Journal of Clinical Neuroscience 19 (2012) 262–266

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Journal of Clinical Neuroscience

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Clinical Study

Clinical presentation and outcome of patients with intradural spinal cord tumours

Mithun Nambiar a, Bhadrakant Kavar a,b,⇑a Department of Surgery (RMH), The University of Melbourne, Parkville, Victoria 3050, Australiab Department of Neurosurgery, The Royal Melbourne Hospital, Grattan Street, Parkville, Victoria 3050, Australia

a r t i c l e i n f o

Article history:Received 27 March 2011Accepted 10 May 2011

Keywords:IntraduralOutcomePresentationSpinal cordSurgeryTumour

0967-5868/$ - see front matter Crown Copyright � 2doi:10.1016/j.jocn.2011.05.021

⇑ Corresponding author. Tel.: +61 3 9342 8219.E-mail address: bhadu.kavar@mh.org.au (B. Kavar)

a b s t r a c t

We aimed to retrospectively investigate the clinical presentation and outcome of surgical intervention ofpatients with intradural spinal cord tumours (IDSCT), and to assess the predictors of surgical outcome. Atotal of 109 patients with IDSCT (57 males and 52 females) (130 admissions; mean age, 45.9 years; range,14–89 years) underwent surgery between 1 January 1994 and 30 June 2009 at The Royal Melbourne Hos-pital. Ninety per cent of tumours were classified as low grade. Pain was the most common symptom atpresentation (60%) and the mean duration of symptoms was 37.8 weeks (0–4 years). Total resection wasachieved in 72.3% of patients with IDSCT. An extramedullary location was the strongest predictor ofgreater extent of tumour resection (odds ratio [OR] = 4.367, 95% confidence interval [CI] = 1.876–10.204, p = 0.001), whereas a rostral location was also a significant predictor of greater resection(OR = 1.393, 95% CI = 1.014–1.908, p = 0.040). The surgical mortality rate was 0.92%. A good pre-operativeclinical grade was the strongest predictor of a positive post-operative neurological status at discharge forIDSCT (OR = 7.382, 95% CI = 4.575–11.912, p < 0.001). The mean follow-up was 37.9 months (16 days–165 months). A good post-operative clinical grade was the most significant predictor of a positive neuro-logical outcome at short-term follow-up (OR = 9.953, 95% CI = 4.941–20.051, p < 0.001), while a goodpre-morbid clinical grade was the most significant predictor of a positive outcome at long-termfollow-up (OR = 9.498, 95% CI = 2.780–32.451, p < 0.001). We concluded that surgical outcome was influ-enced by pre-morbid, pre-operative and post-operative clinical grades, the extent of resection, tumourgrade and tumour location with respect to the spinal parenchyma. Surgical intervention has a high suc-cess rate for tumour control and we recommend total resection where possible.

Crown Copyright � 2011 Published by Elsevier Ltd. All rights reserved.

1. Introduction

Intradural spinal cord tumours (IDSCT) can be classified asbeing either extramedullary (EMSCT) or intramedullary (IMSCT),with IMSCT accounting for 16% to 20% of IDSCT.1,2 IMSCT existwithin the spinal parenchyma, while EMSCT are outside the paren-chyma but within the dural sheath.

In June 1887, Mr (later Sir) Victor Horsley performed the firstresection of an IDSCT, successfully excising a benign extramedul-lary fibromyxoma.3 This pioneering procedure established surgeryas a primary mode of treatment for this rare condition. Since then,advancements in surgical techniques and equipment, such as thebipolar cautery and ultrasonic aspirator, have continued to changemanagement and improve the post-operative outcome in patients.

This study investigates the clinical presentation of patients withIDSCT, and assesses the predictors of neurological outcome aftersurgical intervention.

011 Published by Elsevier Ltd. All

.

2. Methods

2.1. Study design

This retrospective study was carried out at The Royal Mel-bourne Hospital, a tertiary metropolitan hospital that is a majorreferral centre for patients with IDSCT in Victoria. The records of109 patients (130 admissions) who had undergone surgery for IDS-CT between 1 January 1994 and 30 June 2009 were studied toinvestigate the clinical presentation and outcome of patients aftersurgery.

