Neurological outcomes and surgical complications in 221 spinal nerve sheath tumors

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OBJECTIVE

Among all primary spinal neoplasms, approximately two-thirds are intradural extramedullary lesions; nerve sheath tumors, mainly neurofibromas and schwannomas, comprise approximately half of them. Given the rarity of these lesions, reports of surgical complications are limited. The aim of this study was to identify the rates of new or worsening neurological deficits and surgical complications associated with the resection of spinal nerve sheath tumors and the potential factors related to these outcomes.

METHODS

Patients were identified through a search of an institutional neuropathology database and a separate review of current procedural terminology (CPT) codes. Age, sex, clinical presentation, presence of neurofibromatosis (NF), tumor type, tumor location, extent of resection characterized as gross total or subtotal, use of intraoperative neuromonitoring, surgical complications, presence of neurological deficit, and clinical follow-up were recorded.

RESULTS

Two hundred twenty-one tumors in 199 patients with a mean age of 45 years were identified. Fifty-three tumors were neurofibromas; 163, schwannomas; and 5, malignant peripheral nerve sheath tumors (MPNSTs). There were 70 complications in 221 cases, a rate of 32%, which included 34 new or worsening sensory symptoms (15%), 12 new or worsening motor deficits (5%), 10 CSF leaks or pseudomeningoceles (4%), 11 wound infections (5%), 5 cases of spinal deformity (2%), and 6 others (2 spinal epidural hematomas, 1 nonoperative cranial subdural hematoma, 1 deep venous thrombosis, 1 case of urinary retention, and 1 recurrent laryngeal nerve injury). Complications were more common in cervical (36%) and lumbosacral (38%) tumors than in thoracic (18%) lesions (p = 0.021). Intradural and dumbbell lesions were associated with higher rates of CSF leakage, pseudomeningocele, and wound infection. Complications were present in 18 neurofibromas (34%), 50 schwannomas (31%), and 2 MPNSTs (40%); the differences in frequency were not significant (p = 0.834). Higher complication rates were observed in patients with NF than in patients without (38% vs 30%, p = 0.189), although rates were higher in NF Type 2 than in Type 1 (64% vs 31%). There was no difference in the use of intraoperative neuromonitoring when comparing cases with surgical complications and those without (67% vs 69%, p = 0.797). However, the use of neuromonitoring was associated with a significantly higher rate of gross-total resection (79% vs 66%, p = 0.022).

CONCLUSIONS

Resection is a safe and effective treatment for spinal nerve sheath tumors. Approximately 30% of patients developed a postoperative complication, most commonly new or worsening sensory deficits. This rate probably represents an inevitable complication of nerve sheath tumor surgery given the intimacy of these lesions with functional neural elements.

ABBREVIATIONSDVT = deep venous thrombosis; EMG = electromyography; GTR = gross-total resection; MEP = motor evoked potential; MPNST = malignant PNST; NF1, NF2 = neurofibromatosis Type 1, Type 2; PNST = peripheral nerve sheath tumor; SSEP = somatosensory evoked potential; STR = subtotal resection.

OBJECTIVE

Among all primary spinal neoplasms, approximately two-thirds are intradural extramedullary lesions; nerve sheath tumors, mainly neurofibromas and schwannomas, comprise approximately half of them. Given the rarity of these lesions, reports of surgical complications are limited. The aim of this study was to identify the rates of new or worsening neurological deficits and surgical complications associated with the resection of spinal nerve sheath tumors and the potential factors related to these outcomes.

METHODS

Patients were identified through a search of an institutional neuropathology database and a separate review of current procedural terminology (CPT) codes. Age, sex, clinical presentation, presence of neurofibromatosis (NF), tumor type, tumor location, extent of resection characterized as gross total or subtotal, use of intraoperative neuromonitoring, surgical complications, presence of neurological deficit, and clinical follow-up were recorded.

RESULTS

Two hundred twenty-one tumors in 199 patients with a mean age of 45 years were identified. Fifty-three tumors were neurofibromas; 163, schwannomas; and 5, malignant peripheral nerve sheath tumors (MPNSTs). There were 70 complications in 221 cases, a rate of 32%, which included 34 new or worsening sensory symptoms (15%), 12 new or worsening motor deficits (5%), 10 CSF leaks or pseudomeningoceles (4%), 11 wound infections (5%), 5 cases of spinal deformity (2%), and 6 others (2 spinal epidural hematomas, 1 nonoperative cranial subdural hematoma, 1 deep venous thrombosis, 1 case of urinary retention, and 1 recurrent laryngeal nerve injury). Complications were more common in cervical (36%) and lumbosacral (38%) tumors than in thoracic (18%) lesions (p = 0.021). Intradural and dumbbell lesions were associated with higher rates of CSF leakage, pseudomeningocele, and wound infection. Complications were present in 18 neurofibromas (34%), 50 schwannomas (31%), and 2 MPNSTs (40%); the differences in frequency were not significant (p = 0.834). Higher complication rates were observed in patients with NF than in patients without (38% vs 30%, p = 0.189), although rates were higher in NF Type 2 than in Type 1 (64% vs 31%). There was no difference in the use of intraoperative neuromonitoring when comparing cases with surgical complications and those without (67% vs 69%, p = 0.797). However, the use of neuromonitoring was associated with a significantly higher rate of gross-total resection (79% vs 66%, p = 0.022).

CONCLUSIONS

Resection is a safe and effective treatment for spinal nerve sheath tumors. Approximately 30% of patients developed a postoperative complication, most commonly new or worsening sensory deficits. This rate probably represents an inevitable complication of nerve sheath tumor surgery given the intimacy of these lesions with functional neural elements.

