Intramedullary spinal cord metastases: an increasingly common diagnosis

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OBJECT

Intramedullary spinal cord metastases (ISCM) represent a small proportion of intramedullary tumors. However, with the lifespans of patients with malignant tumors increasing, incidents of ISCM are on the rise. Due to threateningly severe disabilities in patients, accompanied by limited life expectancy, every attempt should be made to treat these tumors the same way as metastases elsewhere in the CNS, with the goal of complete removal of the ISCM and preservation of neurological functions. The object of this study is to retrospectively analyze the experiences of 22 patients who were surgically treated for ISCM over a 22-year period.

METHODS

Hospital charts of 22 patients, who were surgically treated for ISCM between 1992 and 2014, were reviewed retrospectively. Demographic data, histopathological diagnoses of primary cancer, chronological sequence of the disease, and neurological status using the simplified McCormick functional classification were collected and reanalyzed.

RESULTS

The most frequent histology was metastasis of lung cancer, followed by brain and breast cancers. The time span from primary cancer diagnosis to the development of symptomatic spinal metastases ranged from 0 to 285 months, with a mean interval of 38 months. The leading presenting sign was dysesthesia (77% of the population), followed by paresis (68%). Only 5 patients (23%) showed urinary retention. Initial performance status represented by the McCormick Scale was on average 2.47. Total or near-total removal was achieved in 87% of cases. Compared with the clinical status 1−2 days after surgery, there was an improvement in the McCormick Scale grade at the last follow-up from 2.47 to 2.12 (p = 0.009). Likewise, an improvement was detected when comparing the preoperative status with the last follow-up (from 2.45 to 2.12; p = 0.029). The mean survival time after surgery was 11.6 months.

CONCLUSIONS

These results suggest that surgery for intramedullary metastases—with all of the challenges of a rare and potentially risky procedure—can be beneficial to patients with advanced stages of cancer. Surgery can be performed with minimal new morbidity and results in maintaining neurological performance status.

ABBREVIATIONSCUP = cancer of unknown primary; CUSA = Cavitron ultrasonic surgical aspirator; IOM = intraoperative monitoring; ISCM = intramedullary spinal cord metastases.

Abstract

OBJECT

Intramedullary spinal cord metastases (ISCM) represent a small proportion of intramedullary tumors. However, with the lifespans of patients with malignant tumors increasing, incidents of ISCM are on the rise. Due to threateningly severe disabilities in patients, accompanied by limited life expectancy, every attempt should be made to treat these tumors the same way as metastases elsewhere in the CNS, with the goal of complete removal of the ISCM and preservation of neurological functions. The object of this study is to retrospectively analyze the experiences of 22 patients who were surgically treated for ISCM over a 22-year period.

METHODS

Hospital charts of 22 patients, who were surgically treated for ISCM between 1992 and 2014, were reviewed retrospectively. Demographic data, histopathological diagnoses of primary cancer, chronological sequence of the disease, and neurological status using the simplified McCormick functional classification were collected and reanalyzed.

RESULTS

The most frequent histology was metastasis of lung cancer, followed by brain and breast cancers. The time span from primary cancer diagnosis to the development of symptomatic spinal metastases ranged from 0 to 285 months, with a mean interval of 38 months. The leading presenting sign was dysesthesia (77% of the population), followed by paresis (68%). Only 5 patients (23%) showed urinary retention. Initial performance status represented by the McCormick Scale was on average 2.47. Total or near-total removal was achieved in 87% of cases. Compared with the clinical status 1−2 days after surgery, there was an improvement in the McCormick Scale grade at the last follow-up from 2.47 to 2.12 (p = 0.009). Likewise, an improvement was detected when comparing the preoperative status with the last follow-up (from 2.45 to 2.12; p = 0.029). The mean survival time after surgery was 11.6 months.

CONCLUSIONS

These results suggest that surgery for intramedullary metastases—with all of the challenges of a rare and potentially risky procedure—can be beneficial to patients with advanced stages of cancer. Surgery can be performed with minimal new morbidity and results in maintaining neurological performance status.

Development of intramedullary spinal cord metastases (ISCM) is still a rare event in the course of malignant diseases. However, it is on the rise due to more effective therapies that result in the prolongation of survival.8 This is reflected in the volume of recently published case reports and small series of ISCM.6,20,22,23,29,30,42,46 Autopsy studies demonstrated an incidence of ISCM up to 2%. Few ISCM are symptomatic and therefore not diagnosed.51 Because of the low frequency of treated cases, therapy standards are still to be defined.

The main goal in treating ISCM is to maintain mobility and neurological functions for patients with limited life expectancy. Surgery is favored but is still second to primarily anti-edematous systemic therapy combined with or followed by radiation. However, the clinical benefit hereby achieved is often very limited and at the level of palliation is associated with considerable side effects, particularly from continuous steroid application.4,17 Reports of surgical removal of ISCM have become more frequent, however, with a wide range of neurological results.3–5,45 In 397 patients with intramedullary lesions who underwent surgical treatment, a strategy of maximal removal was pursued. Of these 397 patients, the clinical findings in our cohort of 22 patients will be reviewed.

