Spinal meningiomas: clinicoradiological factors predicting recurrence and functional outcome

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OBJECTIVE

Spinal meningiomas are benign tumors with a wide spectrum of clinical and radiological features at presentation. The authors analyzed multiple clinicoradiological factors to predict recurrence and functional outcome in a cohort with a mean follow-up of more than 4 years. The authors also discuss the results of clinical studies regarding spinal meningiomas in the last 15 years.

METHODS

The authors retrospectively reviewed the clinical and radiological details of patients who underwent surgery for spinal tumors between 2001 and 2015 that were histopathologically confirmed as meningiomas. Demographic parameters, such as age, sex, race, and association with neurofibromatosis Type 2, were considered. Radiological parameters, such as tumor size, signal changes of spinal cord, spinal level, number of levels, location of tumor attachment, shape of tumor, and presence of dural tail/calcification, were noted. These factors were analyzed to predict recurrence and functional outcome. Furthermore, a pooled analysis was performed from 13 reports of spinal meningiomas in the last 15 years.

RESULTS

A total of 38 patients were included in this study. Male sex and tumors with radiological evidence of a dural tail were associated with an increased risk of recurrence at a mean follow-up of 51.2 months. Ventral or ventrolateral location, large tumors, T2 cord signal changes, and poor preoperative functional status were associated with poor functional outcome at 1-year follow-up.

CONCLUSIONS

Spine surgeons must be aware of the natural history and risk factors of spinal meningiomas to establish a prognosis for their patients.

ABBREVIATIONSNF2 = neurofibromatosis Type 2.

OBJECTIVE

Spinal meningiomas are benign tumors with a wide spectrum of clinical and radiological features at presentation. The authors analyzed multiple clinicoradiological factors to predict recurrence and functional outcome in a cohort with a mean follow-up of more than 4 years. The authors also discuss the results of clinical studies regarding spinal meningiomas in the last 15 years.

METHODS

The authors retrospectively reviewed the clinical and radiological details of patients who underwent surgery for spinal tumors between 2001 and 2015 that were histopathologically confirmed as meningiomas. Demographic parameters, such as age, sex, race, and association with neurofibromatosis Type 2, were considered. Radiological parameters, such as tumor size, signal changes of spinal cord, spinal level, number of levels, location of tumor attachment, shape of tumor, and presence of dural tail/calcification, were noted. These factors were analyzed to predict recurrence and functional outcome. Furthermore, a pooled analysis was performed from 13 reports of spinal meningiomas in the last 15 years.

RESULTS

A total of 38 patients were included in this study. Male sex and tumors with radiological evidence of a dural tail were associated with an increased risk of recurrence at a mean follow-up of 51.2 months. Ventral or ventrolateral location, large tumors, T2 cord signal changes, and poor preoperative functional status were associated with poor functional outcome at 1-year follow-up.

CONCLUSIONS

Spine surgeons must be aware of the natural history and risk factors of spinal meningiomas to establish a prognosis for their patients.

Spinal meningiomas are common, slow-growing tumors with a known association with neurofibromatosis Type 2 (NF2). They account for 25%–45% of all intradural spinal tumors and about 2% of all meningiomas.33 However, they can be extradural, dumbbell shaped, or en plaque type. Safe, complete resection is possible in most cases, with a favorable outcome. Although few studies have discussed the factors predicting recurrence, composite studies of multiple clinicoradiological factors predicting the resection rate, recurrence, and functional outcome in a cohort of long follow-up are relatively scarce in the literature. In this study, we considered several clinical and radiological factors that may possibly influence the aforementioned end point. In addition, we also performed a systematic review of all case series comprising at least 20 patients between 2001 and 2015 that discussed the demographics and surgical outcome of spinal meningiomas.

Methods

In this retrospective study, we reviewed clinical parameters and images for 38 patients who underwent surgery at our institution between 1999 and 2014 with a histological confirmation. Patients with spinal meningiomas extending up to the foramen magnum were excluded. We performed this study with strict adherence to HIPAA (Health Insurance Portability and Accountability Act) guidelines after obtaining permission from the institutional review board at our institution.

Demographic parameters such as age, sex, race, and association with NF2 were considered. Radiological parameters such as tumor size (in comparison with the spinal canal), T2 signal changes of the spinal cord, location in the spinal canal (cervical, thoracic, cervicothoracic, or lumbosacral), number of levels, location of tumor attachment (ventral, lateral, and dorsal), shape (dumbbell or en plaque), and presence of a dural tail and calcification were noted.

The extent of resection was graded based on operative notes and confirmed with postoperative MRI (whenever available) and was classified according to Simpson's grading system.43 Follow-up imaging was done 1 year after surgery for most patients and every 2–3 years thereafter or earlier in case of suspicion of recurrence.

The functional status was analyzed utilizing the modified McCormick grading system to score the patient's functional status before surgery and at the 1-year follow-up.23,25

Statistical Analysis

Statistical analysis was performed using SPSS (version 22.0, IBM). The clinical and radiological factors were dichotomized. The recurrence rate (recurrence vs no recurrence) and functional outcome (satisfactory improvement, i.e., modified McCormick Grades I or II vs unsatisfactory improvement, i.e., modified McCormick Grades III–V) were analyzed. The variables considered were age (> 50 years vs < 50 years), sex (male vs female), race (Caucasian vs African American), preoperative modified McCormick grade (I–III vs IV–V), diameter of the tumor (occupying ≥ 75% of the canal in both transverse and anteroposterior diameters of the spinal canal), craniocaudal extension of the tumor (1- to 2-level vs more than 2 levels), location of attachment (ventral or ventrolateral vs lateral, dorsal, and dorsolateral), presence or absence of T2 signal changes within the spinal cord, dural tail, dumbbell shape, en plaque attachment, and calcification. A binomial regression analysis was performed to examine the association. Survival analysis was performed using the Kaplan-Meier method. Comparison between the 2 groups was performed using an independent t-test.

Literature Review

A literature search was performed for the key words “spinal meningioma” and “spinal cord meningioma” in the English-language literature from 2001 to 2015. The clinical papers that discussed the surgery and outcome in all age groups and all histological types of meningiomas were selected for a pooled analysis. Studies that reported at least 20 patients were included.35 The studies that included spine tumors of more than 1 histopathology were excluded.6 The reports discussing a subset of spinal meningiomas were excluded as well.11,28,37,46,49 The summary of these studies are tabulated (see Table 5).

Results

Patient Demographics and Radiological Findings

The median age of the study population was 56 years (range 12–92 years) with a male-to-female ratio of 1:4.42. Patients with NF2 (n = 6) were younger at presentation than patients without NF2 (p < 0.0001). Approximately two-thirds of the tumors were located in the thoracic region. Only 10% of tumors had extension of more than 2 levels in the craniocaudal direction. Most tumors were laterally placed in relation to the spinal cord; the other tumors were situated ventrolateral to the cord in about one-third of the patients and ventral to the cord in only 5% of cases. A dural tail was present in only 15.8% of cases. Calcification was documented on images and operative notes in only 1 patient. The clinical and radiological characteristics are summarized in Table 1. Table 2 provides a summary of the patients with primary tumors from the multicenter, comparative review. Images of 3 illustrative cases are shown in Fig. 1.