Primary spinal column tumors arising from the neural elements are relatively rare lesions representing approximately 5% of adult primary central nervous system tumors.2,7,10 They can occur in a variety of anatomical locations including intramedullary, intradural extramedullary, dumbbell (intradural, both intraspinal and extraspinal), and extradural. Intramedullary tumors are primarily glial (ependymomas and astrocytomas), while extradural lesions consist of metastases, hematopoietic tumors, and primary bony tumors. Intradural extramedullary spinal cord tumors consist primarily of peripheral nerve sheath tumors (PNSTs) and meningiomas.16 Other entities include lipomas, spinal nerve sheath myxomas, paragangliomas, sarcomas, and vascular tumors.1

Spinal neurofibromas are found in up to 38% of patients with neurofibromatosis Type 1 (NF1),9,19,26,27 one of the most common autosomal dominant disorders, affecting 1 in 3500 individuals, with significant heterogeneity in its clinical manifestation.30 Spinal neurofibromas reportedly cause symptoms in approximately 5% of these patients; however, this estimate is probably too low.12,27,29 Familial spinal neurofibromatosis is an alternate form of neurofibromatosis that is categorized by multiple neurofibromas symmetrically affecting the entire axial spine.5,20,28 Spinal schwannomas are relatively rare with an incidence of 0.3–0.4 cases per 100,000 persons per year, and patients with these tumors generally present in the 4th or 5th decades of life.24 An estimated 90% of schwannomas are sporadic and solitary lesions, 4% arise in the setting of NF Type 2 (NF2), and another 5% occur in multiples but are unassociated with NF2.4 Neurofibromatosis Type 2 has an estimated incidence of 1 case in 25,000–40,000 persons and has the hallmark imaging finding of bilateral vestibular schwannomas.17 A newer diagnosis of schwannomatosis has been described and by definition includes the phenotypic hallmark of multiple schwannomas without the involvement of cranial nerve VIII. Its prevalence is unknown, but its reported incidence ranges from 1 case in 40,000–700,000 persons, with most authors suggesting an incidence similar to that of NF2.17 Malignant PNSTs have a worse prognosis than neurofibromas and schwannomas with an incidence of 1 case in 10,000 persons, but they are more common in patients with NF1, where over half of these tumors are found.25

Spinal nerve sheath tumors are rare entities, and published studies are limited to single-institution case series.3,6,8,11,14,22–24 Studies focusing purely on surgical complications are limited. Among the studies in which surgical complications are defined as events such as wound infections, CSF leaks, deep venous thrombosis (DVT), or pulmonary complications, those by Fernandes et al.11 and Seppälä et al.23 cite rates of around 10%, whereas Nanda et al.18 cite rates up to 30%; however, this latter study includes recurrence as a type of complication. When examining neurological outcomes such as new or worsening motor and sensory deficits, rates range from 5% to 30%.6,14,15,22–24 The goal of the present study was to identify the rates of new or worsening neurological deficits and surgical complications associated with the resection of spinal nerve sheath tumors treated at our institution and the potential factors related to these outcomes.

Methods

The Committee on Human Research, our institutional review board, approved all research activities.

Data Collection

Two authors (N.M.B. and C.P.A.) identified patients through a search of our institutional neuropathology database and a separate review of current procedural terminology (CPT) codes. These databases included 25 years of patient records (1991–present); however, most identified patients had been treated over the past decade (2006–2016). In total, 5 surgeons contributed cases to this series: N.M.B, D.C., P.V.M., P.R.W., and C.P.A. Pathology records were reviewed to include the following PNSTs: neurofibromas, schwannomas, and malignant PNSTs (MPNSTs). Medical records were reviewed to include patient age at surgery and patient sex, presence of NF1 or NF2 according to clinical criteria, presenting symptoms and their duration, tumor location, tumor size (defined by spinal levels spanned by the tumor and its maximum diameter [cm] on MRI when available), extent of resection (defined by postoperative MRI or operative report), use of spinal fusion and number of levels fused, time to last follow-up, follow-up imaging, date of recurrence, and fusion-related complications. With respect to schwannomatosis, since it represents a new diagnostic entity, it is unknown how many patients included in the present study actually had this diagnosis compared with a diagnosis of sporadic schwannomas. Tumor location was classified by the level of the involved nerve root (cervical, thoracic, or lumbosacral) and anatomical location was classified as intradural, extradural, dumbbell, or paraspinal (tumors originating beyond the neural foramen). Extent of resection was defined as gross total if there was no evidence of residual disease on postoperative MRI and as subtotal if residual tumor was present. The use of intraoperative neuromonitoring was recorded and categorized as somatosensory evoked potentials (SSEPs), motor evoked potentials (MEPs), electromyography (EMG), or evoked EMG. Fusion-related complications were identified through postoperative progress notes, outpatient clinic notes, and postoperative imaging studies including conventional radiographs and CT scans. Complications were classified as follows: new or worsening sensory symptoms (numbness, paresthesias, dysesthesias), new or worsening weakness, wound infection, CSF leak or pseudomeningocele, spinal deformity (defined as any new symptomatic deformity requiring surgical correction), or other.

Statistical Analysis

Univariate analysis of continuous variables was performed using the Student t-test, and categorical variables were compared using the chi-square or Fisher's exact test. Statistical significance was defined as p < 0.05. All analyses were performed with SPSS version 22 (IBM Corp.).

Results

Patient Demographics

A total of 221 tumors in 199 patients were identified. Mean patient age at the time of surgery was 45 years with a range of 1–88 years. Demographics are summarized in Table 1. There was a slight male predominance with 123 tumors (56%) in men and 98 tumors (44%) in women. A clinical diagnosis of NF1 was present in 42 cases (19%), NF2 in 11 cases (5%), and absent in 168 cases (76%). The mean duration of symptoms was 16 months, with pain as the most common presenting symptom (76%), followed by weakness (36%) and sensory changes (34%). There were 163 schwannomas (74%), 53 neurofibromas (24%), and 5 MPNSTs (2%). Tumors were distributed as follows: 85 cervical (38%), 62 thoracic (28%), and 74 lumbosacral (33%). Location was intradural in 130 cases (59%), extradural in 26 cases (12%), dumbbell in 52 cases (24%), and paraspinal in 13 cases (6%). The majority of lesions (75%) were treated with gross-total resection (GTR). The mean followup time was 32 months.

TABLE 1

Summary of patient demographics and tumor characteristics among 221 cases of PNST

CharacteristicValue
Age at surgery in yrs
  Mean45
  Median46
  Range1–88
No. of cases
  Male123 (56%)
  Female98 (44%)
Cases of NF
  Type 142 (19%)
  Type 211 (5%)
  None168 (76%)
Symptom duration in mos
  Mean16
  Median6
  Range0–120
Clinical presentation
  Spinal pain168 (76%)
  Weakness79 (36%)
  Sensory symptoms76 (34%)
  Gait disturbance12 (5%)
  Bowel/bladder incontinence12 (5%)
  Incidental finding4 (2%)
Tumor type
  Neurofibroma53 (24%)
  Schwannoma163 (74%)
  MPNST5 (2%)
Tumor level
  Cervical85 (38%)
  Thoracic62 (28%)
  Lumbosacral74 (33%)
Tumor location
  Intradural130 (59%)
  Extradural26 (12%)
  Dumbbell52 (24%)
  Paraspinal13 (6%)
Extent of resection
  GTR166 (75%)
  STR54 (24%)
  Biopsy1 (0.4%)
  Surgical complications70 (32%)
Follow-up in mos
  Mean32
  Median16
  Range0–162