Methods

This study is a retrospective analysis of data from 22 patients who were surgically treated for ISCM. Hospital data collected over a period of 22 years (1992−2014), both at the time of treatment and at follow-up where available, were used. Six patients were treated before 2005, and 16 between 2006 and 2014, 15 of them within the last 4 years of the range, indicating a trend of higher incidence. The mean age of the patients was 55 years. No pediatric patients were included. Imaging was based on MRI in T1-and T2-weighted images with and without gadolinium in sagittal, axial, and coronal slices. Histological examinations were performed in-house with standard histopathological and immunohistological staining. Data obtained from the hospital archives included demographics, histopathological diagnoses of primary cancer, site of primary cancer, clinical symptoms leading to the diagnosis of ISCM, time since the primary cancer was diagnosed, pre- and postoperative neurological deficit using the simplified McCormick Scale functional classification,41 location of the spinal metastasis, approximate radiological size of the metastasis, methods used during surgery, extent of resection, further treatments postoperatively, and ambulatory status at last follow-up. The extent of resection was based on the judgment of the surgeon and the postoperative MRI.

The McCormick Scale (simplified) is a functional classification of intramedullary spinal cord tumors with the appropriate validation. This was used to evaluate the clinical condition of the patients pre- and postoperatively, as well as in the follow-up (Table 1).41 Data are shown as the mean. Descriptive statistics were used to characterize the study population. The Student t-test was used to compare means of metric variables.

TABLE 1.

McCormick Scale functional classification of intramedullary spinal cord tumors

GradeCharacteristics
INeurologically normal, mild focal deficits, normal gait
IISensorimotor deficits affecting function, severe pain, gait difficulties, can still walk
IIIModerate neurological deficit, needs cane for ambulation, ± arms affected, ± independent
IVAs above + arms affected, usually not independent

Results

Demographic Data

Since 1986, 397 intramedullary lesions have been treated in our institution, but metastases have been part of the spectrum only since 1992. Since then, 22 cases have been treated, with the frequency markedly increasing during the last 4 years of this analysis.

Thirteen male patients and 9 female patients were treated (Tables 2 and 3). The mean age among all patients was 55 years (range 21−86 years). On average, the male population was younger than the female population (p = 0.48). The mean age of men was 52 years (range 21−86 years). The mean age of women was 58 years (range 33−79 years). Metastases in the cervical and thoracic spine were identified in 77% of patients (n = 17), whereas metastases in the thoracolumbar region (i.e., conus medullaris) could be identified only in 23% of patients (n = 5). The times-pan from primary cancer diagnosis to the development of symptomatic spinal metastases ranged from 0 to 285 months, with a mean interval of 38 months. In women, the period of time from primary cancer diagnosis to spinal metastasis was an average of 55.8 months. The corresponding period of time in men was remarkably shorter, with an average of 25.5 months (p = 0.35).

TABLE 2.

Preoperative characteristics of patients with ISCM

Case No.SexAge (yrs)Yr of OpPrimary CancerMos Since Primary CancerLocationAccessSize (l × w × d [mm])*Other ManifestationsSymptomsMcCormick Scale Grade Preop
1M772014NSCLC, CUP0T-12/L-1Hemilaminectomy T-1211 × 17NoneDysesthesiaI
2F792014Ovarian cancer30C4−7Laminotomy 4 levels38 × 15 × 11Liver, peritonealParesis, paresthesiaIV
3M472014Anaplastic astrocytoma54C2−5Laminotomy 1 level C-342 × 10NoneParesis, hypoesthesiaII
4F682014Breast cancer11T11−12Laminotomy 2 levelsNSBrainHypoesthesia, bladder dysfunction, paresisIII
5F712014Melanoma285C2−3Laminotomy 2 levels10 × 8 × 7Bone, skin, soft tissue, liverParesis, gait disturbanceII
6M672014Neuroendocrine tumor, CUP0T9−10Laminotomy 2 levels31 × 9 × 6BrainParaplegia, CBDIV
7M602013Prostate cancer74T5−6Laminotomy 1 level25 × 15 × 15Bone, liver, brain, lymph nodeParaparesis, painII
8F642012Neuroendocrine tumor of the lung6T5−6Laminotomy 2 levels24 × 7 × 7NoneParesis, painIII
9F342012Neuroendocrine tumor of the lung49T−9Laminotomy 1 level6 × 5 × 13BrainParesis, CBD, hypoesthesiaIV
10M612012Kidney cancer96C−7Laminotomy 2 levelsNSBrain, lung, boneGait disturbance, hypoesthesiaII
11M862012Bladder cancer48C−5Laminotomy 1 level14 × 8 × 7NoneHypoesthesia, paresisIII
12F632012Breast cancer52C6−T1Corpectomy 1 level32 × 5 × 7NoneParesis, hypoesthesiaII
13F332012Carcinoma, CUP0T7−8Laminotomy 1 level11 × 3 × 7NoneDysesthesiaI
14M272011NSCLC13T5−6Laminotomy 2 levels11 × 10 × 20Lymph node, liver, bone, brainCBD, gait disturbance, hypoesthesiaII
15M382011Melanoma0T−11Laminotomy 2 levels32 × 8 × 12NoneGait disturbance, paresisII
16F562006Breast cancer28T-12/L-1Laminotomy 2 levels50Lung, brainParesis, dysesthesiaIII
17M602002Adenocarcinoma of the lung0C4−5Laminotomy 1 level13 × 8NoneParesis, hypoesthesiaII
18F541999Ependymoma Grade III41T-12/L-1Hemilaminectomy 2 levels10 × 20NonePain, hypoesthesiaII
19M541997Adenocarcinoma of the lung46T-12/L-1Laminectomy 2 levelsNSBrainPain, hypoesthesiaII
20M591996Squamous epithelial carcinoma0T-12/L-1Laminectomy 2 levelsNSNoneParaparesis, hypoesthesia, CBDIII
21M211994Carcinoma0C5−6Laminectomy 1 levelNSNoneAcute paraparesisI
22M221992Medulloblastoma0C3−5Laminectomy 3 levelsNSBrainTetraparesisIV

CBD = colon-bladder dysfunction; NS = not specified; NSCLC = non-small-cell lung cancer.