TABLE 1.

Clinicoradiological features of the patient cohort

VariableValue*
Total no. of patients38
Age in yrs
  Complete cohort
    Median56
    Range12–92
  w/NF2
    Median19.50
    Range12–44
  w/o NF2
    Median61
    Range15–92
Sex
  Male7 (18.42)
  Female31 (81.58)
Race
  White or Caucasian18 (47.37)
  Black or African American13 (34.21)
  Other7 (18.42)
Associated w/NF26 (15.79)
Tumor location
  Cervical10 (26.32)
  Cervicothoracic4 (10.53)
  Thoracic24 (63.16)
Craniocaudal tumor extension
  1–2 levels34 (89.47)
  ≥3 levels4 (10.53)
Relation of tumor to spinal cord
  Ventral2 (5.26)
  Ventrolateral12 (31.58)
  Lateral20 (52.63)
  Dorsal/dorsolateral2 (5.26)
  Extraforaminal extension/dumbbell-shaped2 (5.26)
Tumor occupying ≥75% of spinal canal in AP & transverse directions21 (55.26)
T2 hyperintense signal changes10 (26.32)
Dural tail6 (15.79)
Calcification1 (2.63)
Preop MMG
  III24 (63.16)
  IV13 (34.21)
  V1 (2.63)

AP = anteroposterior; MMG = modified McCormick grade.

Values are presented as the number of patients (%) unless specified otherwise.

TABLE 2.

Surgery, complications, and follow-up

VariableValue*
WHO grade
  I35 (92.1)
  II3 (7.89)
Complete resection
  Simpson Grade I2 (5.26)
  Simpson Grade II35 (92.1)
  Overall37 (97.37)
Complications
  CSF leakage2 (5.26)
  Wound complications4 (10.53)
Follow-up duration in mos
  Mean51.2 ± 22.4
  Range12–82
Recurrence4 (10.53)
RFS
  Median48
  Range12–82
  1 yr29/29 (100)
  2 yr24/25 (96)
  5 yrs13/16 (81.25)
Functional outcome (at 1-yr follow-up)
  Satisfactory outcome29 (76.32)
  Unsatisfactory outcome9 (23.68)

RFS = recurrence-free survival

Values are presented as the number of patients (%) unless indicated otherwise.

Improvement to McCormick Grade 1 or 2.

McCormick Grade III–V or unchanged over preoperative status.

FIG. 1.
FIG. 1.

A–D: Case 1. A 76-year-old woman presented with back pain, gait instability, and myelopathic features. MRI revealed an intradural extramedullary lesion at T7–8. The tumor was occupying more than three-fourths of the spinal canal and had a lateral attachment. Postcontrast sagittal (A), coronal (B), and axial (C) images are shown. The patient underwent a T7–8 laminectomy and Simpson Grade II excision of the lesion. The biopsy sample was suggestive of WHO Grade I meningioma. Ki-67 showed positive staining in fewer than 2% of the tumor cells. The MR image obtained at 1-year follow-up (D) did not reveal any recurrence. E–H: Case 2. A 41-year-old man presented with myelopathic features. MRI revealed an intradural extramedullary lesion at T2–3. A dural tail was evident on postcontrast sagittal (E) and axial (F) images (arrows). A hypointense rim of calcification was also evident (F and G, arrowheads). The patient underwent a T1–3 laminoplasty and Simpson Grade II excision of the meningioma, followed by instrumentation and fusion. The MR image at 1-year follow-up did not show any recurrence (H). I–L: Case 3. A 41-year-old woman presented with a 3-week history of radicular and myelopathic features. MRI revealed a dumbbell-shaped tumor extending from C-1 to C-4 with vertebral artery encasement (I–K). The patient underwent a C1–4 laminectomy and excision of the tumor, followed by instrumentation and fusion. Simpson Grade III resection was achieved, as portions of tumor remained around the vertebral artery. The MR image at 2-year follow-up did not show any progression (L).

Surgery and Complications

Gross-total resection was achieved in all but 1 patient. The dural attachment was resected in 2 patients (Simpson Grade I resection). In all other cases, the dural attachment was coagulated (Simpson II excision). Apart from 3 tumors, all other meningiomas were WHO Grade I. Among Grade II meningiomas, 2 were atypical and 1 was chordoid subtype.

Four patients had wound complications. Among these 4 patients, 2 had CSF leakage as well.

Recurrence and Survival

The mean follow-up was 51.2 months. One-, 2-, and 5-year follow-up data were available for 29, 25, and 16 patients, respectively. Four patients had tumor recurrence. Three of these patients had WHO Grade I histopathology at initial surgery. The time to recurrence was 36, 40, and 64 months for these 3 Grade I meningiomas. In 1 patient with an atypical meningioma, recurrence was discovered at the 19-month follow-up. The tumor exhibited mild-to-moderate nuclear atypia, a mitotic count of 5–6 per 10 hpf, a high Ki-67 proliferative index (20%–25%), and strong nuclear staining for progesterone receptor in 70% of tumor cells at the first surgery. Two patients did not undergo postoperative MRI at 1 year and were asymptomatic after surgery. They developed recurrence of symptoms after more than 3 years (36 and 64 months) when follow-up imaging revealed a recurrence.

Although male patients had a lower incidence rate overall, they were found to be more prone to recurrence. Among other factors, presence of a dural tail was significantly associated with more recurrences. The details of the analysis are tabulated in Table 3. Kaplan-Meier analyses of statistically significant results are shown in Fig. 2.

TABLE 3.

Prognostic factors for recurrence

VariableStratificationp Value*
Age<50 vs ≥50 yrs0.201
SexMale vs female<0.001
RaceCaucasian vs African American0.745
Association w/NF2NF2 vs non-NF20.605
WHO gradeI vs II0.189
Lesion levelCervical & cervicothoracic vs thoracic0.099
Craniocaudal tumor extension1–2 vs ≥3 levels0.332
Lesion planeVentral & ventrolateral vs dorsal & dorsolateral0.112
Tumor sizeOccupying ≥75% of spinal canal in AP & transverse directions vs <75%0.208
T2 signal intensity changes of spinal cordPresent vs absent0.951
Dural tailPresent vs absent0.04

Boldface type indicates statistical significance.

FIG. 2.
FIG. 2.

Left: Kaplan-Meier analysis showing the difference in recurrence-free survival between male and female patients. Right: Kaplan-Meier analysis showing the difference in recurrence-free survival between patients with or without a dural tail on MRI.