2.2. Patient selection

Patients who had undergone surgery for IDSCT were identifiedfrom the hospital and neurosurgery department databases. Pa-tients who had been treated surgically for cavernous haemangio-mas, arteriovenous fistulas and arteriovenous malformationswere excluded.

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Table 1Clinical/functional classification scheme of neurological functiona

McCormickgrade

Description*

I Neurologically normal; mild focal deficit not significantlyaffecting function of involved limb; mild spasticity or reflexabnormality; normal gait

II Presence of sensorimotor deficit affecting function of involvedlimb; mild to moderate gait difficulty; severe pain ordysesthetic syndrome impairing patient’s quality of life; stillfunctions and ambulates independently

III More severe neurological deficit; requires cane/brace forambulation or significant bilateral upper extremityimpairment; may or may not function independently

IV Severe deficit; requires wheelchair or cane/brace withbilateral upper extremity impairment; usually notindependent

* In our study, patients who were completely neurologically normal with nodeficits were classified as grade 0, rather than grade 1.

a Table reprinted with the kind permission of the American Association of Neu-rosurgeons, from McCormick PC, Torres R, Post KD, Stein BM. Intramedullaryependymoma of the spinal cord. J Neurosurg 1990;72:523–32.

Table 2Histopathology and medullary location of intradural spinal cord tumours for 130admissions (109 patients)

Histopathology IMSCT EMSCT Total

Astrocytoma 6 – 6Ependymoma 23 11 34Haemangioblastoma 2 3 5Haemangiopericytoma – 2 2Intraneural perineuroma – 1 1Meningioma – 45 45Metastasis 2 1 3Neurofibroma – 9 9Oligoastrocytoma – 1 1Paraganglioma 1 – 1Schwannoma – 22 22PNET – 1 1

Total 34 96 130

EMSCT = extramedullary spinal cord tumour, IMSCT = intradural spinal cordtumour, PNET = primitive neuroectodermal tumour.

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2.3. Data collection

Patient records were studied retrospectively to collect informa-tion regarding patient admission, pre-morbid status, symptoms atpresentation, tumour resection score (biopsy, partial, subtotal ortotal), and surgical outcomes. According to the World Health Orga-nisation (WHO) classification of CNS tumours,4 grade 1 and 2 tu-mours were considered as low-grade, while grade 3 and 4tumours were high-grade. Each recorded admission involved sur-gery for the IDSCT. Primary tumours were those not preceded byneoplasms of the same histopathological subtype. Secondary tu-mours represented a recurrence, seeding or metastasis. A recur-rence has been defined as a secondary tumour that re-occurs inthe same location as the primary tumour, or the further growthof an IDSCT after surgery, while seeding involves the spread of a tu-mour through the cerebrospinal fluid (CSF) from the cranial to thespinal region, or from one spinal region to another.

Only symptoms that were directly attributable to the IDSCTwere classified as presenting symptoms. In patients with recur-rences, only new or worsening symptoms were classified as pre-senting symptoms for the next admission.

The McCormick grade5 of neurological function (Table 1) wasused to determine the pre-morbid and pre-operative status as wellas outcome at discharge (post-operative), short-term and long-term follow-up after discharge. Short-term follow-up was definedas 0–12 months after discharge, while long-term follow-up re-ferred to 12–36 months after discharge.

After surgery, an improvement in status was defined as a de-crease of at least one McCormick grade, whereas deteriorationwas represented by an increase of at least one grade. Recovery re-ferred to a McCormick grade of 0 after surgery, and implies that thepre-operative status was not 0.

Surgical mortality referred to death from any cause within30 days of surgery, whereas the IDSCT mortality rate referred topatients who had died as a result of IDSCT progression.

Fig. 1. A photograph of a 15-year-old male showing muscle atrophy as a result of aC1–C3 tancytic ependymoma. (This figure is available in colour atwww.sciencedirect.com.)