Surgical Complications

There were 70 complications among the 221 tumors for a rate of 32%. The demographics of patients with and without complications are reviewed in Table 2. There was no significant difference in age, sex, or presenting symptoms among patients who developed complications. Neurofibromatosis Type 2 was more common among patients with complications (10% vs 2%, p = 0.039), while NF1 was not (19% vs 19%, p = 0.911). Cervical and lumbosacral tumors had higher rates of complications (36% and 38%, respectively) than thoracic lesions (18%, p = 0.021). Complication rates among tumor locations were as follows: intradural (34 [26%] of 130), extradural (8 [31%] of 26), dumbbell (25 [48%] of 52), and paraspinal (3 [23%] of 13), a difference that was statistically significant (p = 0.033). Tumor pathology was not associated with complication rates; however, neurofibromas were associated with a lower rate of GTR. Complications were more common in the subtotal resection (STR) group than in the GTR group (44% vs 28%), although the difference between the 2 groups was not significant (p = 0.022). Neither the number of vertebral levels spanned by the tumor (1.2 vs 1.2 levels) nor the maximum tumor diameter (3.3 vs 3.8 cm) was associated with complication rates.

TABLE 2

Summary of characteristics in PNST cases with or without surgical complications

CharacteristicSurgical ComplicationsNo Complicationsp Value
No. of cases70 (32%)151 (68%)
Patient age in yrs
  Mean42460.131
  Range5–881–79
Sex of cases
  Male44 (63%)79 (52%)0.142
  Female26 (37%)72 (48%)
Cases of NF
  Type 113 (19%)29 (19%)0.911
  Type 27 (10%)4 (3%)0.039*
  None50 (71%)118 (78%)0.277
Spinal location
  Cervical31 (44%)54 (36%)0.226
  Thoracic11 (16%)51 (34%)0.005
  Lumbosacral28 (40%)46 (30%)0.162
Vertebral levels spanned by tumor1.21.20.993
Max tumor diameter in cm3.33.80.346
Tumor location
  Intradural34 (48%)96 (64%)0.035
  Extradural8 (11%)18 (12%)0.916
  Dumbbell25 (36%)27 (18%)0.004
  Paraspinal3 (4%)10 (7%)0.759*
Tumor pathology
  Neurofibroma18 (26%)35 (23%)0.681
  Schwannoma50 (71%)113 (75%)0.592
  MPNST2 (3%)3 (2%)0.653*
Intraop neuromonitoring
  Any modality47 (67%)104 (69%)0.797
  MEP45 (64%)96 (64%)0.919
  SSEP45 (64%)99 (66%)0.853
  EMG45 (64%)104 (69%)0.498
  Evoked EMG4 (6%)13 (9%)0.452
Extent of resection
  GTR46 (66%)120 (79%)0.028
  STR24 (34%)30 (20%)0.020
  Biopsy0 (0%)1 (1%)1.000*
Follow-up in mos
  Mean32310.835
  Range0–1600–163

Fisher's exact test.

Intraoperative neuromonitoring was used in 47 (67%) of the 70 cases with postoperative complications compared with 104 (69%) of 151 cases without complications (p = 0.797). Among the 46 patients with any new or worsening motor or sensory symptom, intraoperative neuromonitoring was used in 35 cases (76%), compared with 116 (66%) of 175 cases without new neurological symptoms (p = 0.204). Among the 34 patients with new or worsening sensory symptoms, intraoperative neuromonitoring was used in 27 cases (79%); among the 12 patients with new or worsening motor deficits, neuromonitoring was used in 8 cases (67%). It was not feasible, and is beyond the scope of this paper, to determine whether neuromonitoring prevented postoperative deficits when it was used, because of changes in technique. Microsurgical technique was used in all cases. Surgical adjuncts such as ultrasonic aspirator and laser were used as indicated with no documented impact on individual complications.

Among the 70 complications, the most common were 34 new or worsening sensory symptoms (15%). Other complications included new or worsening weakness in 12 cases (5%), CSF leak or pseudomeningocele in 10 cases (4%), wound infection (including superficial and deep) in 11 cases (5%), and spinal deformity requiring surgical intervention in 5 cases (2%). Among the 12 cases of new or worsening weakness, 6 were new deficits and 6 represented a worsening of prior symptoms. Six cases involved planned nerve root sacrifice with expected postoperative deficits. Ten of the 12 cases involved weakness in a nerve root distribution, and 6 of those resulted in only mild deficits without any reported physical impairment. Two patients developed worsening bilateral lower-extremity weakness after surgery. One case occurred in a patient with multiple schwannomas from T-12 to L-3 who had presented with lower-extremity weakness and underwent tumor debulking for spinal cord compression. The second case was a patient with a large cervical schwannoma and intramedullary hemorrhage who had presented with weakness and myelopathy and underwent debulking for alleviation of spinal cord compression. Among the 10 CSF leaks or pseudomeningoceles, 8 were symptomatic with 5 of those requiring surgical repair; 2 cases were asymptomatic but nonetheless required surgical repair. Less common complications included 2 spinal epidural hematomas requiring a return to the operating room, 1 nonoperative cranial subdural hematoma, 1 DVT, 1 case of urinary retention, and 1 recurrent laryngeal nerve injury. Complications are summarized in Table 3.

TABLE 3

Summary of surgical complications among 221 cases of PNST

ComplicationNo. (%)
New/worsening sensory symptom34 (15)
New/worsening weakness12 (5)
CSF leak/pseudomeningocele10 (4)
Wound infection11 (5)
Spinal deformity5 (2)
Other6 (3)

Among the 221 tumors, only 5 cases were associated with new spinal deformity. Four of these cases occurred in pediatric patients with NF1 who underwent multilevel cervical laminectomies for resection of neurofibromas without associated fusion procedures. Kyphotic deformities developed in each case, requiring return to the operating room for spinal fusion. One patient who underwent a spinal fusion with initial tumor resection developed a new spinal deformity. He had initially presented with a giant extradural schwannoma with paraspinal extension causing vena cava compression. He underwent L3–4 laminectomies with an L-3 pedicle subtraction osteotomy and L2–S1 instrumented posterior spinal fusion with pelvic fixation, followed by L2–4 anterior spinal fusion with partial L-3 corpectomy and interbody cage placement. He presented 2 years later with worsening back pain and right lower-extremity weakness. Imaging revealed proximal junctional kyphosis at L1–2 with an associated disc herniation causing severe canal stenosis. He underwent L1–2 laminectomies with discectomy and extension of his posterior instrumented fusion to T-10. At the last follow-up 53 months from his initial surgery, the patient was doing well with normal neurological function.