Functional Outcome

The patients' functional status was assessed using the modified McCormick grading system. Patients were considered to have achieved a satisfactory outcome when they had no or minimal deficit (modified McCormick Grade I and II) at 1-year follow-up. In contrast, patients who remained unchanged or had postoperative modified McCormick Grades of III–V were considered as having an unsatisfactory outcome. Although 1 patient experienced transient deterioration after surgery, no patient was clinically worse at 1-year follow-up than at initial presentation.

Regression analysis suggested ventral and ventrolateral location, tumor occupying 75% or more of the spinal canal, T2 hyperintense signal of the spinal cord, and poor preoperative modified McCormick grade were associated with poor functional recovery. The details of the analysis are tabulated in Table 4.

TABLE 4.

Prognostic factors for improvement

VariableStratificationp Value*
Age<50 vs ≥50 yrs0.909
SexMale vs female0.745
RaceCaucasian vs African American0.606
Association w/NF-2NF2 vs non-NF20.557
WHO gradeI vs II0.432
Level of lesionCervical & cervicothoracic vs thoracic0.6
Cranio-caudal extension of the tumor1–2 vs ≥3 levels0.201
Plane of the lesionVentral & ventrolateral vs dorsal & dorsolateral0.003
Tumor sizeOccupying ≥75% of spinal canal in both anteroposterior & transverse direction vs <75%0.02
T2 signal intensity changes of spinal cordPresent vs absent0.022
Dural tailPresent vs absent0.557
Preop MMGIII vs IV & V0.003

Boldface type indicates statistical significance.

Literature Review

The literature review yielded 13 studies in the last 15 years (2001–2015) meeting the aforementioned selection criteria. All of these studies were retrospective. Summaries of these studies are tabulated in Table 5.3–5,9,12,20,29,31,33,39,41,42,50

TABLE 5.

Reports of spinal meningiomas: review of the literature

Authors & YearNo. of PtsAge (yrs)Sex (M/F)Ventral/Ventrolateral Location (%)C, CT, T, TL, LS LevelsWHO Grade I/II/IIIGTR (%)Op Complications (%)Mortality (%)Outcome (improve/intact) (%)Recurrence (%)Mean FU (mos)
Gottfried et al., 200325Mean 601:4.2164, 0, 19, 0, 225/0/0920092423 (1–64)
Cohen-Gadol et al., 200380Mean 50.8 (range 9–89)12:6831.7*24, 0, 55, 0, 280/1/087.613.609013.7582/88
Peker et al., 200541Mean 50 (range 16–73)9:32817, 0, 34, 0, 041/0/0989.70100023.2 (12–120)
Schaller, 200533Mean 63 (range 20–88)3:30ND10, 0, 23, 0, 033/0/085NDND97396 ± 48 (12–172)
Setzer et al., 200780Mean 61.9 ± 16 (range 20–91)22:5858.817, 6, 48, 6, 370/6/49551.293.51043.5 ± 24.8
Yoon et al., 200738Mean 52 (range 19–80)7:31136, 2, 28, 1, 136/0/284.210.55.394.715.873 (16–223)
Sandalcioglu et al., 2008131Mean 69 (range 17–88)17:1143821, 7, 95, 6, 2129/2/09730.896.2360
Boström et al., 200861Mean 61 (range 28–80)11:5021.3ND61/0/098.363.301008.284
Maiuri et al., 2011117Median 59 (range 18–84)30, 877.825, 0, 90, 0, 2115/2/094.9ND0.8ND3.6ND
Postalci et al., 201146Mean 52 (range 17–76)13:3315.24, 0, 39, 0, 344/2/082150911760
Nakamura et al., 201268Mean 56 ± 1712:5655.914, 0, 50, 0, 467/0/191NDNDND9.7144
Iacob, 201432Mean 54.7 (range 34–82)4:2818.75ND32/0/01006.2501006.2524
Arima et al., 201423Mean 60.3 (range 21–84)8:1565.214, 0, 9, 0, 0ND90NDND95.7NDND
Present study38Mean 53.47 ± 20.28 (range 12–92)7:3136.8410, 4, 24, 0, 035/3/097.3710.53010010.5351.2

C = cervical; CT = cervicothoracic; FU = follow-up; GTR = gross-total resection; LS = lumbosacral; ND = no data; Pts = patients; T = thoracic; TL = thoracolumbar.

The distribution is mentioned for the younger cohort of the patients (n = 41) but not for the older group.

The tumors were classified in ventral (7.8%), lateral (both ventrolateral and dorsolateral, 77.7%), and dorsal (14.5%).

Clinicoradiological features of 813 patients (including the present study) were analyzed. The mean age was 56.2 years, and there was significant female preponderance (male/female ratio 1:4). However, patients with NF2 were not included in a few studies, which might have influenced these findings. Thoracic location was approximately 3.3 times more common than cervical location. Meningioma in the lumbar location was an exceedingly rare phenomenon. The incidence of ventral or ventrolateral tumors varied widely (13%–81%). However, tumors exactly ventral to the spinal cord were rare; most tumors had lateral attachment. Spinal meningiomas were predominantly WHO Grade I meningiomas. With advancement of microsurgery and neuromonitoring, a gross-total resection was rarely impossible. A ventral attachment was generally considered as difficult for complete resection, but Peker et al.31 and Setzer et al.42 achieved a good resection rate despite a ventral or ventrolateral location of tumors in more than half of their cases. Operative complications varied from 0% to 15%. CSF leakage, wound complications, and transient deterioration of neurological status were the most common postoperative complications. The most frequent cause of death during the postoperative period was pulmonary embolism. The recurrence rate varied significantly, from 0% to 20% depending on the duration of follow-up. Surgery for spinal meningiomas had a generally favorable outcome. In more than 90% of cases, the patient either improved or at least remained in the same functional grade after surgery.

Discussion

Demographic Features

There are very few population-based reports estimating the incidence of spinal meningiomas.42 A report of a hospital-based population suggested that the incidence varied from 0.5 to 2 per 100,000 persons per year.42 The prevalence seems to be higher, considering the slow progress of these tumors. Spinal meningiomas account for 15%–46% of all primary spinal cord tumors.1,31,36,44 They are less common than their cranial counterparts, accounting for less than 2% of all meningiomas of the central nervous system.33 However, this proportion increases in patients with NF2. For patients with NF2, approximately 10% of meningiomas requiring resection are located in the spine.10,32 Mautner et al. found spinal meningiomas in one-third of patients with NF2.24 The tumor is more prevalent in the elderly population, with a peak incidence between the 6th and 8th decades.42 However, as expected, spinal meningiomas can present earlier in patients with NF2. A strong female predominance is seen in the present study, similar to that in available literature.17,50

The clinical course is often indolent, although the longer duration of symptoms is an independent variable of nonimprovement.42 The clinical symptoms vary depending on tumor location.