Some data are missing.

TABLE 3.

Intra- and postoperative characteristics of patients with ISCM

Case No.Symptoms PostopMcCormick Scale Grade, PostopExtent of ResectionMethods Used During Surgery*ComplicationST, RTLast Neurological Follow-Up (mos)McCormick Scale Grade At Last Follow-Up
1SameIPartlyIntravenous corticosteroids, IOM, laserNoneNone3I
2SameIVSubtotalSono, intravenous corticosteroids, IOM, laserNoneST7IV
3WorseIIIBiopsySono, intravenous corticosteroids, IOMNoneST, RT6III
4SameIIISubtotalSono, intravenous corticosteroidsNoneRT6III
5SameIITotalIntravenous corticosteroids, IOM, laserNoneST6II
6SameIVSubtotalIntravenous corticosteroids, IOMNoneRT2IV
7BetterISubtotalIntravenous corticosteroids, IOMNoneST2I
8BetterIISubtotalIntravenous corticosteroids, IOMNoneRT4II
9SameIVTotalIntravenous corticosteroids, IOMNoneST6III
10WorseIIITotalIntravenous corticosteroids, IOM, laserNoneRT3II
11SameIIITotalSono, intravenous corticosteroids, IOM, CUSANoneNS9II
12SameIITotalSono, intravenous corticosteroids, IOM, CUSANoneST, RT3I
13WorseIISubtotalSono, intravenous corticosteroids, IOM, CUSANoneRT6I
14BetterISubtotalIntravenous corticosteroids, IOM, laserNoneST13I
15WorseIIITotalIntravenous corticosteroids, IOM, laserSpinal fluid leakageRT, ST25II
16SameIIISubtotalIntravenous corticosteroids, IOM, laserNoneST2III
17BetterIPartlyIntravenous corticosteroids, IOMNoneRT3I
18SameIITotalIntravenous corticosteroids, IOMNoneSTNSNS
19SameIISubtotalIntravenous corticosteroids, IOMNoneNoneNSNS
20NSNSSubtotalIntravenous corticosteroids, laserNSNSNSNS
21NSNSSubtotalIntravenous corticosteroids, laserNSNSNSNS
22NSNSSubtotalIntravenous corticosteroids, laserNSNSNSNS

RT = radiation; ST = systemic therapy.

Intravenous corticosteroids refer to intravenous administration of methylprednisolone (dependent on the patient’s weight) over a period of 24 hours; Sono means ultrasound was additionally used during surgery to evaluate extent of resection (before myelotomy, ultrasound is used routinely).

In 17 cases, the primary cancer was known or could be identified after obtaining the histopathology of the spinal metastasis. Lung cancer was the most frequent primary malignant disease (5 cases), followed by brain and breast cancers (3 cases each). Malignant melanoma was found twice. Bladder, prostate, ovarian, and kidney cancers, each represented by 1 case, were rare events. The brain metastases originated from 1 each anaplastic astrocytoma, ependymoma, and medulloblastoma.

In 8 patients, spinal metastases were the first clinical manifestation of malignant disease, thus representing a cancer of unknown primary (CUP) syndrome. In 5 of these patients, there was still no finding of a primary malignant tumor in subsequent staging. In 1 patient, the origin of the primary tumor was still unknown 12 months after treatment of ISCM. Another patient, in whom a renal carcinoma was the most probable origin of malignancy, died 4 months after spinal surgery without confirmation of the primary tumor source. Eleven patients (50%) had additional metastases at the time of presentation, 9 of them (41%) with tumors that had metastasized into the brain, 4 into the bone and liver, and 2 into the lung and lymph nodes. One patient had a skin metastasis (melanoma).

Fifty-nine percent of patients (n = 13) showed only mild clinical symptoms on the day of admission and were still able to walk autonomously (McCormick Scale Grade I or II). Eighteen percent of patients (n = 4) were severely disabled, with McCormick Scale Grade IV. Dysesthesia was the most common clinical symptom, with 77% of the study population reporting it before the time of surgery. The second-most common clinical symptom was paresis (68% of patients). Only 5 patients (23%) showed urinary and/or anal disorders.

Findings on MRI

In each case, the radiological finding was obtained by an MRI with and without gadolinium enhancement. T1 and T2 imaging sequences were obtained. The typical enhancement was an intramedullary nodulus, which could be seen in all but 1 case (Figs. 1 and 2). In this 1 case, which proved to be a metastasis of an anaplastic astrocytoma WHO Grade III, there was no enhancement in the gadolinium-enhanced T1 sequence, but the tumor could be clearly seen in the T2 FLAIR sequence (Fig. 3).