Tumor Pathology and Complications

Complications among the different tumor pathologies were compared (Table 4). Among 53 neurofibromas, there were 18 complications (34%) compared with 50 complications among 163 schwannomas (31%) and 2 complications among 5 MPNSTs (40%), differences that were not significant (p = 0.834). The rate of new or worsening sensory symptoms (21%) and motor deficits (8%) was slightly higher among neurofibromas than schwannomas (13% and 5%, respectively) or MPNSTs (20% and 0%, respectively); however, these differences were not significant (p = 0.427 and 0.658, respectively). Cerebrospinal fluid leaks or pseudomeningoceles (6%) and wound infections (7%) were more common among schwannomas than neurofibromas (2% and 0%, respectively) or MPNSTs (0% and 0%, respectively); again, however, these differences were not significant (p = 0.408 and 0.128, respectively). There was a higher rate of spinal deformity in the neurofibroma group (8%) than in the schwannoma (0.1%) or MPNST (0%) groups, and this difference was significant (p = 0.012).

TABLE 4

Summary of characteristics among 221 PNST cases, according to tumor type

CharacteristicNeurofibromaSchwannomaMPNSTp Value
No. of tumors531635
Mean patient age in yrs364842<0.001
NF
  Type 139 (74%)2 (1%)1 (20%)<0.001
  Type 21 (2%)10 (6%)0 (0%)0.408
  None13 (24%)151 (93%)4 (80%)<0.001
Location
  Cervical39 (74%)44 (27%)2 (40%)<0.001
  Thoracic7 (13%)55 (34%)0 (0%)0.006
  Lumbosacral7 (13%)64 (39%)3 (60%)0.001
Dural location
  Intradural27 (51%)102 (62%)1 (20%)0.067
  Extradural6 (11%)20 (12%)0 (0%)0.699
  Dumbbell15 (28%)33 (20%)4 (80%)0.005
  Paraspinal5 (9%)8 (5%)0 (0%)0.407
Extent of resection
  GTR27 (51%)135 (83%)4 (80%)<0.001
  STR26 (49%)27 (16%)1 (20%)<0.001
  Biopsy0 (0%)1 (1%)0 (0%)0.836
Cases w/surgical complications18 (34%)50 (31%)2 (40%)0.834
Complication type
  New/worse sensory symptom11 (21%)22 (13%)1 (20%)0.427
  New/worse motor deficit4 (8%)8 (5%)0 (0%)0.658
  CSF leak/pseudomeningocele1 (2%)9 (6%)0 (0%)0.481
  Wound infection0 (0%)11 (7%)0 (0%)0.128
  Spinal deformity4 (8%)1 (1%)0 (0%)0.012
  Other0 (0%)4 (2%)2 (40%)<0.001

Tumor Location and Complications

Complications after surgery for tumors in the cervical, thoracic, and lumbosacral spine were compared (Table 5). There were 85 cervical, 62 thoracic, and 74 lumbosacral lesions with no significant differences in age or sex. Neurofibromatosis Type 1 was present in 31 cases of cervical tumors (36%) compared with 6 thoracic (10%) and 5 lumbosacral (7%) cases, a significant difference (p < 0.001). Cervical tumors were associated with lower rates of pain at presentation (64%) than the rates associated with thoracic (82%) and lumbosacral (85%) lesions (p = 0.006). Complications were identified in 31 cervical (36%), 11 thoracic (18%), and 28 (38%) lumbosacral tumors, which was a significant difference (p = 0.021). There were no significant differences in sensory or motor deficits among tumor locations. Cerebrospinal fluid leaks or pseudomeningoceles (8%) and wound infections (8%) were more common among lumbosacral tumors than cervical (4% and 2%, respectively) and thoracic (2% and 5%, respectively) tumors; however, these differences were not significant (p = 0.164 and 0.250, respectively). Rates of deformity were higher among cervical lesions (6%) than those among thoracic and lumbosacral lesions (0 and 1%, respectively, p = 0.065).

TABLE 5

Summary of characteristics among 221 PNSTs, according to spinal level

CharacteristicCervicalThoracicLumbosacralp Value
No. of tumors856274
Mean patient age in yrs4246480.099
Neurofibromatosis
  Type 131 (36%)6 (10%)5 (7%)<0.001
  Type 25 (6%)1 (2%)5 (7%)0.345
  None49 (58%)55 (89%)64 (86%)<0.001
Tumor pathology
  Neurofibroma39 (46%)7 (11%)7 (9%)<0.001
  Schwannoma44 (52%)55 (89%)64 (86%)<0.001
  MPNST2 (2%)0 (0%)3 (4%)0.285
Dural location
  Intradural49 (58%)32 (52%)49 (66%)0.218
  Extradural7 (8%)9 (14%)10 (14%)0.430
  Dumbbell24 (28%)16 (26%)12 (16%)0.180
  Paraspinal5 (6%)5 (8%)3 (4%)0.613
Extent of resection
  GTR47 (55%)56 (90%)63 (85%)<0.001
  STR38 (45%)6 (10%)10 (14%)<0.001
  Biopsy0 (0%)0 (0%)1 (1%)0.369
Cases w/surgical complications31 (36%)11 (18%)28 (38%)0.021
Complication type
  New/worse sensory symptom14 (16%)8 (13%)12 (16%)0.815
  New/worse motor deficit5 (6%)1 (2%)6 (8%)0.243
  CSF leak/pseudomeningocele3 (4%)1 (2%)6 (8%)0.164
    Symptomatic3 (4%)1 (2%)4 (5%)0.498
    Requiring surgical repair1 (1%)1 (2%)5 (7%)0.096
  Wound infection2 (2%)3 (5%)6 (8%)0.250
  Spinal deformity5 (6%)0 (0%)1 (1%)0.065
  Other3 (4%)0 (0%)3 (4%)0.294

Potential associations between surgical complications and intradural, dumbbell, extradural, and paraspinal locations were explored and are summarized in Table 6. Dumbbell tumors were associated with the highest rate of complications (48%) compared with intradural (26%), extradural (31%), and paraspinal (23%) tumors, a difference that was significant (p = 0.033). There was no statistically significant difference when comparing the type of complication and tumor location, but new or worsening motor deficits were higher among dumbbell tumors (6 [12%] of 52) compared with intradural (4 [3%] of 130), extradural (1 [4%] of 26), and paraspinal (1 [8%] of 13) lesions. The rate of GTR was also notably lower for dumbbell tumors (60%) compared with intradural (79%), extradural (85%), and paraspinal (77%) tumors, a difference that was significant (p = 0.027). Cerebrospinal fluid leaks, pseudomeningoceles, and wound infections were only present among intradural and dumbbell tumors.