Imaging Features

MRI is the diagnostic modality of choice, unless there is any contraindication. Klekamp and Samii noted that the advent of MRI has shortened the time to diagnosis by 6 months.16 Spinal meningiomas are generally isointense to the spinal cord (on both T1- and T2-weighted images) and show enhancement after administration of contrast.42

Spinal meningiomas are more prevalent in the thoracic region. Although meningiomas are often considered to be located ventral to the spinal cord, they are truly ventral in less than 10% of cases;42 most often they are ventrolateral to the cord.42 Tumors are purely dorsal in less than 5% of cases.42

Spinal meningiomas can show a dural tail or linear enhancement of the adjacent dura after gadolinium administration, similar to intracranial meningiomas.2,8 Although a dural tail is not specific to meningiomas, its presence often distinguishes meningiomas from other intradural extramedullary lesions.2 Also, nerve sheath tumors are more commonly hyperintense to the spinal cord than meningiomas on T2-weighted images.30 Intratumoral calcifications are less common than intracranial meningiomas.

Most meningiomas are intradural extramedullary in location. Extradural meningiomas are also known and need to be distinguished from metastases and lymphomas. Extradural en plaque meningiomas are distinct entities and occur most often in young patients, without sex predilection. They may infiltrate surrounding structures, and tissue planes are often obliterated. Complete resection is nearly impossible. They also tend to cause spinal arachnoiditis. An intramedullary location is exceedingly rare for spinal meningiomas. Dumbbell-shaped meningiomas with foraminal extension are also rare.

Spinal meningiomas rarely extend more than 2 levels in the craniocaudal direction. Tumors often occupy more than two-thirds of the spinal canal in the transverse and anteroposterior directions. A hyperintense signal change within the spinal cord on T2-weighted images may also become evident, suggesting chronic compression.

Treatment

The optimum approach to spinal meningiomas depends on the location and extent of the tumors. A 1- or 2-level laminectomy or hemilaminectomy is adequate for most dorsal or dorsolateral tumors. More lateral exposure is required for tumors located ventrolateral or ventral to the cord. A costotransversectomy or partial vertebrectomy may be required to improve exposure and allow for a safer removal. Instrumentation may be required in these cases, especially at the cervicothoracic or thoracolumbar junctional level. Postoperative instability may result in late-onset chronic pain due to asymmetrical load sharing. Misra and Morgan proposed a classification of the surgical corridor to predict the need of instrumentation.27

The goal of surgery is complete and safe resection. Dorsal or dorsolateral lesions are easier to resect. For ventrally located lesions, sequential debulking and dissection may be helpful. Complete resection (Simpson Grades I and II) can be achieved in most cases.12,33 In previous reports, total resection was reported to have been attained in 82% to 100% of cases. However, the need for resection of the dural attachment is controversial. Most authors prefer to coagulate the dural attachment, but wide variability exists. The resection of the dural attachment with suturing of a patch graft has also been advocated. However, on most occasions, dural resection was not attempted when the tumor was located ventrally. A dura-splitting dissection technique may be useful in cases in which the margin of the tumor is excised in continuity with the inner layer of the dura.38 Preservation of the outer layer of the dura minimizes the postresection dural defect, preventing CSF leakage. Surgery for recurrence is difficult because of arachnoid scarring and the lack of a clear plane of dissection.16

Intraoperative ultrasonography has been recommended to localize the tumor. Moreover, it allows the assessment of adequacy of the surgical corridor.27 We found that intraoperative ultrasonography may be especially useful for ventrally located tumors, but it may not be required for dorsal or dorsolateral lesions. The hyperechoic uniform echogenicity without any cystic changes may differentiate meningiomas from nerve sheath tumors based on intraoperative ultrasonography findings, when the preoperative image is equivocal.21,22,27 Intraoperative monitoring (somatosensory evoked potential and/or motor evoked potential) may be useful as well. Whittle et al. suggested that dual monitoring of somatosensory evoked potentials and motor evoked potentials is better than either of them alone.48 However, intraoperative neurophysiology was not used in most of the recent reports. Complete resection without any neurological deterioration was possible even without intraoperative monitoring.

Complications of Surgery

The reported morbidity and mortality rates were low in previous reports of spinal meningiomas. The major cause of death was pulmonary embolism during the postoperative period. CSF leakage and wound complication were the most common surgical complications, occurring in 0%–4% and 0%–6% of cases, respectively.

Histopathology

Most spinal meningiomas are assigned to WHO Grade I. The frequency of WHO Grade II meningiomas is lower in the spine than in the cranium. Setzer et al. found that histopathological grade is an independent predictor of tumor recurrence.42 The WHO grading system for meningiomas was vague prior to 2000. The criteria for designation of atypical meningioma were not uniform in the literature. Setzer et al. reported a recurrence rate of 1.4%, 50%, and 100% for WHO Grade I, II, and III lesions, respectively.42 No correlations have been found between histological subtypes and functional outcome. Maiuri et al. found a higher Ki-67 labeling index in spinal meningiomas with recurrence (p = 0.0001).20

Adjuvant Therapy

The role of adjuvant therapy is controversial for spinal meningiomas. Although initial reports have suggested that CyberKnife frameless stereotactic radiosurgery is a feasible and effective option, it is only used in a few centers. The reports of chemotherapy for spinal meningiomas are limited, and the outcome is not satisfactory. In the present cohort, no patients received chemotherapy or stereotactic radiosurgery.

Tumor Recurrence

The recurrence rate of spinal meningiomas is low. However, the length of follow-up and histological grade of the tumors must be carefully assessed while considering the recurrence of spinal meningiomas.

Generally, spinal meningiomas tend to recur less than intracranial meningiomas. Mirimanoff et al. reported the 5- and 10-year recurrence/progression rates for spinal meningiomas to be 0% and 13%, respectively.26 This incidence was lower than that reported for convexity (3% and 25%), parasagittal (18% and 24%), and sphenoid ridge (34% and 54%) meningiomas.26 In a report of 78 spinal meningiomas, King et al. documented only 1 recurrence 14 years after the initial surgery.15 Levy et al.17 and Solero et al.45 found the recurrence rate to be 3.1% and 6.4%, respectively. Klekamp and Samii16 reported a much higher recurrence: 21% after 1 year and 40.3% after 5 years, clearly distinct from the rest of the reports.