FIG. 1.
FIG. 1.

Left: Typical enhancement in the gadolinium-enhanced T1 sequence of an intramedullary metastasis originating from an ovarian carcinoma at the level of C4–6. Right: The tumor extending in a transversal slice is shown.

FIG. 2.
FIG. 2.

Patient 1 with a space-occupying lesion in the conus medullaris in sagittal (A and C) and transversal (B and D) T2 and T1 sequences with contrast enhancement. The postsurgical results with remaining edema (E) and the small approach (F) are shown.

FIG. 3.
FIG. 3.

T2 FLAIR sequence of an intramedullary metastasis of a known anaplastic astrocytoma WHO Grade III in the cervical spine. There was no enhancement in the T1-enhanced sequence. Sagittal T2 FLAIR sequence (left) and transversal MRI (right) are shown, with good visualization of the tumor.

The assumable volume of the tumor, where length (l), width (w), and depth (d) could be obtained, was calculated using the equation for ellipsoid volumes: vs = v = 4/3 π * l * w * d. Fifteen tumors could be calculated with a mean volume of 2980 μl, ranging from 513 to 8360 μl. In the remaining 7 patients, only 2 values could be established due to lack of original MRI data. Therefore, a volume could not be calculated. However, volume did not correlate with length of survival, neurological symptoms, extent of resection, or origin of the tumor.

Therapy

All 22 patients underwent microsurgical treatment, with 1 biopsy and 21 resections. In 7 patients (32%), a total resection was obtained. In 12 patients (55%), the final degree of resection could be described as subtotal (small layers on the border zone to the healthy spinal cord were left intentionally due to electrophysiological changes), and in 2 patients the tumor was only partly removed. In 77% of patients, a hemi-laminectomy or an osteoplastic laminotomy with reconstruction of the posterior spinal column was conducted to reach the intradural pathology. In the remaining 5 patients, a corpectomy (n = 1) or laminectomy (n = 4) was performed. Only in 2 patients (9%) was > 2 levels of lamina opening necessary to obtain the whole dimension of the tumor. After opening the dura, the spinal cord was approached through the sulcus medianus posterior, proving to be the approach with the lowest chance of neurological side effects.

Ultrasound was used in all cases to identify the dimension of the tumor prior to resection, especially in cases where the tumor did not reach the dorsal surface and therefore could not be identified visually through the microscope. Besides ultrasound, further methods used during surgery included the application of intravenous cortico-steroids, CO2 laser, Cavitron ultrasonic surgical aspirator (CUSA), and intraoperative monitoring (IOM). Continuous intra- and postoperative administration of weight-dependent intravenous corticosteroids over 24 hours was conducted in all cases, with the aim to diminish swelling of the spinal cord. The CO2 laser (Surgilase 25) was used 10 times (in 45% of patients). In 6 patients, ultrasound was additionally used during the tumor preparation to identify the borders to the healthy tissue. IOM was applied in 82% of patients. In 3 patients (14%), a CUSA was used.

Postoperatively, 6 patients underwent radiation of the resected area with up to 30 Gy, 7 had systemic chemotherapy, and 4 had a combination of these 2 treatments. In 2 cases, no further therapy was applied. In 1 case, a patient with a CUP did not want any further therapy, and the patient was discharged with no neurological symptoms. The source of the metastasis was still unknown 12 months after surgery, and the patient still did not show any neurological deficit.

Due to a general deterioration in 2 patients during the weeks after surgery, no further therapy was conducted in these cases. One patient with a kidney carcinoma treated with postsurgery radiation relapsed after 11 months at the same site and underwent a second surgery due to clinical worsening. A patient with a malignant melanoma showed a meningeal carcinomatous spreading in the follow-up MRI after 22 months and received a ventriculoperitoneal shunt 2 months later. Only 1 patient had a postoperative complication (a dural leakage), which had to be revised surgically.

One to 2 days after surgery, 11 of 19 patients (58%) showed no neurological difference, with 4 patients (21%) improving and 4 patients (21%) worsening. Immediately after surgery, 11 patients (58%) had either more or less trouble walking, compared with 7 patients (37%) before surgery. Although the clinical outcome immediately after surgery showed a decrease in “walking safely” as determined by the mean McCormick Scale grade, there was no change in the Student’s t-test (p = 1.0).

For 5 patients who were treated before the year 1999, valid follow-up information could not be obtained. The last follow-up time for the patients still alive (n = 17) was a mean of 6.24 months (range 2−22 months) from the time of surgery. Death was confirmed in 11 patients, with a mean survival time of 11.6 months after surgery; the shortest survival time was 2 months and the longest was 30 months (data not shown in Table 3).

The clinical status represented by the McCormick Scale grade in the 17 patients for whom follow-up data were available showed a mean of 2.12, where 6 patients had almost no clinical disability (McCormick Scale Grade I) and 2 patients were severely disabled (McCormick Scale Grade IV). Compared with the clinical status 1−2 days after surgery, there was an improvement in the McCormick Scale grade at the last follow-up from 2.47 to 2.12 (p = 0.009). Likewise, an improvement was detected when comparing the preoperative status (2.45) with the last follow-up status (2.12; p = 0.029).