TABLE 6

Summary of characteristics among 221 PNST cases, according to tumor location

CharacteristicIntraduralDumbbellExtraduralParaspinalp Value
No. of tumors130522613
Mean patient age in yrs454545420.935
NF
  Type 122 (17%)13 (25%)3 (12%)4 (31%)0.297
  Type 28 (6%)2 (4%)1 (4%)0 (0%)0.736
  None100 (77%)37 (71%)22 (85%)9 (69%)0.549
Tumor pathology
  Neurofibroma27 (21%)15 (29%)6 (23%)5 (38%)0.405
  Schwannoma102 (78%)33 (63%)20 (77%)8 (62%)0.140
  MPNST1 (1%)4 (8%)0 (0%)0 (0%)0.027
Location
  Cervical49 (38%)24 (46%)7 (27%)5 (38%)0.424
  Thoracic32 (25%)16 (31%)9 (35%)5 (38%)0.531
  Lumbosacral49 (38%)12 (23%)10 (38%)3 (23%)0.214
Extent of resection
  GTR103 (79%)31 (60%)22 (85%)10 (77%)0.027
  STR27 (21%)21 (40%)4 (15%)2 (15%)0.020
  Biopsy0 (0%)0 (0%)0 (0%)1 (8%)<0.001
Cases w/surgical complications34 (26%)25 (48%)8 (31%)3 (23%)0.033
Complication type
  New/worse sensory symptom14 (11%)12 (23%)6 (23%)2 (15%)0.129
  New/worse motor deficit4 (3%)6 (12%)1 (4%)1 (8%)0.142
  CSF leak/pseudomeningocele7 (5%)3 (6%)0 (0%)0 (0%)0.521
    Symptomatic5 (4%)3 (6%)0 (0%)0 (0%)0.537
    Requiring surgical repair7 (5%)0 (0%)0 (0%)0 (0%)0.167
  Wound infection8 (6%)3 (6%)0 (0%)0 (0%)0.477
  Spinal deformity3 (2%)1 (2%)1 (4%)0 (0%)0.891
  Other1 (1%)4 (8%)0 (0%)1 (8%)0.034

Extent of Resection and Complications

Rates of surgical complications were compared between patients who underwent GTR and those who underwent STR (Table 7). There were 166 patients in the GTR group and 54 in the STR group, with those in the former having a slightly older age (46 vs 41 years, p = 0.031) and those in the latter having a higher rate of NF1 (46% vs 10%, p < 0.001). Rates of NF2 were similar between the groups. Among the subtotally resected tumors, there were a higher rate of cervical lesions and lower rates of thoracic and lumbosacral lesions compared with rates among the gross totally resection lesions. Tumors in the STR group were also more likely to be neurofibromas and possess a dumbbell morphology compared with the GTR group. Tumors in the STR group were larger with a maximum diameter of 4.4 cm compared with 3.3 cm in the GTR group; however, this difference was not statistically significant (p = 0.072).

TABLE 7

Summary of characteristics in 221 PNST cases, according to extent of resection

CharacteristicGTRSTRp Value
No. of tumors16654
Mean patient age in yrs46410.031
NF
  Type 117 (10%)25 (46%)<0.001
  Type 26 (4%)5 (9%)0.098
  None143 (86%)24 (44%)<0.001
Tumor location
  Cervical47 (28%)38 (70%)<0.001
  Thoracic56 (34%)6 (11%)0.001
  Lumbosacral63 (38%)10 (18%)0.008
Dural location
  Intradural103 (62%)27 (50%)0.118
  Extradural22 (13%)4 (7%)0.248
  Dumbbell31 (19%)21 (39%)0.002
  Paraspinal10 (6%)2 (4%)0.735*
Tumor pathology
  Neurofibroma27 (16%)26 (48%)<0.001
  Schwannoma135 (81%)27 (50%)<0.001
  MPNST4 (2%)1 (2%)1.000*
Tumor size
  Max diameter in cm3.34.40.072
  Vertebral levels spanned1.21.20.352
Cases w/surgical complications46 (28%)24 (44%)0.022
Complication type
  New/worse sensory symptom25 (15%)9 (17%)0.777
  New/worse motor deficit8 (5%)4 (7%)0.467
  CSF leak/pseudomeningocele9 (5%)1 (2%)0.457*
  Wound infection7 (4%)4 (7%)0.470*
  Spinal deformity2 (1%)3 (6%)0.096*
  Other4 (2%)2 (4%)0.637*
Intraop neuromonitoring
  Any modality120 (72%)30 (56%)0.022
  MEP112 (67%)28 (52%)0.038
  SSEP114 (69%)29 (54%)0.045
  EMG119 (72%)29 (54%)0.014
  Evoked EMG13 (8%)4 (7%)1.000*

Fisher's exact test.

There were 24 complications in the STR group (44%) compared with 46 (28%) in the GTR group (p = 0.022). Rates of new or worsening sensory symptoms were 15% in the GTR group and 17% in the STR group (p = 0.777). Rates of new or worsening weakness were similar in the STR and GTR groups (7% vs 5%, respectively). There were no significant differences in the rates of CSF leak or pseudomeningocele, wound infection, or postoperative spinal deformity between the 2 groups. It was not possible to determine retrospectively if the use of neuromonitoring influenced whether GTR or STR was accomplished; however, the rate of GTR among cases with neuromonitoring was 79% compared with 66% in those without (p = 0.022). This difference remained significant for different modalities including MEPs, SSEPs, and EMG.

Discussion

The goal of this study was to describe outcomes in spinal nerve sheath tumor surgery and identify factors associated with new or worsening postoperative neurological deficits and surgical complications. Among the 221 tumors included in this study, there were 70 complications for a rate of 32%. We included new or worsening neurological deficits (motor and sensory) as complications even in cases in which they were expected given the need for nerve root sacrifice. Overall, the rate of new or worsening sensory symptoms was 15%; the rate of new or worsening weakness was 5%. Kim et al. examined their experience in the management of spinal schwannomas more than 20 years ago and found that among 31 patients who had undergone nerve sacrifice, 7 (22%) developed partial loss of strength or sensation, though none was debilitating.15 Preoperative EMG was performed in a subset of these patients and showed that denervation was associated with an increased risk of postoperative deficit. These authors concluded that spinal roots associated with spinal schwannomas were often nonfunctional and that the risk of disabling neurological injury after nerve sacrifice was small.