Multiple clinicoradiological factors have been associated with increased recurrence rates. Cohen-Gadol et al.5 reported on younger patients (age < 50 years) with cervical meningiomas; extradural extension and en plaque growth were associated with higher recurrence rates than older patients. Maiuri et al. reported increased recurrence in a younger population as well.20 Klekamp and Samii reported that en plaque or infiltrating meningiomas, arachnoid scarring, and partial resection were significantly associated with increased recurrence.16 The role of resection of the dural attachment is controversial, and contrasting results are available. Nakamura et al. found that the recurrence rate was lower for Simpson Grade I resection than for Simpson Grade II.29 In contrast, King et al. reported a low recurrence rate even when dural resection was not performed.15

Multiple reports suggest that, although meningiomas are more common in females, the incidence of atypical and anaplastic meningiomas is higher in males.14,18 The recurrence rate has also been described as higher for males when all histopathological grades of intracranial meningiomas were considered.13 However, similar observation for spinal meningiomas is not available in the literature, presumably due to fewer reported recurrences. A dural tail can be present in up to half of the cases of spinal meningiomas.2,34 However, their association with recurrence had been rarely evaluated.

Finally, a prolonged follow-up is mandatory as late recurrence is a rule, rather than exception, for these patients.

Functional Outcome

As different functional outcome scales have been described in the literature, a direct comparison is not feasible. The Nurick grade,5 Frankel grade,4,39 or modified Japanese Orthopaedic Association score49 have been used by different authors. The McCormick grade (or modified McCormick grade), although originally used to classify intramedullary tumors, has been used by many authors for assessment of functional outcome.3,35,42 A good outcome is generally described by patients who either improved or remained stable in comparison with their preoperative status. Setzer et al. found that invasion of the arachnoidpia and preoperative McCormick grade were independent predictors of poor long-term outcome.42 Other reports have suggested increased surgical morbidity for meningiomas in ventral locations,7,36,40 en plaque shapes,36 and intratumoral calcifications.36 However, in many of these reports, the study of the radiological factors was incomplete. Tumor size did not influence functional outcome in the report by Schaller.41 We found that larger tumors were associated with poor outcome, similar to Arima et al.3 Presence of a T2 hyperintense signal within the spinal cord generally results from chronic compression in cervical spondylotic myelopathy.47 However, the size of the tumor within the spinal canal and T2 hyperintense signal changes in relation to functional outcome have rarely been studied.3 King et al.15 and Haegelen et al.11 reported significant improvement in their patients with severe preoperative deficit. In contrast, other reports have suggested that severe preoperative neurological impairment is a limiting factor for complete recovery.7,40

Limitations

The study has multiple limitations inherent to retrospective analyses. The operative impression of extent of resection could not be confirmed with postoperative MRI for 9 patients (23.7%). The reported recurrence-free survival could be falsely high in this series, if a clinically silent recurrence develops before it is diagnosed on imaging. We had only 1 patient with radiologically evident calcification and only 2 patients harboring meningioma with foraminal extension. Multiple reports suggest that clear cell meningioma19 and WHO Grade II or III meningiomas46 are prone to recurrence. We did not have a sufficient number of patients with these characteristics. Therefore, no significant analysis could be performed for many risk factors.

Conclusions

Spinal meningiomas can have varied radiological presentations. Young patients with spinal meningiomas should be evaluated for the presence of NF2. Although the incidence is rare in males, they are more likely to experience recurrence. The presence of a dural tail should be carefully analyzed in predicting recurrence. Patients exhibiting a dural tail on imaging need undergo long-duration follow-up, as late recurrence is a known phenomenon. Large tumors with ventral attachment causing spinal cord signal changes are associated with poor functional outcome. Complete resection of meningiomas can result in functional recovery, although prognosis is guarded for those with severe preoperative neurological deficits.

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    Alorainy IA: Dural tail sign in spinal meningiomas. Eur J Radiol 60:3873912006

  • 3

    Arima HTakami TYamagata TNaito KAbe JShimokawa N: Surgical management of spinal meningiomas: A retrospective case analysis based on preoperative surgical grade. Surg Neurol Int 5:Suppl 7S333S3382014

    • Search Google Scholar
    • Export Citation
  • 4

    Boström ABürgel UReinacher PKrings TRohde VGilsbach JM: A less invasive surgical concept for the resection of spinal meningiomas. Acta Neurochir (Wien) 150:5515562008

    • Search Google Scholar
    • Export Citation
  • 5

    Cohen-Gadol AAZikel OMKoch CAScheithauer BWKrauss WE: Spinal meningiomas in patients younger than 50 years of age: a 21-year experience. J Neurosurg 98:3 Suppl2582632003

    • Search Google Scholar
    • Export Citation
  • 6

    De Verdelhan OHaegelen CCarsin-Nicol BRiffaud LAmlashi SFBrassier G: MR imaging features of spinal schwannomas and meningiomas. J Neuroradiol 32:42492005

    • Search Google Scholar
    • Export Citation
  • 7

    Gezen FKahraman SCanakci ZBedük A: Review of 36 cases of spinal cord meningioma. Spine (Phila Pa 1976) 25:7277312000

  • 8

    Goldsher DLitt AWPinto RSBannon KRKricheff II: Dural “tail” associated with meningiomas on Gd-DTPA-enhanced MR images: characteristics, differential diagnostic value, and possible implications for treatment. Radiology 176:4474501990

    • Search Google Scholar
    • Export Citation
  • 9

    Gottfried ONGluf WQuinones-Hinojosa AKan PSchmidt MH: Spinal meningiomas: surgical management and outcome. Neurosurg Focus 14:6e22003

    • Search Google Scholar
    • Export Citation
  • 10

    Goutagny SKalamarides M: Meningiomas and neurofibromatosis. J Neurooncol 99:3413472010

  • 11

    Haegelen CMorandi XRiffaud LAmlashi SFLeray EBrassier G: Results of spinal meningioma surgery in patients with severe preoperative neurological deficits. Eur Spine J 14:4404442005

    • Search Google Scholar
    • Export Citation
  • 12

    Iacob G: Spinal meningiomas. Personal experience and review of literature. Romanian Neurosurgery 21:1461602014

  • 13

    Ildan FErman TGöçer AITuna MBağdatoğlu HCetinalp E: Predicting the probability of meningioma recurrence in the preoperative and early postoperative period: a multivariate analysis in the midterm follow-up. Skull Base 17:1571712007

    • Search Google Scholar
    • Export Citation
  • 14

    Kane AJSughrue MERutkowski MJShangari GFang SMcDermott MW: Anatomic location is a risk factor for atypical and malignant meningiomas. Cancer 117:127212782011

    • Search Google Scholar
    • Export Citation
  • 15

    King ATSharr MMGullan RWBartlett JR: Spinal meningiomas: a 20-year review. Br J Neurosurg 12:5215261998

  • 16

    Klekamp JSamii M: Surgical results for spinal meningiomas. Surg Neurol 52:5525621999

  • 17

    Levy WJ JrBay JDohn D: Spinal cord meningioma. J Neurosurg 57:8048121982

  • 18

    Liang RFXiu YJWang XLi MYang YMao Q: The potential risk factors for atypical and anaplastic meningiomas: clinical series of 1,239 cases. Int J Clin Exp Med 7:569657002014

    • Search Google Scholar
    • Export Citation
  • 19

    Liu PILiu GCTsai KBLin CLHsu JS: Intraspinal clear-cell meningioma: case report and review of literature. Surg Neurol 63:2852892005