2.4. Statistical analysis

A univariate analysis was used to help identify variables formultivariate analysis. Backward stepwise logistic regression andordinal logistic regression were used for multivariate analyses ofdichotomous and ordinal variables respectively.

3. Results

3.1. Study population

A total of 109 patients (57 male, 52.3%; 52 female, 47.7%), whocomprised 130 admissions (96 for EMSCT resections, 73.8%; 34 forIMSCT, 26.2%) were included. The overall mean age at admissionwas 45.9 years (range, 14–89 years).

3.2. Histopathology

Tumour histopathology and location with respect to the spinalparenchyma is detailed in Table 2. Meningiomas (34.6%), ependy-momas (26.2%) and nerve sheath tumours (NST – schwannomasand neurofibromas) (23.8%) were the most prevalent histopatholo-gical subtypes. Furthermore, tumours such as ependymomas,haemangioblastomas and tumour metastases presented as eitherEMSCT or IMSCT (Fig. 1).

The tumour grade for each tumour subtype is included in Ta-ble 3. Most (90%) of the tumours were low grade, while one patienthad an astrocytoma of unknown grade. The three metastatic tu-mours were from lung, melanoma and rectal primarymalignancies.

Table 3Grade of intradural spinal cord tumours for 130 admissions (109 patients)

Tumour type Tumour grade

Low (n [%]) High (n [%])

EMSCT 89 (92.7) 7 (7.3)IMSCT* 28 (82.4) 5 (14.7)Overall* 117 (90) 12 (9.2)Subtypes

Astrocytoma* 3 (50) 2 (33.3)Ependymoma 33 (97.1) 1 (2.9)Haemangioblastoma 5 (100) –Haemangiopericytoma 1 (50) 1 (50)Intraneural perineuroma 1 (100) –Meningioma 42 (93.3) 3 (6.7)Metastasis – 3 (100)Neurofibroma 9 (100) –Oligoastrocytoma 1 (100) –Paraganglioma 1 (100) –Schwannoma 21 (95.5) 1 (4.5)PNET – 1 (100)

EMSCT = extramedullary spinal cord tumour, IMSCT = intradural spinal cordtumour, PNET = primitive neuroectodermal tumour.

* One patient with an astrocytoma had an unknown tumour grade.

264 M. Nambiar, B. Kavar / Journal of Clinical Neuroscience 19 (2012) 262–266

3.3. Clinical presentation

The mean duration of symptoms before presentation for pa-tients with IDSCT was 37.8 weeks (range, 0–4 years). Those withIMSCT had a mean duration of symptoms of 52.5 weeks (range,0–3 years) compared to those with EMSCT of 32.5 weeks (range,0–4 years). In particular, patients with meningioma had a meanduration of symptoms of 26.8 weeks (range, 0–120 weeks).

Pain was the most common symptom at presentation amongpatients with IDSCT (60%) as well as IMSCT (73.5%) and EMSCT(55.2%). Other symptoms at presentation are detailed in Table 4.Pain was also the most common earliest symptom, being the firstsymptom in 70 (53.8%) admissions.

The grades (Table 1) of the 130 admissions were: eight withgrade 0 (6.2%); 41 with grade 1 (31.5%); 43 with grade 2 (33.1%);23 with grade 3 (17.7%); and 15 with grade 4 (11.5%). EMSCTadmissions, and in particular 22 (48.9%) admissions with meningi-oma, had a preoperative McCormick grade of 3 or 4, compared toeight (23.5%) admissions for IMSCT.

The thoracic region was the most common site of IDSCT (44.6%),followed by the cervical region (20%), lumbar region (20%), cervico-thoracic region (7.7%) and thoracolumbar region (7.7%). Although

Table 4Symptoms of 109 patients (130 admissions) with intradural spinal cord tumours(IDSCT) at presentation

IDSCT (n = 130)(n [%])

EMSCT (n = 96)(n [%])

IMSCT (n = 34)(n [%])

Pain 78 (60.0) 53 (55.2) 25 (73.5)Parasthaesia 65 (50.0) 49 (51) 16 (47.1)Mobility dysfunction 59 (45.4) 45 (46.9) 14 (41.2)