In subsequent studies, Seppälä and colleagues assessed both neurological outcomes and complications related to wound healing and infection.24 Among 142 spinal schwannomas with follow-up, 10 (7%) were considered clinically worse postoperatively; however, the specific symptoms were not described. Nineteen of the 187 patients in the study suffered complications related to wound infection or dehiscence, bleeding, DVT, or the lungs. In a similar study of 32 spinal neurofibromas, Seppälä et al. reported 5 neurological deteriorations (16%).23 Late complications included spinal deformity in 2 patients and severe dysesthesias in another 2 patients. Among the 15 patients with nerve sacrifice who were alive at the last follow-up, 6 (40%) had sensory deficits and 5 (33%) had motor deficits, all of which were mild. In a more contemporary series, Safavi-Abbasi et al. examined complications in a cohort in which neurophysiological monitoring was used in most cases.22 Among 131 cases of schwannoma, 16 (12%) developed sensory deficits and 3 (2%) had motor weakness. An additional 14 (11%) had CSF leaks or pseudomeningoceles, 5 (4%) had wound infections, 4 (3%) had meningitis, and 1 (1%) had spinal deformity. In other recent studies, Fernandes et al. reported a complication rate of 10% that included CSF fistula, wound infection, DVT, and pulmonary complication.11 Nanda et al. reported 18 complications in 61 patients for a rate of 30%, which included pseudomeningocele and CSF leak in 5 cases (8%), instability in 2 cases (3%), wound infection in 3 cases (5%), and 1 case each of DVT, pulmonary embolism, incomplete recurrent laryngeal nerve injury, trigeminal nerve injury, and pseudarthrosis.18

In the current study we describe neurological outcomes and surgical complications in a series of 221 tumors treated at a single center. There was no difference in age, sex, clinical presentation, symptom duration, or extent of resection among patients when comparing those with new or worsening neurological outcomes and surgical complications and those without such outcomes. There was a higher incidence of NF2 in patients with complications, and although this difference was statistically significant, it may be related to the small sample size. There was no difference in complications when comparing different tumor pathologies or sizes; however, spinal level was an important factor since complications were more common among cervical and lumbosacral tumors than among thoracic spine lesions. Not surprisingly, this difference appears to be driven by increased rates of CSF leak, pseudomeningocele, and motor deficits. Rates of new or worsening neurological deficits did not significantly differ by spinal level; however, as expected, rates were lower among thoracic tumors compared with those among cervical or lumbosacral lesions. We observed a higher complication rate among dumbbell tumors; these lesions had the highest rate of new or worsening motor deficits and rates of CSF leak or pseudomeningocele and a wound infection rate that was similar to that for intradural lesions, although none of these differences met statistical significance.

Among 221 tumors, only 5 were associated with new spinal deformity. Four of these were cervical neurofibromas in pediatric patients who had undergone multilevel laminectomies without spinal fusion at the initial surgery. It is therefore appropriate to consider spinal fusion in these patients given their risk. We reported outcomes for patients with spinal nerve sheath tumors who had undergone spinal fusion with tumor resection and found that fusions were most common among dumbbell and extradural tumors as well as tumors at the cervicothoracic junction.21 Rates of new or worsening neurological deficit, CSF leak, pseudomeningocele, and infection were no different among patients who underwent fusions compared with those who did not.

The rate of GTR in this series was 75%, which on initial review may seem lower than expected; however, the rate was driven by a high number of cervical neurofibromas in patients with NF1. Among schwannomas, the rate of GTR was 83% compared with 51% among neurofibromas. Among 53 neurofibromas included in this analysis, 74% of cases involved patients with NF1, 74% were located in the cervical spine, and 79% were either intradural or dumbbell lesions. The high rate of cervical lesions is probably driven by the fact that these tumors are more likely to be symptomatic and treated compared with neurofibromas at other spinal levels. The lower rate of GTR can be explained by the fact that NF1 is not a curable entity and that the goal of surgery in these cases is decompression of the spinal cord and neural elements and not necessarily complete tumor resection.

With respect to the use of intraoperative neuromonitoring, there was no difference in complication rates when comparing cases with and without this adjunct. This finding does not imply that neuromonitoring is not a useful tool in the resection of these lesions, but rather that the likelihood of a postoperative deficit is probably more attributable to the invasive nature of the specific tumor rather than an inability to identify functional nerve roots. Additionally, even in cases with neuromonitoring, tumor resection may inevitably require nerve root sacrifice, thus explaining the similar rates of postoperative motor and sensory deficits. Our overall rates of new or worsening sensory symptoms (15%) and new or worsening weakness (5%) are consistent with other reports. Interestingly, we found higher rates of intraoperative neuromonitoring use among tumors treated with GTR than among tumors treated with STR. The retrospective nature of this study makes it difficult to determine if the use of neuromonitoring was directly responsible for the higher rates of GTR, and although these findings are intuitive, they warrant future study.

This study is limited by its retrospective design and limited follow-up. The mean time from surgery to the last clinic visit was 32 months; therefore, our rates of new or worsening neurological deficit may actually be overestimates since in some cases neurological function can improve over time. Although we identified a statistically significant increase in surgical complications among patients with NF2, the sample numbers are too small to make any definitive conclusions about the increased risk in these patients, and future studies should investigate this potential relationship. The rarity of these lesions makes prospective analysis challenging, but future studies may also focus on pre- and postoperative imaging features that can predict ease of resection or anticipate intraoperative challenges so that a particular technique can be avoided to prevent postoperative deficits.

Conclusions

Resection is a safe and effective treatment for spinal nerve sheath tumors. New or worsening neurological deficits or surgical complications were present in 32% of cases. The most common was new or worsening sensory symptoms (15%), followed by new or worsening weakness (5%), CSF leak or pseudomeningocele (5%), wound infection (5%), and spinal deformity (2%). Complications were more common in cervical and lumbosacral tumors but had no association with patient age, clinical presentation, symptom duration, tumor size, or tumor pathology. Intradural and dumbbell tumors were associated with higher rates of CSF leak, pseudomeningocele, and wound infection. Use of intraoperative neuromonitoring was associated with a higher rate of GTR; however, determining the true effect of neuromonitoring in minimizing postoperative neurological deficits and enhancing the extent of resection was not feasible given the retrospective nature of this study. Although undesirable, neurological deficits and surgical complications represent an inevitable consequence of spinal nerve sheath tumor surgery given the intimacy of these lesions with functional neural elements.