    • Search Google Scholar
    • Export Citation
  • 20

    Maiuri FDe Caro MLde Divitiis OVergara PMariniello G: Spinal meningiomas: age-related features. Clin Neurol Neurosurg 113:34382011

    • Search Google Scholar
    • Export Citation
  • 21

    Maiuri FIaconetta Gde Divitiis O: The role of intraoperative sonography in reducing invasiveness during surgery for spinal tumors. Minim Invasive Neurosurg 40:8121997

    • Search Google Scholar
    • Export Citation
  • 22

    Maiuri FIaconetta GGallicchio BStella L: Intraoperative sonography for spinal tumors. Correlations with MR findings and surgery. J Neurosurg Sci 44:1151222000

    • Search Google Scholar
    • Export Citation
  • 23

    Manzano GGreen BAVanni SLevi AD: Contemporary management of adult intramedullary spinal tumors-pathology and neurological outcomes related to surgical resection. Spinal Cord 46:5405462008

    • Search Google Scholar
    • Export Citation
  • 24

    Mautner VFLindenau MBaser MEHazim WTatagiba MHaase W: The neuroimaging and clinical spectrum of neurofibromatosis 2. Neurosurgery 38:8808861996

    • Search Google Scholar
    • Export Citation
  • 25

    McCormick PCTorres RPost KDStein BM: Intramedullary ependymoma of the spinal cord. J Neurosurg 72:5235321990

  • 26

    Mirimanoff RODosoretz DELinggood RMOjemann RGMartuza RL: Meningioma: analysis of recurrence and progression following neurosurgical resection. J Neurosurg 62:18241985

    • Search Google Scholar
    • Export Citation
  • 27

    Misra SNMorgan HW: Avoidance of structural pitfalls in spinal meningioma resection. Neurosurg Focus 14:6e12003

  • 28

    Morandi XHaegelen CRiffaud LAmlashi SAdn MBrassier G: Results in the operative treatment of elderly patients with spinal meningiomas. Spine (Phila Pa 1976) 29:219121942004

    • Search Google Scholar
    • Export Citation
  • 29

    Nakamura MTsuji OFujiyoshi KHosogane NWatanabe KTsuji T: Long-term surgical outcomes of spinal meningiomas. Spine (Phila Pa 1976) 37:E617E6232012

    • Search Google Scholar
    • Export Citation
  • 30

    Parsa ATLee JParney IFWeinstein PMcCormick PCAmes C: Spinal cord and intradural-extraparenchymal spinal tumors: current best care practices and strategies. J Neurooncol 69:2913182004

    • Search Google Scholar
    • Export Citation
  • 31

    Peker SCerçi AOzgen SIsik NKalelioglu MPamir MN: Spinal meningiomas: evaluation of 41 patients. J Neurosurg Sci 49:7112005

    • Search Google Scholar
    • Export Citation
  • 32

    Perry AGiannini CRaghavan RScheithauer BWBanerjee RMargraf L: Aggressive phenotypic and genotypic features in pediatric and NF2-associated meningiomas: a clinicopathologic study of 53 cases. J Neuropathol Exp Neurol 60:99410032001

    • Search Google Scholar
    • Export Citation
  • 33

    Postalci LTugcu BGungor AGuclu G: Spinal meningiomas: recurrence in ventrally located individuals on long-term follow-up; a review of 46 operated cases. Turk Neurosurg 21:4494532011

    • Search Google Scholar
    • Export Citation
  • 34

    Quekel LGVersteege CW: The “dural tail sign” in MRI of spinal meningiomas. J Comput Assist Tomogr 19:8908921995

  • 35

    Riad HKnafo SSegnarbieux FLonjon N: Spinal meningiomas: surgical outcome and literature review. Neurochirurgie 59:30342013

  • 36

    Roux FXNataf FPinaudeau MBorne GDevaux BMeder JF: Intraspinal meningiomas: review of 54 cases with discussion of poor prognosis factors and modern therapeutic management. Surg Neurol 46:4584641996

    • Search Google Scholar
    • Export Citation
  • 37

    Sacko OHaegelen CMendes VBrenner ASesay MBrauge D: Spinal meningioma surgery in elderly patients with paraplegia or severe paraparesis: a multicenter study. Neurosurgery 64:5035102009

    • Search Google Scholar
    • Export Citation
  • 38

    Saito TArizono TMaeda TTerada KIwamoto Y: A novel technique for surgical resection of spinal meningioma. Spine (Phila Pa 1976) 26:180518082001

    • Search Google Scholar
    • Export Citation
  • 39

    Sandalcioglu IEHunold AMüller OBassiouni HStolke DAsgari S: Spinal meningiomas: critical review of 131 surgically treated patients. Eur Spine J 17:103510412008

    • Search Google Scholar
    • Export Citation
  • 40

    Saraceni CHarrop JS: Spinal meningioma: chronicles of contemporary neurosurgical diagnosis and management. Clin Neurol Neurosurg 111:2212262009

    • Search Google Scholar
    • Export Citation
  • 41

    Schaller B: Spinal meningioma: relationship between histological subtypes and surgical outcome?. J Neurooncol 75:1571612005

  • 42

    Setzer MVatter HMarquardt GSeifert VVrionis FD: Management of spinal meningiomas: surgical results and a review of the literature. Neurosurg Focus 23:4E142007

    • Search Google Scholar
    • Export Citation
  • 43

    Simpson D: The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 20:22391957

  • 44

    Slin'ko EIAl-Qashqish II: Intradural ventral and ventrolateral tumors of the spinal cord: surgical treatment and results. Neurosurg Focus 17:1ECP22004

    • Search Google Scholar
    • Export Citation
  • 45

    Solero CLFornari MGiombini SLasio GOliveri GCimino C: Spinal meningiomas: review of 174 operated cases. Neurosurgery 25:1531601989

    • Search Google Scholar
    • Export Citation
  • 46

    Sun SQCai CRavindra VMGamble PYarbrough CKDacey RG: Simpson Grade I–III resection of spinal atypical (World Health Organization Grade II) meningiomas is associated with symptom resolution and low recurrence. Neurosurgery 76:7397462015

    • Search Google Scholar
    • Export Citation
  • 47

    Vedantam ARajshekhar V: Does the type of T2-weighted hyperintensity influence surgical outcome in patients with cervical spondylotic myelopathy? A review. Eur Spine J 22:961062013

    • Search Google Scholar
    • Export Citation
  • 48

    Whittle IRJohnston IHBesser M: Recording of spinal somatosensory evoked potentials for intraoperative spinal cord monitoring. J Neurosurg 64:6016121986

    • Search Google Scholar
    • Export Citation
  • 49

    Wu LYang TDeng XYang CZhao LYao N: Spinal extradural en plaque meningiomas: clinical features and long-term outcomes of 12 cases. J Neurosurg Spine 21:8928982014

    • Search Google Scholar
    • Export Citation
  • 50

    Yoon SHChung CKJahng TA: Surgical outcome of spinal canal meningiomas. J Korean Neurosurg Soc 42:3003042007

Disclosures

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

Author Contributions

Conception and design: Maiti, Bir, Patra, Kalakoti. Acquisition of data: Maiti, Bir, Patra, Kalakoti. Analysis and interpretation of data: Maiti, Bir, Patra, Kalakoti. Drafting the article: Maiti, Bir, Patra, Kalakoti. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Nanda. Statistical analysis: Maiti, Bir, Patra, Kalakoti. Administrative/technical/material support: Nanda. Study supervision: Nanda.