Mild/moderate gaitdisturbance

24 (18.5) 18 (18.8) 6 (17.6)

Ambulates with aid 20 (15.4) 16 (16.7) 4 (11.8)Unable to ambulate 15 (11.5) 11 (11.5) 4 (11.8)

Weakness 51 (39.2) 36 (37.5) 15 (44.1)Urinary dysfunction 30 (23.1) 22 (22.9) 8 (23.5)Falls 14 (10.8) 12 (12.5) 2 (5.9)Bowel dysfunction 11 (8.5) 8 (8.3) 3 (8.8)Stiffness 6 (4.6) 3 (3.1) 3 (8.8)Headache/nausea/

vomiting5 (3.8) 3 (3.1) 2 (5.9)

Sexual dysfunction 2 (1.5) 1 (1.0) 1 (2.9)No (new) symptoms 15 (11.5) 12 (12.5) 3 (8.8)

EMSCT = extramedullary spinal cord tumour, IMSCT = intradural spinal cordtumour.

34 of 45 meningiomas (75.6%) were found in the thoracic region,the lumbar region was the most common site for ependymomas(38.2%), followed by the thoracic region (26.5%).

3.4. Surgery

Total resection was achieved in 94 of 130 (72.3%) tumours.EMSCT were more amenable to total surgical resection (80.2%),compared to IMSCT (50%). By tumour type: 95.5% of schwannomaswere completely resected, except for one malignant neuroepithe-lial schwannoma that was partially resected; 84.4% of meningio-mas were totally resected, compared to 50% of ependymomas;77.8% of neurofibromas were completely resected, compared tolow grade astrocytoma where total resection was achieved in onlyone. Five biopsies (3.8%) were performed: one of a high gradeastrocytoma; one of a low grade astrocytoma; two of ependymo-mas; and one of a low grade oligoastrocytoma.

Extramedullary tumour location was the strongest predictor ofa greater extent of tumour resection (OR = 4.367, 95% CI = 1.876–10.204, p = 0.001), while rostral tumour location was also a signif-icant predictor of a greater extent of resection (OR = 1.393, 95%CI = 1.014–1.908, p = 0.040).

3.5. Post-operative outcome

At discharge, 11 (8.5%) admissions had resulted in recovery. Therecovery rate was highest for NST (16.1%), followed by ependymo-mas (8.8%) and meningiomas (6.7%). Further improvement wasseen in 11 NST (35.5%), 23 meningiomas (51.1%) and seven epend-ymomas (20.6%). Seven admissions with IMSCT (20.6%) resulted indeterioration before discharge, compared to eight EMSCT admis-sions (8.3%).

A low pre-operative McCormick grade was the most significantpredictor of a positive post-operative neurological outcome at dis-charge (OR = 7.382, 95% CI = 4.575–11.912, p < 0.001). Other signif-icant predictors of good neurological outcome included lowtumour grade (OR = 6.080, 95% CI = 1.753–21.093, p = 0.004) andextramedullary tumour location (OR = 3.516, 95% CI = 1.537–8.043, p = 0.003).

3.6. Adjuvant therapy

A total of 20 admissions (15.4%) had radiotherapy after surgery,while six (4.6%) underwent chemotherapy. All patients who under-went chemotherapy had also undergone radiotherapy.

Radiotherapy was implemented for four astrocytomas, 12ependymomas, one meningioma, one metastasis from a mela-noma, one oligoastrocytoma and one primitive neuroectodermaltumour (PNET). Chemotherapy was administered to two admis-sions with astrocytomas, two with ependymomas, one with ananaplastic meningioma and one with a PNET.

3.7. Complications

The surgical mortality rate was 0.92%, due to the death of onepatient who had metastatic disease from a primary lung carci-noma, and who died of an unspecified cause 16 days afterdischarge.