Discussion

The occurrence of ISCM during the course of a malignant disease is still very rare.8,22,23,45,48,51 Nevertheless, with improved survival due to more effective treatments for many cancers, the incidence of ISCM will increase. This is already reflected by a continuous growth in the number of cases published in recent years (Fig. 4). Our findings support this trend, with almost 60% of all ISCM treated in the last 3 years out of a period of 22 years. There are a rising number of reports on the medical treatment of ISCM. However, generally applicable therapy algorithms are only just emerging. One explanation might be the considerable inconsistencies of published data in terms of localization, treatment option, and outcome of cancer patients with ISCM.

FIG. 4.
FIG. 4.

Number of publications in PubMed including case reports, series of up to 19 cases, and review of the literature concerning intramedullary metastasis.

Comparing our series with other published reports, we find comparable data in terms of mean age at ISCM presentation (55 years) and delay of diagnosis.8,22,51 Interesting within this context is the fact that the delay in diagnosis of spinal pathologies shows a similar difference between men and women in spinal dural arteriovenous malformations, indicating that the often insidious onset of symptoms is frequently misinterpreted in women.

With respect to distribution between men and women, as well as localization of ISCM in the spinal cord, there is no clear picture emerging. In our series, 41% of ISCM were found in the cervical region, followed by the thoracic spine (36%). Only 23% were located in the conus medullaris, which is in line with the findings of Kalayci et al.22 but is in contrast to the results of Dam-Hieu et al.,8 who describe the most common site of ISCM as in the conus medullaris (11/19; 58%).

Our experience, with lung cancer being the primary tumor (n = 5, 23%), followed by breast cancer (n = 3, 14%), is shared with other publications.4,8,18,22,26,32,34,37,39,40,43,49 The findings of systemic spreading are also similar to other published data. Only 1 patient showed > 1 ISCM at the time of surgery. Nine patients (41%) had no other metastatic manifestations, leaving more than 50% with systemic migration, of which almost 80% proved to have brain metastases.5,8,22,30 The metastatic spread of a malignant disease into the CNS, and especially into the spinal cord, is associated with a very poor prognosis, limiting the time of survival.4,5,8,26,37,51

Within our cohort, only 3 patients (14%) had concomitant brain metastasis. One proved to be a metastasis of an unknown medulloblastoma in the cerebellum. Only very few cases of this entity are published.19,27 The second proved to be a metastasis originating from an ependymoma WHO Grade III, diagnosed in the brain 41 months prior to the spinal occurrence. Unfortunately, as these cases were treated in 1992 and 1999, respectively, the patients were lost to follow-up. The third brain metastasis originated from an anaplastic astrocytoma WHO Grade III, which was diagnosed 54 months earlier. ISCM was located in the cervical spine, and after biopsy in 2014, the patient was treated with radiation. The patient’s neurological functions declined after biopsy (raising the McCormick Scale grade from II to III) and did not improve over time. However, the patient was still alive 6 months after surgery, with stable neurological impairment.

In 2 patients (9%), a malignant melanoma proved to be the primary tumor, the percentage being similar to other published reports.17,33,51 The remaining histologies—small cell renal, bladder, prostate, and ovarian carcinomas— were represented by 1 case each. A review of the literature shows that these obviously rare types of ISCM are usually represented only by case reports.1,2,7,9,13,14,16,21,28,35,36

Interestingly, we encountered 5 cases (23%) of ISCM as the primary finding of a malignant disease, which is very consistent with the findings of Kalayci et al.22 but stands in contrast to those of Dam-Hieu et al.8 In the latter series, every patient except for 1 had a previously diagnosed tumor.8,22 In the case of 1 patient in our cohort, the origin of the primary tumor was still unknown 12 months after initial diagnosis. No second treatment after surgery has been conducted due to the decision of the patient and the absence of clinical impairment. This suggests that although ISCM are known to be a sign for poor prognosis, they still do not predict a fast lethal outcome in every case. Furthermore, length of survival apparently does not depend on the existence or absence of other metastatic manifestations. One patient in our series presented with a neuro-endocrine cancer without further systemic spreading but died 3 months after surgical intervention. Another patient, diagnosed with the same primary tumor and who also showed brain metastases at the time of surgery, died 30 months later. ISCM due to malignant melanoma as a primary cancer seems to be associated with a longer length of survival.33 One patient developed a systemic meningeal carcinomatous after 22 months and received a ventriculoperitoneal shunt 2 months later. The last follow-up was after 25 months. The second patient with ISCM of malignant melanoma was treated in 2014 and is still alive. This finding is in line with the results of Wilson et al.51 as well as Conill et al.4

Using an ellipsoid volume assumption, taking into account peak open volume in width, length, and depth presented on the gadolinium-enhanced MRI before surgery, we could not find any correlation relating to length of survival, the McCormick Scale grade before and after surgery, tumor origin, or degree of resection. As there is no mention of any connection between size and any parameter in the literature, we cannot compare these findings with other authors’ experiences.

Of the 18 patients (we were able to obtain up-to-date information from their family doctor), 11 died. In this group, the mean length of survival after spine surgery was 11.6 months. This is distinctly longer compared with reported survival times for many other series and meta-analyses.8,22,51 Comparing conservatively treated patients with surgically treated ISCM, Kalayci et al. demonstrated a surgical benefit in terms of increasing the length of survival from 5 months to 9.4 months, suggesting that surgical removal of the tumor without much delay has a positive effect on the further development of the disease.22 However, Wilson et al.,51 as well as Watanabe et al.,48 could not find a benefit from surgery concerning the length of survival in their respective series. Nevertheless, their patients had preoperative urinary retention, which is accompanied by a progressive neurological deficit and poor prognosis (in our series, only 5 cases).