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

INCLUDE WHEN CITING DOI: 10.3171/2016.5.FOCUS16163.

Correspondence Anil Nanda, Department of Neurosurgery, LSU Health-Shreveport, 1501 Kings Hwy., Shreveport, LA 71103-3932. email: ananda@lsuhsc.edu.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    A–D: Case 1. A 76-year-old woman presented with back pain, gait instability, and myelopathic features. MRI revealed an intradural extramedullary lesion at T7–8. The tumor was occupying more than three-fourths of the spinal canal and had a lateral attachment. Postcontrast sagittal (A), coronal (B), and axial (C) images are shown. The patient underwent a T7–8 laminectomy and Simpson Grade II excision of the lesion. The biopsy sample was suggestive of WHO Grade I meningioma. Ki-67 showed positive staining in fewer than 2% of the tumor cells. The MR image obtained at 1-year follow-up (D) did not reveal any recurrence. E–H: Case 2. A 41-year-old man presented with myelopathic features. MRI revealed an intradural extramedullary lesion at T2–3. A dural tail was evident on postcontrast sagittal (E) and axial (F) images (arrows). A hypointense rim of calcification was also evident (F and G, arrowheads). The patient underwent a T1–3 laminoplasty and Simpson Grade II excision of the meningioma, followed by instrumentation and fusion. The MR image at 1-year follow-up did not show any recurrence (H). I–L: Case 3. A 41-year-old woman presented with a 3-week history of radicular and myelopathic features. MRI revealed a dumbbell-shaped tumor extending from C-1 to C-4 with vertebral artery encasement (I–K). The patient underwent a C1–4 laminectomy and excision of the tumor, followed by instrumentation and fusion. Simpson Grade III resection was achieved, as portions of tumor remained around the vertebral artery. The MR image at 2-year follow-up did not show any progression (L).

  • View in gallery

    Left: Kaplan-Meier analysis showing the difference in recurrence-free survival between male and female patients. Right: Kaplan-Meier analysis showing the difference in recurrence-free survival between patients with or without a dural tail on MRI.

References

  • 1

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

  • 2

    Alorainy IA: Dural tail sign in spinal meningiomas. Eur J Radiol 60:3873912006

  • 3

    Arima HTakami TYamagata TNaito KAbe JShimokawa N: Surgical management of spinal meningiomas: A retrospective case analysis based on preoperative surgical grade. Surg Neurol Int 5:Suppl 7S333S3382014

    • Search Google Scholar
    • Export Citation
  • 4

    Boström ABürgel UReinacher PKrings TRohde VGilsbach JM: A less invasive surgical concept for the resection of spinal meningiomas. Acta Neurochir (Wien) 150:5515562008

    • Search Google Scholar
    • Export Citation
  • 5

    Cohen-Gadol AAZikel OMKoch CAScheithauer BWKrauss WE: Spinal meningiomas in patients younger than 50 years of age: a 21-year experience. J Neurosurg 98:3 Suppl2582632003

    • Search Google Scholar
    • Export Citation
  • 6

    De Verdelhan OHaegelen CCarsin-Nicol BRiffaud LAmlashi SFBrassier G: MR imaging features of spinal schwannomas and meningiomas. J Neuroradiol 32:42492005

    • Search Google Scholar
    • Export Citation
  • 7

    Gezen FKahraman SCanakci ZBedük A: Review of 36 cases of spinal cord meningioma. Spine (Phila Pa 1976) 25:7277312000

  • 8

    Goldsher DLitt AWPinto RSBannon KRKricheff II: Dural “tail” associated with meningiomas on Gd-DTPA-enhanced MR images: characteristics, differential diagnostic value, and possible implications for treatment. Radiology 176:4474501990

    • Search Google Scholar
    • Export Citation
  • 9

    Gottfried ONGluf WQuinones-Hinojosa AKan PSchmidt MH: Spinal meningiomas: surgical management and outcome. Neurosurg Focus 14:6e22003

    • Search Google Scholar
    • Export Citation
  • 10

    Goutagny SKalamarides M: Meningiomas and neurofibromatosis. J Neurooncol 99:3413472010

  • 11

    Haegelen CMorandi XRiffaud LAmlashi SFLeray EBrassier G: Results of spinal meningioma surgery in patients with severe preoperative neurological deficits. Eur Spine J 14:4404442005

    • Search Google Scholar
    • Export Citation
  • 12

    Iacob G: Spinal meningiomas. Personal experience and review of literature. Romanian Neurosurgery 21:1461602014

  • 13

    Ildan FErman TGöçer AITuna MBağdatoğlu HCetinalp E: Predicting the probability of meningioma recurrence in the preoperative and early postoperative period: a multivariate analysis in the midterm follow-up. Skull Base 17:1571712007

    • Search Google Scholar
    • Export Citation
  • 14

    Kane AJSughrue MERutkowski MJShangari GFang SMcDermott MW: Anatomic location is a risk factor for atypical and malignant meningiomas. Cancer 117:127212782011

    • Search Google Scholar
    • Export Citation
  • 15

    King ATSharr MMGullan RWBartlett JR: Spinal meningiomas: a 20-year review. Br J Neurosurg 12:5215261998

  • 16

    Klekamp JSamii M: Surgical results for spinal meningiomas. Surg Neurol 52:5525621999

  • 17

    Levy WJ JrBay JDohn D: Spinal cord meningioma. J Neurosurg 57:8048121982

  • 18

    Liang RFXiu YJWang XLi MYang YMao Q: The potential risk factors for atypical and anaplastic meningiomas: clinical series of 1,239 cases. Int J Clin Exp Med 7:569657002014

    • Search Google Scholar
    • Export Citation
  • 19

    Liu PILiu GCTsai KBLin CLHsu JS: Intraspinal clear-cell meningioma: case report and review of literature. Surg Neurol 63:2852892005

    • Search Google Scholar
    • Export Citation
  • 20

    Maiuri FDe Caro MLde Divitiis OVergara PMariniello G: Spinal meningiomas: age-related features. Clin Neurol Neurosurg 113:34382011