References

  • 1

    Abul-Kasim KThurnher MMMcKeever PSundgren PC: Intradural spinal tumors: current classification and MRI features. Neuroradiology 50:3013142008

  • 2

    Aghayev KVrionis FChamberlain MC: Adult intradural primary spinal cord tumors. J Natl Compr Canc Netw 9:4344472011

  • 3

    Albanese VPlatania N: Spinal intradural extramedullary tumors. Personal experience. J Neurosurg Sci 46:18242002

  • 4

    Antinheimo JSankila RCarpén OPukkala ESainio MJääskeläinen J: Population-based analysis of sporadic and type 2 neurofibromatosis-associated meningiomas and schwannomas. Neurology 54:71762000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Carey JCViskochil DH: Neurofibromatosis type 1: A model condition for the study of the molecular basis of variable expressivity in human disorders. Am J Med Genet 89:7131999

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Celli P: Treatment of relevant nerve roots involved in nerve sheath tumors: removal or preservation?. Neurosurgery 51:6846922002

  • 7

    Chamberlain MCTredway TL: Adult primary intradural spinal cord tumors: a review. Curr Neurol Neurosci Rep 11:3203282011

  • 8

    Conti PPansini GMouchaty HCapuano CConti R: Spinal neurinomas: retrospective analysis and long-term outcome of 179 consecutively operated cases and review of the literature. Surg Neurol 61:34442004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Egelhoff JCBates DJRoss JSRothner ADCohen BH: Spinal MR findings in neurofibromatosis types 1 and 2. AJNR Am J Neuroradiol 13:107110771992

  • 10

    Engelhard HHVillano JLPorter KRStewart AKBarua MBarker FG: Clinical presentation, histology, and treatment in 430 patients with primary tumors of the spinal cord, spinal meninges, or cauda equina. J Neurosurg Spine 13:67772010

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

    Fernandes RLLynch JCWelling LGonçalves MTragante RTemponi V: Complete removal of the spinal nerve sheath tumors. Surgical technics and results from a series of 30 patients. Arq Neuropsiquiatr 72:3123172014

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

    Huson SMHarper PSCompston DA: Von Recklinghausen neurofibromatosis. A clinical and population study in southeast Wales. Brain 111:135513811988

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Jeon JHHwang HSJeong JHPark SHMoon JGKim CH: Spinal schwannoma; analysis of 40 cases. J Korean Neurosurg Soc 43:1351382008

  • 14

    Jinnai TKoyama T: Clinical characteristics of spinal nerve sheath tumors: analysis of 149 cases. Neurosurgery 56:5105152005

  • 15

    Kim PEbersold MJOnofrio BMQuast LM: Surgery of spinal nerve schwannoma. Risk of neurological deficit after resection of involved root. J Neurosurg 71:8108141989

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

    Klekamp JSamii M: Surgery of Spinal Tumors New YorkSpringer2007

  • 17

    Koontz NAWiens ALAgarwal AHingtgen CMEmerson REMosier KM: Schwannomatosis: the overlooked neurofibromatosis?. AJR Am J Roentgenol 200:W646W6532013

    • Search Google Scholar
    • Export Citation
  • 18

    Nanda AKukreja SAmbekar SBollam PSin AH: Surgical strategies in the management of spinal nerve sheath tumors. World Neurosurg 83:8868992015

  • 19

    Poyhonen MLeisti ELKytölä SLeisti J: Hereditary spinal neurofibromatosis: a rare form of NF1?. J Med Genet 34:1841871997

  • 20

    Riccardi VM: Neurofibromatosis: Phenotype Natural History and Pathogenesis ed 2BaltimoreJohns Hopkins University Press1992

  • 21

    Safaee MOh TBarbaro NMChou DMummaneni PVWeinstein PR: Results of spinal fusion after spinal nerve sheath tumor resection. World Neurosurg 90:6132016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Safavi-Abbasi SSenoglu MTheodore NWorkman RKGharabaghi AFeiz-Erfan I: Microsurgical management of spinal schwannomas: evaluation of 128 cases. J Neurosurg Spine 9:40472008

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

    Seppälä MTHaltia MJSankila RJJääskeläinen JEHeiskanen O: Long-term outcome after removal of spinal neurofibroma. J Neurosurg 82:5725771995

  • 24

    Seppälä MTHaltia MJSankila RJJääskeläinen JEHeiskanen O: Long-term outcome after removal of spinal schwannoma: a clinicopathological study of 187 cases. J Neurosurg 83:6216261995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Stadler JA IIIQadri UTang JAScheer JKMelkonian SCSmith ZA: Malignant peripheral nerve sheath tumors of the spine: a SEER database analysis. J Clin Neurosci 21:110611112014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Thakkar SDFeigen UMautner VF: Spinal tumours in neurofibromatosis type 1: an MRI study of frequency, multiplicity and variety. Neuroradiology 41:6256291999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Tonsgard JHKwak SMShort MPDachman AH: CT imaging in adults with neurofibromatosis-1: frequent asymptomatic plexiform lesions. Neurology 50:175517601998

  • 28

    Viskochil DCarey JCAlternate and related forms of the neurofibromatoses. Huson SMHughes RAC: The Neurofibromatoses: A Pathogenetic and Clinical Overview LondonChapman and Hall Medical1994

    • Search Google Scholar
    • Export Citation
  • 29

    von Deimling AKrone WMenon AG: Neurofibromatosis type 1: pathology, clinical features and molecular genetics. Brain Pathol 5:1531621995

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Wimmer KMühlbauer MEckart MCallens TRehder HBirkner T: A patient severely affected by spinal neurofibromas carries a recurrent splice site mutation in the NF1 gene. Eur J Hum Genet 10:3343382002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

Disclosures

Dr. Ames is a consultant for DePuy, Stryker, Medtronic; owns stock in Doctors Research Group; holds a patent with Fish & Richardson, PC; and receives royalties from Biomet Spine and Stryker. Dr. Chou is a consultant for Globus, Medtronic, and Orthofix. Dr. Mummaneni is a consultant for DePuy Spine; owns stock in Spinicity/ISD; receives royalties from Thieme Publishing, DePuy Spine, Springer Publishing, and Taylor and Francis Publishing; receives honoraria from Globus and AOSpine; and receives funding from the NREF.