Surgical resection of an ISCM should, if chosen as the primary therapy, aim for a total resection. Considering the importance of total tumor resection in the case of cerebral metastases, one could postulate a similar importance when surgically removing ISCM. On the one hand, similar to intracranial metastases, ISCM are often well delineated, allowing for a dissection plane such that gross total resection can be achieved with minimal parenchymal injury. On the other hand, as there is more edema in the parenchymal tissue than in the well-differentiated intrinsic intramedullary tumors, there is an increased vulnerability. Perioperative neuroprotection with high-dose methylprednisolone is used on a regular basis in combination with an IOM as feedback for possible surgical stress, so that surgical steps can be adapted and postsurgical impairment minimized.25,50 Intraoperative ultrasound is also used regularly to confirm adequate extent of exposure before opening the dura and to assess extent of tumor resection.12

A CO2 laser is useful for minimizing mechanical stress during resection of an ISCM. It was applied in 10 cases in our series. Using all or a combination of these methods, it was possible to achieve at least a subtotal resection of the tumor in 85% of cases. Due to the heterogeneous origin of the primary histology, there is great variation in surface texture and infiltration at the tumor border. Therefore, in some cases, a small infiltrative tumorous layer was left deliberately. To enhance resection in these cases, a defocused, lowered-intensity CO2 laser coagulation after resection of the main tumor mass was performed. In the postoperative MRI, no contrast-enhanced tumor could be seen. In 7 patients (32%), the surgeon described the anticipated total resection, which could be confirmed by postoperative MRI, showing no enhancement after gadolinium application. In 3 cases, only biopsy or partial removal was possible due to distinctive adhesions and worsening of intraoperative neuromonitoring.

Gasser et al. analyzed 146 spinal cord tumors, 13 of which were metastases, and postulated that radical resection depends on histology alone. Their data showed that sarcomas and poorly differentiated carcinomas could not be totally resected due to lack of a clear border between the tumor and the spinal cord.15 In our data, there was no correlation between the extent of resection and the postoperative clinical outcome or length of survival, which was also described by Gasser et al.15

When extrapolating treatment of CNS metastases to the spinal cord, radiation therapy and chemotherapy have to be evaluated as part of treatment options. Radiation is usually considered for patients without neurological symptoms and can be well tolerated if the correct indications are made.8,31,38,44,47 On the other hand, Lee et al.,26 in a series of 11 patients undergoing radiotherapy and 1 patient without treatment, and Conill et al.4 reporting on 6 cases treated with radiotherapy combined with steroids, showed that after a short period of clinical improvement, a rather fast decline occurred in neurological functions, sometimes within only a few days. Thus, one could assume that unless radiation leads to an expected rapid shrinking of the tumor, surgery should be considered even when patients are oligosymptomatic.

Surgery is usually offered to patients suffering from neurological impairment or in the case of an unknown primary where a tissue diagnosis is required.30,44,47,51 Kalayci et al., having analyzed 32 published cases where surgery on ISCM was performed, showed that no patients developed new postoperative neurological deficits and an overall clinical improvement was found, with the length of survival being nearly twice as long compared with patients treated conservatively.22

Our study did not compare different modalities in the therapy of ISCM. Thus, we cannot answer the question of which therapy is better to use concerning postinterventional clinical decline or length of survival. It should be acknowledged that randomized trials to answer these clinical questions will probably never be performed due to recruitment barriers. But as can be seen throughout data published to date, each case must be considered individually to offer the best possible treatment. The different modalities involved—neurosurgery, radiotherapy, and oncology—must work closely together to achieve this. Surgery should be considered for the patient who shows fast neurological impairment, taking into consideration the primary disease (if known), the prognosis from the oncological point of view, and the decision of the patient. The preoperative neurological condition seems to be a reliable predictive factor for functional outcome after surgery and must therefore be taken into consideration when advising the patient.8,42,51 In the future, with an expected higher incidence of ISCM, initial neurological symptoms should be taken seriously and proper diagnostic measures initiated accordingly. Increasing neurological impairment seems to lead to a poor neurological outcome after surgery; thus, time is essential, the goal being to provide as much good quality of life as possible.

In cases of primary brain tumors or brain metastases, maximizing cytoreduction is known to have a positive effect on length of survival. This may also be essential in the case of ISCM and therefore should be set as the main goal of surgical treatment.24 Second, early decompression of the spinal cord may result in preserving or even improving neurological functions, as the growing understanding of spondylotic myelopathy has shown in the past.11 Taking all of this into account, the timely surgical treatment of ISCM must be considered an option to protect the remaining functional intact spinal cord. Technology for traction-free dissection, IOM, corticosteroids, potentially fluorescence guidance, and good anatomical knowledge help to achieve positive results.10

Conclusions

The occurrence of ISCM in the course of malignant disease is usually predictive of shortened life expectancy and is often associated with severe and worsening neurological deficits. We showed in 22 patients that surgery on ISCM, conducted under certain preconditions, can extend length of survival. The knowledge of incidence of intramedullary metastasis and its course is still very heterogeneous.