    • Search Google Scholar
    • Export Citation
  • 21

    Maiuri FIaconetta Gde Divitiis O: The role of intraoperative sonography in reducing invasiveness during surgery for spinal tumors. Minim Invasive Neurosurg 40:8121997

    • Search Google Scholar
    • Export Citation
  • 22

    Maiuri FIaconetta GGallicchio BStella L: Intraoperative sonography for spinal tumors. Correlations with MR findings and surgery. J Neurosurg Sci 44:1151222000

    • Search Google Scholar
    • Export Citation
  • 23

    Manzano GGreen BAVanni SLevi AD: Contemporary management of adult intramedullary spinal tumors-pathology and neurological outcomes related to surgical resection. Spinal Cord 46:5405462008

    • Search Google Scholar
    • Export Citation
  • 24

    Mautner VFLindenau MBaser MEHazim WTatagiba MHaase W: The neuroimaging and clinical spectrum of neurofibromatosis 2. Neurosurgery 38:8808861996

    • Search Google Scholar
    • Export Citation
  • 25

    McCormick PCTorres RPost KDStein BM: Intramedullary ependymoma of the spinal cord. J Neurosurg 72:5235321990

  • 26

    Mirimanoff RODosoretz DELinggood RMOjemann RGMartuza RL: Meningioma: analysis of recurrence and progression following neurosurgical resection. J Neurosurg 62:18241985

    • Search Google Scholar
    • Export Citation
  • 27

    Misra SNMorgan HW: Avoidance of structural pitfalls in spinal meningioma resection. Neurosurg Focus 14:6e12003

  • 28

    Morandi XHaegelen CRiffaud LAmlashi SAdn MBrassier G: Results in the operative treatment of elderly patients with spinal meningiomas. Spine (Phila Pa 1976) 29:219121942004

    • Search Google Scholar
    • Export Citation
  • 29

    Nakamura MTsuji OFujiyoshi KHosogane NWatanabe KTsuji T: Long-term surgical outcomes of spinal meningiomas. Spine (Phila Pa 1976) 37:E617E6232012

    • Search Google Scholar
    • Export Citation
  • 30

    Parsa ATLee JParney IFWeinstein PMcCormick PCAmes C: Spinal cord and intradural-extraparenchymal spinal tumors: current best care practices and strategies. J Neurooncol 69:2913182004

    • Search Google Scholar
    • Export Citation
  • 31

    Peker SCerçi AOzgen SIsik NKalelioglu MPamir MN: Spinal meningiomas: evaluation of 41 patients. J Neurosurg Sci 49:7112005

    • Search Google Scholar
    • Export Citation
  • 32

    Perry AGiannini CRaghavan RScheithauer BWBanerjee RMargraf L: Aggressive phenotypic and genotypic features in pediatric and NF2-associated meningiomas: a clinicopathologic study of 53 cases. J Neuropathol Exp Neurol 60:99410032001

    • Search Google Scholar
    • Export Citation
  • 33

    Postalci LTugcu BGungor AGuclu G: Spinal meningiomas: recurrence in ventrally located individuals on long-term follow-up; a review of 46 operated cases. Turk Neurosurg 21:4494532011

    • Search Google Scholar
    • Export Citation
  • 34

    Quekel LGVersteege CW: The “dural tail sign” in MRI of spinal meningiomas. J Comput Assist Tomogr 19:8908921995

  • 35

    Riad HKnafo SSegnarbieux FLonjon N: Spinal meningiomas: surgical outcome and literature review. Neurochirurgie 59:30342013

  • 36

    Roux FXNataf FPinaudeau MBorne GDevaux BMeder JF: Intraspinal meningiomas: review of 54 cases with discussion of poor prognosis factors and modern therapeutic management. Surg Neurol 46:4584641996

    • Search Google Scholar
    • Export Citation
  • 37

    Sacko OHaegelen CMendes VBrenner ASesay MBrauge D: Spinal meningioma surgery in elderly patients with paraplegia or severe paraparesis: a multicenter study. Neurosurgery 64:5035102009

    • Search Google Scholar
    • Export Citation
  • 38

    Saito TArizono TMaeda TTerada KIwamoto Y: A novel technique for surgical resection of spinal meningioma. Spine (Phila Pa 1976) 26:180518082001

    • Search Google Scholar
    • Export Citation
  • 39

    Sandalcioglu IEHunold AMüller OBassiouni HStolke DAsgari S: Spinal meningiomas: critical review of 131 surgically treated patients. Eur Spine J 17:103510412008

    • Search Google Scholar
    • Export Citation
  • 40

    Saraceni CHarrop JS: Spinal meningioma: chronicles of contemporary neurosurgical diagnosis and management. Clin Neurol Neurosurg 111:2212262009

    • Search Google Scholar
    • Export Citation
  • 41

    Schaller B: Spinal meningioma: relationship between histological subtypes and surgical outcome?. J Neurooncol 75:1571612005

  • 42

    Setzer MVatter HMarquardt GSeifert VVrionis FD: Management of spinal meningiomas: surgical results and a review of the literature. Neurosurg Focus 23:4E142007

    • Search Google Scholar
    • Export Citation
  • 43

    Simpson D: The recurrence of intracranial meningiomas after surgical treatment. J Neurol Neurosurg Psychiatry 20:22391957

  • 44

    Slin'ko EIAl-Qashqish II: Intradural ventral and ventrolateral tumors of the spinal cord: surgical treatment and results. Neurosurg Focus 17:1ECP22004

    • Search Google Scholar
    • Export Citation
  • 45

    Solero CLFornari MGiombini SLasio GOliveri GCimino C: Spinal meningiomas: review of 174 operated cases. Neurosurgery 25:1531601989

    • Search Google Scholar
    • Export Citation
  • 46

    Sun SQCai CRavindra VMGamble PYarbrough CKDacey RG: Simpson Grade I–III resection of spinal atypical (World Health Organization Grade II) meningiomas is associated with symptom resolution and low recurrence. Neurosurgery 76:7397462015

    • Search Google Scholar
    • Export Citation
  • 47

    Vedantam ARajshekhar V: Does the type of T2-weighted hyperintensity influence surgical outcome in patients with cervical spondylotic myelopathy? A review. Eur Spine J 22:961062013

    • Search Google Scholar
    • Export Citation
  • 48

    Whittle IRJohnston IHBesser M: Recording of spinal somatosensory evoked potentials for intraoperative spinal cord monitoring. J Neurosurg 64:6016121986

    • Search Google Scholar
    • Export Citation
  • 49

    Wu LYang TDeng XYang CZhao LYao N: Spinal extradural en plaque meningiomas: clinical features and long-term outcomes of 12 cases. J Neurosurg Spine 21:8928982014

    • Search Google Scholar
    • Export Citation
  • 50

    Yoon SHChung CKJahng TA: Surgical outcome of spinal canal meningiomas. J Korean Neurosurg Soc 42:3003042007

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