Complications before discharge included five patients with uri-nary tract infections, three with dural CSF leakages, two with hae-matomas, two with pneumonia, two with wound infections, onewith a pseudomeningocoele and stroke. In 28 admissions (21.5%),new symptoms, many of which were transient and did not influ-ence the McCormick grade, developed post-operatively. In ninepatients (6.9%) the symptoms evident pre-operatively becameworse after surgery. After discharge, readmissions were required

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for the following further surgical complications: two dural CSFleakages, two meningocoeles, two wound infections and the devel-opment of a pseudomeningocoele.

3.8. Follow-up

Thirty-one admissions (23.8%) were lost to follow-up. The meanfollow-up duration was 37.9 months (16 days–165 months). Over-all, eight patients (7.3%) died during follow-up, which includeddeath from unrelated causes. The IDSCT mortality rate due to tu-mour progression was 0.92%, which was attributed to one patientwho died of an infiltrative astrocytoma 10 months after surgery(Fig. 2).

Short-term follow-up, up to 12 months after discharge, wasavailable for 93 admissions (68 with EMSCT and 25 with IMSCT)(71.5%). Fifteen patients with EMSCT (22.1%) recovered in the shortterm, compared to three patients with IMSCT (12%). Five patientswith IMSCT (20%) deteriorated compared to two patients withEMSCT (2.9%).

A good post-operative McCormick grade was the most signifi-cant predictor of positive neurological outcome at short-term fol-low-up (OR = 9.953, 95% CI = 4.941–20.051, p < 0.001). A greaterextent of tumour resection was also a significant predictor of goodneurological outcome in this period (OR = 4.132, 95% CI = 1.855–9.259, p = 0.001), while a secondary tumour was a significant pre-dictor of worse neurological outcome (OR = 4.821, 95% CI = 1.243–18.696, p = 0.023).

Sixty-one admissions (46 with EMSCT and 15 with IMSCT)(46.9%) had long-term follow-up information available (12–36 months post-discharge), Thirteen patients with EMSCT (28.3%)had recovered at long-term follow-up, compared to one with IMS-CT (6.7%). One admission with EMSCT (2.2%) deteriorated com-pared to two (13.3%) with IMSCT.

A good pre-morbid McCormick grade was the most significantpredictor of a positive neurological outcome at long-term follow-up (OR = 9.498, 95% CI = 2.780–32.451, p < 0.001), while a goodpost-operative grade was also a significant predictor of a positiveneurological outcome (OR = 5.443, 95% CI = 2.319–12.777,p < 0.001).

3.9. Recurrence

The tumour recurred in 12 patients (11.0%) during the study, inwhom surgery was performed for seven patients (6.4%), and

Fig. 2. Sagittal post-contrast T1-weighted MRI of the thoracic spine from a 23-year-old male patient showing a T5–T8 intramedullary astrocytoma.

recurrence was noted on imaging findings but surgery not per-formed for five patients (4.6%). Of the patients with a recurrence,one patient also had surgery for a seeded tumour. A further two pa-tients (1.8%) had surgery for secondary tumours that had seeded.

4. Discussion

4.1. Clinical presentation

The symptoms of IDSCT are due to spinal cord compression, andinclude pain and sensorimotor disturbances as well as sphincterdysfunction.6 Pain was the most common symptom at presenta-tion for IDSCT in our series, which was also noted in Jenkinsonet al.7 Bowel dysfunction and sexual dysfunction were only notedin 11 (8.5%) and two (1.5%) admissions respectively, and thismay be underestimated, due to the difficulty in determining thesesymptoms.

We report a mean symptom duration before presentation of32.5 weeks for EMSCT and 52.5 weeks for IMSCT. The Jenkinsonet al.7 study noted a mean symptom duration for EMSCT of17 months and IMSCT of 20 months. The El-Mahdy et al.8 studyof EMSCT found a mean symptom duration of 30 months, whilethe Manzano et al.9 study of IMSCT found a mean symptom dura-tion of 25.3 months. In particular, for meningiomas we found amean symptom duration of 26.8 weeks, which was less than the9.5 months to 23 months noted in the literature.10–16 Older studies,such as Levy et al.12 which reports a mean duration of symptomsprior to diagnosis of 23 months, have longer time to diagnosiscompared to recent studies, which cite a mean duration of symp-toms of 9.5 months to 13.7 months.10,15,16 This suggests thatadvancements in imaging and tumour detection have shortenedthe symptomatic duration of patients before admission by aidingearlier diagnosis. Furthermore, secondary tumours are now oftendetected early, due to the periodic follow-up of patients after theinitial primary tumour resection, and therefore had a shortersymptomatic period, which further contributes to the overallshorter symptom duration before admission.