It depends on the histology of the primary tumor, whether it has spread to other organs, operative and conservative treatment strategies, and the patient’s overall condition. In the future, a sophisticated treatment algorithm will be of great importance, as the incidence of ISCM will probably increase further. Larger, prospective studies are needed.

Author Contributions

Conception and design: Eicker, Payer. Acquisition of data: Eicker, Payer, Mende. Analysis and interpretation of data: Eicker, Payer. Drafting the article: Eicker. Critically revising the article: Mende, Westphal. Reviewed submitted version of manuscript: Westphal. Approved the final version of the manuscript on behalf of all authors: Eicker.

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    Abdulazim ABackhaus MStienen MNCitak MBrokinkel BKuhlmann T: Intramedullary spinal cord metastasis and multiple brain metastases from urothelial carcinoma. J Clin Neurosci 18:140514072011

  • 2

    Ateaque AMartin JLO’Brien C: Intramedullary spinal cord metastases from a hypernephroma 11 years following the diagnosis and treatment of the primary lesion. Br J Neurosurg 14:4744762000

  • 3

    Chi JHParsa AT: Intramedullary spinal cord metastasis: clinical management and surgical considerations. Neurosurg Clin N Am 17:45502006

  • 4

    Conill CMarruecos JVerger EBerenguer JLomeña FDomingo-Domènech J: Clinical outcome in patients with intramedullary spinal cord metastases from lung cancer. Clin Transl Oncol 9:1721762007

  • 5

    Connolly ES JrWinfree CJMcCormick PCCruz MStein BM: Intramedullary spinal cord metastasis: report of three cases and review of the literature. Surg Neurol 46:3293381996

  • 6

    Constantini SMiller DCAllen JCRorke LBFreed DEpstein FJ: Radical excision of intramedullary spinal cord tumors: surgical morbidity and long-term follow-up evaluation in 164 children and young adults. J Neurosurg 93:2 Suppl1831932000

  • 7

    Crowley RWSherman JHLe BHJane JA: Intramedullary spinal cord metastasis from bladder carcinoma: case report. Neurosurgery 63:E611E6122008

  • 8

    Dam-Hieu PSeizeur RMineo J-FMetges J-PMeriot PSimon H: Retrospective study of 19 patients with intramedullary spinal cord metastasis. Clin Neurol Neurosurg 111:10172009

  • 9

    Donovan DJFreeman JH: Solitary intramedullary spinal cord tumor presenting as the initial manifestation of metastatic renal cell carcinoma: case report. Spine (Phila Pa 1976) 31:E460E4632006

  • 10

    Eicker SOFloeth FWKamp MSteiger HJHänggi D: The impact of fluorescence guidance on spinal intradural tumour surgery. Eur Spine J 22:139414012013

  • 11

    Eicker SOLangen KJGalldiks NStoffels GHerdmann JSteiger HJ: Clinical value of 2-deoxy-[18F]fluoro-D-glu-cose positron emission tomography in patients with cervical spondylotic myelopathy. Neurosurg Focus 35:1E22013

  • 12

    Epstein FJFarmer JPSchneider SJ: Intraoperative ultraso-nography: an important surgical adjunct for intramedullary tumors. J Neurosurg 74:7297331991

  • 13

    Fakih MSchiff DErlich RLogan TF: Intramedullary spinal cord metastasis (ISCM) in renal cell carcinoma: a series of six cases. Ann Oncol 12:117311772001

  • 14

    Gao JLi YYang ZWang R: Intramedullary spinal cord metastasis of renal cell carcinoma 6 years following the nephrectomy. Turk Neurosurg 24:2942962014

  • 15

    Gasser TSandalcioglu IEEl Hamalawi Bvan de Nes JAStolke DWiedemayer H: Surgical treatment of intramedullary spinal cord metastases of systemic cancer: functional outcome and prognosis. J Neurooncol 73:1631682005

  • 16

    Guo LZhong CJiang JQiu Y: A rare intramedullary spinal cord metastasis from prostate carcinoma. Neurol India 61:4444462013

  • 17

    Hashii HMizumoto MKanemoto AHarada HAsakura HHashimoto T: Radiotherapy for patients with symptomatic intramedullary spinal cord metastasis. J Radiat Res (Tokyo) 52:6416452011

  • 18

    Holoye PLibnoch JCox JKun LByhardt RAlmagro U: Spinal cord metastasis in small cell carcinoma of the lung. Int J Radiat Oncol Biol Phys 10:3493561984

  • 19

    Inoue TKumabe TTakahashi TNakajima TWatanabe MTominaga T: Spinal intramedullary metastasis of medulloblastoma at initial diagnosis. Childs Nerv Syst 23:1131162007

  • 20

    Ishii TTerao TKomine KAbe T: Intramedullary spinal cord metastases of malignant melanoma: an autopsy case report and review of the literature. Clin Neuropathol 29:3343402010

  • 21

    Isoya ESaruhash YKatsuura ATakahashi SMatsusue YHukuda S: Intramedullary spinal cord metastasis of ovarian tumor. Spinal Cord 42:4854872004

  • 22

    Kalayci MCağavi FGül SYenidünya SAçikgöz B: Intramedullary spinal cord metastases: diagnosis and treatment - an illustrated review. Acta Neurochir (Wien) 146:134713542004