Author Contributions

Conception and design: Safaee, Ames. Acquisition of data: Safaee, Lyon, Chin, Tihan, Ames. Analysis and interpretation of data: all authors. Drafting the article: Safaee, Ames. Critically revising the article: Safaee, Lyon, Barbaro, Chou, Mummaneni, Weinstein, Tihan, Ames. Reviewed submitted version of manuscript: Safaee, Ames. Approved the final version of the manuscript on behalf of all authors: Safaee. Administrative/technical/material support: Ames. Study supervision: Ames.

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Article Information

INCLUDE WHEN CITING Published online July 29, 2016; DOI: 10.3171/2016.5.SPINE15974.

Correspondence Michael Safaee, Department of Neurological Surgery, 505 Parnassus Ave., Rm. M779, San Francisco, CA 94143. email: michael.safaee@ucsf.edu.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1

    Abul-Kasim KThurnher MMMcKeever PSundgren PC: Intradural spinal tumors: current classification and MRI features. Neuroradiology 50:3013142008

  • 2

    Aghayev KVrionis FChamberlain MC: Adult intradural primary spinal cord tumors. J Natl Compr Canc Netw 9:4344472011

  • 3

    Albanese VPlatania N: Spinal intradural extramedullary tumors. Personal experience. J Neurosurg Sci 46:18242002

  • 4

    Antinheimo JSankila RCarpén OPukkala ESainio MJääskeläinen J: Population-based analysis of sporadic and type 2 neurofibromatosis-associated meningiomas and schwannomas. Neurology 54:71762000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Carey JCViskochil DH: Neurofibromatosis type 1: A model condition for the study of the molecular basis of variable expressivity in human disorders. Am J Med Genet 89:7131999

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Celli P: Treatment of relevant nerve roots involved in nerve sheath tumors: removal or preservation?. Neurosurgery 51:6846922002

  • 7

    Chamberlain MCTredway TL: Adult primary intradural spinal cord tumors: a review. Curr Neurol Neurosci Rep 11:3203282011

  • 8

    Conti PPansini GMouchaty HCapuano CConti R: Spinal neurinomas: retrospective analysis and long-term outcome of 179 consecutively operated cases and review of the literature. Surg Neurol 61:34442004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Egelhoff JCBates DJRoss JSRothner ADCohen BH: Spinal MR findings in neurofibromatosis types 1 and 2. AJNR Am J Neuroradiol 13:107110771992

  • 10

    Engelhard HHVillano JLPorter KRStewart AKBarua MBarker FG: Clinical presentation, histology, and treatment in 430 patients with primary tumors of the spinal cord, spinal meninges, or cauda equina. J Neurosurg Spine 13:67772010

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

    Fernandes RLLynch JCWelling LGonçalves MTragante RTemponi V: Complete removal of the spinal nerve sheath tumors. Surgical technics and results from a series of 30 patients. Arq Neuropsiquiatr 72:3123172014

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

    Huson SMHarper PSCompston DA: Von Recklinghausen neurofibromatosis. A clinical and population study in southeast Wales. Brain 111:135513811988

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Jeon JHHwang HSJeong JHPark SHMoon JGKim CH: Spinal schwannoma; analysis of 40 cases. J Korean Neurosurg Soc 43:1351382008

  • 14

    Jinnai TKoyama T: Clinical characteristics of spinal nerve sheath tumors: analysis of 149 cases. Neurosurgery 56:5105152005

  • 15

    Kim PEbersold MJOnofrio BMQuast LM: Surgery of spinal nerve schwannoma. Risk of neurological deficit after resection of involved root. J Neurosurg 71:8108141989

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

    Klekamp JSamii M: Surgery of Spinal Tumors New YorkSpringer2007

  • 17

    Koontz NAWiens ALAgarwal AHingtgen CMEmerson REMosier KM: Schwannomatosis: the overlooked neurofibromatosis?. AJR Am J Roentgenol 200:W646W6532013

    • Search Google Scholar
    • Export Citation
  • 18

    Nanda AKukreja SAmbekar SBollam PSin AH: Surgical strategies in the management of spinal nerve sheath tumors. World Neurosurg 83:8868992015

  • 19

    Poyhonen MLeisti ELKytölä SLeisti J: Hereditary spinal neurofibromatosis: a rare form of NF1?. J Med Genet 34:1841871997

  • 20

    Riccardi VM: Neurofibromatosis: Phenotype Natural History and Pathogenesis ed 2BaltimoreJohns Hopkins University Press1992

  • 21

    Safaee MOh TBarbaro NMChou DMummaneni PVWeinstein PR: Results of spinal fusion after spinal nerve sheath tumor resection. World Neurosurg 90:6132016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Safavi-Abbasi SSenoglu MTheodore NWorkman RKGharabaghi AFeiz-Erfan I: Microsurgical management of spinal schwannomas: evaluation of 128 cases. J Neurosurg Spine 9:40472008

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

    Seppälä MTHaltia MJSankila RJJääskeläinen JEHeiskanen O: Long-term outcome after removal of spinal neurofibroma. J Neurosurg 82:5725771995

  • 24

    Seppälä MTHaltia MJSankila RJJääskeläinen JEHeiskanen O: Long-term outcome after removal of spinal schwannoma: a clinicopathological study of 187 cases. J Neurosurg 83:6216261995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Stadler JA IIIQadri UTang JAScheer JKMelkonian SCSmith ZA: Malignant peripheral nerve sheath tumors of the spine: a SEER database analysis. J Clin Neurosci 21:110611112014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Thakkar SDFeigen UMautner VF: Spinal tumours in neurofibromatosis type 1: an MRI study of frequency, multiplicity and variety. Neuroradiology 41:6256291999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Tonsgard JHKwak SMShort MPDachman AH: CT imaging in adults with neurofibromatosis-1: frequent asymptomatic plexiform lesions. Neurology 50:175517601998

  • 28

    Viskochil DCarey JCAlternate and related forms of the neurofibromatoses. Huson SMHughes RAC: The Neurofibromatoses: A Pathogenetic and Clinical Overview LondonChapman and Hall Medical1994

    • Search Google Scholar
    • Export Citation
  • 29

    von Deimling AKrone WMenon AG: Neurofibromatosis type 1: pathology, clinical features and molecular genetics. Brain Pathol 5:1531621995

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Wimmer KMühlbauer MEckart MCallens TRehder HBirkner T: A patient severely affected by spinal neurofibromas carries a recurrent splice site mutation in the NF1 gene. Eur J Hum Genet 10:3343382002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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