4.2. Resection

Rostral and extramedullary tumour locations were significantpredictors of a greater extent of tumour resection in IDSCT. Thisis able to be partly explained by the predisposition of meningio-mas, which are extramedullary tumours amenable to total resec-tion, to appear in the thoracic and cervical regions of the cord.Furthermore, ependymomas, which commonly occurred in thecaudal region were not always amenable to total resection, whichwas also noted in Chang et al.17 where only 40% of conus ependy-momas were totally resectable compared to 97% of tumours inother regions.17

4.3. Outcome of surgery

The division of the follow-up into short-term and long-termperiods aimed to investigate the progressive outcome of patients.Unfortunately, the loss of patients to follow-up meant that certainsignificant predictors of patient outcome may have been deemedto be non-significant.

Multivariate analysis yielded extramedullary location to be asignificant predictor of good post-operative outcome at dischargefor IDSCT (OR = 3.516, 95% CI = 1.537–8.043, p = 0.003). This isdue to the less invasive procedures required to surgically removeEMSCT compared to IMSCT, thus leading to a better post-operativeoutcome.

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A good pre-operative status was a significant predictor of a po-sitive outcome at discharge, which was also noted by previousauthors.15,18,19 We agree with the hypothesis of Epstein et al.19

that, particularly in IMSCT, worse post-operative outcome in pa-tients with large, long-standing tumours may be attributed to thin-ning of the spinal parenchyma.

Although 48.9% of meningioma admissions had a pre-operativeMcCormick grade of 3 or 4, 57.8% of admissions resulted in animprovement or total neurological recovery at discharge, whichwas better than all other tumour types. Similarly, Sacko et al.16

in a series of 102 elderly patients with meningioma with severepre-operative neurological dysfunction, found that 72.5% of pa-tients had improved at discharge. Hence, patients with meningio-mas, though presenting with marked neurological dysfunction,have a relatively high rate of total neurological recovery.

The mortality rate due to progression of the IDSCT was under-standably low, at 0.92%. However, only a total of eight patientswere noted to have died from any cause within the follow-up per-iod and this may be less than the true value, given the loss of pa-tients to follow-up.

The overall 11.0% recurrence rate in our study is similar to the10.4% recurrence rate noted in Jenkinson et al.7 However, wemay have underestimated the overall recurrence rate due to theunavailability of many follow-up and imaging reports. Our studyalso had a strict definition of ‘‘recurrence’’, in contrast to ‘‘seeding’’.

Adjuvant therapy administration was not significantly associ-ated with any post-operative or follow-up outcomes. With only20 admissions (15.4%) involving adjuvant therapy, there wereinsufficient data to properly assess the benefits of such therapy.

4.4. Future directions

Given the rarity of IDSCT, multicentre approaches would allowfor the study of a greater number of patients. Particular tumoursubtypes, such as astrocytomas and other glial tumours, requirefurther study, since the literature regarding the outcomes of sur-gery and adjuvant therapy for such tumours is sparse, and opinionis divided regarding the guidelines for treatment. Randomised con-trol trials may be important to determine the effectiveness of adju-vant therapy in the treatment of IDSCT.

5. Conclusion

Despite their rarity, IDSCT often present with common clinicalsymptoms of pain, sensorimotor deficits and sphincter

dysfunction, and must therefore be considered in patients whopresent with these symptoms in clinical practice. Although IDSCTare a rare source of mortality, they are a significant cause ofmorbidity. Outcomes are influenced by pre-morbid, pre-operativeand post-operative clinical grades, extent of resection, tumourgrade and location with respect to the spinal parenchyma. Surgicalintervention has a high success rate for tumour control and werecommend total resection of tumours where possible.

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