 122:236239, 1993

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Mahoney FI, Barthel DW: Functional evaluation: the Barthel Index. Md State Med J 14:6165, 1965

  • 25

    Malcharek MJ, Loeffler S, Schiefer D, Manceur MA, Sablotzki A, Gille J, et al. : Transcranial motor evoked potentials during anesthesia with desflurane versus propofol—a prospective randomized trial. Clin Neurophysiol 126:18251832, 2015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    McCormick PC, Torres R, Post KD, Stein BM: Intramedullary ependymoma of the spinal cord. J Neurosurg 72:523532, 1990

  • 27

    Mehta AI, Mohrhaus CA, Husain AM, Karikari IO, Hughes B, Hodges T, et al. : Dorsal column mapping for intramedullary spinal cord tumor resection decreases dorsal column dysfunction. J Spinal Disord Tech 25:205209, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Mehta GU, Asthagiri AR, Bakhtian KD, Auh S, Oldfield EH, Lonser RR: Functional outcome after resection of spinal cord hemangioblastomas associated with von Hippel-Lindau disease. J Neurosurg Spine 12:233242, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Neumann HP, Eggert HR, Weigel K, Friedburg H, Wiestler OD, Schollmeyer P: Hemangioblastomas of the central nervous system. A 10-year study with special reference to von Hippel-Lindau syndrome. J Neurosurg 70:2430, 1989

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Odom GL, Finney W, Woodhall B: Cervical disk lesions. JAMA 166:2328, 1958

  • 31

    Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. : Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5:649655, 1982

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Park CH, Lee CH, Hyun SJ, Jahng TA, Kim HJ, Kim KJ: Surgical outcome of spinal cord hemangioblastomas. J Korean Neurosurg Soc 52:221227, 2012

  • 33

    Parker F, Aghakhani N, Ducati LG, Yacubian-Fernandes A, Silva MV, David P, et al. : Results of microsurgical treatment of medulla oblongata and spinal cord hemangioblastomas: a comparison of two distinct clinical patient groups. J Neurooncol 93:133137, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Pavesi G, Feletti A, Berlucchi S, Opocher G, Martella M, Murgia A, et al. : Neurosurgical treatment of von Hippel-Lindau-associated hemangioblastomas: benefits, risks and outcome. J Neurosurg Sci 52:2936, 2008

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Quiñones-Hinojosa A, Lyon R, Zada G, Lamborn KR, Gupta N, Parsa AT, et al. : Changes in transcranial motor evoked potentials during intramedullary spinal cord tumor resection correlate with postoperative motor function. Neurosurgery 56:982993, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Roonprapunt C, Silvera VM, Setton A, Freed D, Epstein FJ, Jallo GI: Surgical management of isolated hemangioblastomas of the spinal cord. Neurosurgery 49:321328, 2001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Ryu SI, Kim DH, Chang SD: Stereotactic radiosurgery for hemangiomas and ependymomas of the spinal cord. Neurosurg Focus 15:5 E10, 2003

  • 38

    Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, et al. : Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery 58:11291143, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Shrivastava RK, Epstein FJ, Perin NI, Post KD, Jallo GI: Intramedullary spinal cord tumors in patients older than 50 years of age: management and outcome analysis. J Neurosurg Spine 2:249255, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Slosar PJ, Reynolds JB, Schofferman J, Goldthwaite N, White AH, Keaney D: Patient satisfaction after circumferential fusion. Spine (Phila Pa 1976) 25:722726, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Sun , Özduman K, Usseli , Özgen S, Pamir MN: Sporadic spinal hemangioblastomas can be effectively treated by microsurgery alone. World Neurosurg 82:836847, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Xiao R, Miller JA, Abdullah KG, Lubelski D, Mroz TE, Benzel EC: Quality of life outcomes following resection of adult intramedullary spinal cord tumors. Neurosurgery 78:821828, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Yang S, Yang X, Hong G: Surgical treatment of one hundred seventy-four intramedullary spinal cord tumors. Spine (Phila Pa 1976) 34:27052710, 2009

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