  • 23

    Kalita O: Current insights into surgery for intramedullary spinal cord metastases: a literature review. Int J Surg Oncol 2011:9895062011

  • 24

    Kamp MADibué MSantacroce AZella SMNiemann LSteiger HJRapp MSabel M: The tumour is not enough or is it? Problems and new concepts in the surgery of cerebral metastases. Ecancermedicalscience 7:3062013

  • 25

    Kothbauer KDeletis VEpstein FJ: Intraoperative spinal cord monitoring for intramedullary surgery: an essential adjunct. Pediatr Neurosurg 26:2472541997

  • 26

    Lee SSKim MKSym SJKim SWKim WKKim S-B: Intramedullary spinal cord metastases: a single-institution experience. J Neurooncol 84:85892007

  • 27

    Madhugiri VSPandey PIndira Devi BSantosh VYasha TC: Intramedullary metastasis in a case of vermian medulloblastoma. Br J Neurosurg 26:2782802012

  • 28

    Miranpuri ASRajpal SSalamat MSKuo JS: Upper cervical intramedullary spinal metastasis of ovarian carcinoma: a case report and review of the literature. J Med Case Reports 5:3112011

  • 29

    Mortimer NHughes DO’Byrne KJ: Intramedullary spinal cord metastasis. Lancet Oncol 2:6072001

  • 30

    Mut MSchiff DShaffrey ME: Metastasis to nervous system: spinal epidural and intramedullary metastases. J Neurooncol 75:43562005

  • 31

    Nieder CGrosu ALAndratschke NHMolls M: Update of human spinal cord reirradiation tolerance based on additional data from 38 patients. Int J Radiat Oncol Biol Phys 66:144614492006

  • 32

    Nikolaou MKoumpou MMylonakis NKarabelis APectasides DKosmas C: Intramedullary spinal cord metastases from atypical small cell lung cancer: a case report and literature review. Cancer Invest 24:46492006

  • 33

    Nishihara MSasayama TKondoh TTanaka KKohmura EKudo H: Long-term survival after surgical resection of primary spinal malignant melanoma. Neurol Med Chir (Tokyo) 49:5465482009

  • 34

    Okamoto HShinkai TMatsuno YSaijo N: Intradural parenchymal involvement in the spinal subarachnoid space associated with primary lung cancer. Cancer 72:258325881993

  • 35

    Park JChung SWKim KTCho DCHwang JHSung JK: Intramedullary spinal cord metastasis in renal cell carcinoma: a case report of the surgical experience. J Korean Med Sci 28:125312562013

  • 36

    Poggi MMPatronas NButtman JAHewitt SMFuller B: Intramedullary spinal cord metastasis from renal cell carcinoma: detection by positron emission tomography. Clin Nucl Med 26:8378392001

  • 37

    Potti AAbdel-Raheem MLevitt RSchell DAMehdi SA: Intramedullary spinal cord metastases (ISCM) and non-small cell lung carcinoma (NSCLC): clinical patterns, diagnosis and therapeutic considerations. Lung Cancer 31:3193232001

  • 38

    Rades DRudat VVeninga TStalpers LJAHoskin PJSchild SE: Prognostic factors for functional outcome and survival after reirradiation for in-field recurrences of metastatic spinal cord compression. Cancer 113:109010962008

  • 39

    Rostami RSafarpour DTavassoli FAJabbari B: Intramedullary metastasis in breast cancer-a comprehensive literature review. J Neurol Sci 332:16202013

  • 40

    Rykken JBDiehn FEHunt CHSchwartz KMEckel LJWood CP: Intramedullary spinal cord metastases: MRI and relevant clinical features from a 13-year institutional case series. AJNR Am J Neuroradiol 34:204320492013

  • 41

    Samandouras G: Oxford Medicine Online: The Neurosurgeon’s Handbook (http://www.oxfordmedicine.com/view/10.1093/med/9780198570677.001.0001/med-9780198570677)Accessed June 24 2015

  • 42

    Sandalcioglu IEGasser TAsgari SLazorisak AEngelhorn TEgelhof T: Functional outcome after surgical treatment of intramedullary spinal cord tumors: experience with 78 patients. Spinal Cord 43:34412005

  • 43

    Schiff DO’Neill BP: Intramedullary spinal cord metastases: clinical features and treatment outcome. Neurology 47:9069121996

  • 44

    Shin DAHuh RChung SSRock JRyu S: Stereotactic spine radiosurgery for intradural and intramedullary metastasis. Neurosurg Focus 27:6E102009

  • 45

    Sung WSSung MJChan JHManion BSong JDubey A: Intramedullary spinal cord metastases: a 20-year institutional experience with a comprehensive literature review. World Neurosurg 79:5765842013

  • 46

    Sutter BArthur ALaurent JChadduck JFriehs GClarici G: Treatment options and time course for intramedullary spinal cord metastasis. Report of three cases and review of the literature. Neurosurg Focus 4:5e31998

  • 47

    Veeravagu ALieberson REMener AChen Y-RSoltys SGGibbs IC: CyberKnife stereotactic radiosurgery for the treatment of intramedullary spinal cord metastases. J Clin Neurosci 19:127312772012

  • 48

    Watanabe MNomura TToh ESato MMochida J: Intramedullary spinal cord metastasis: a clinical and imaging study of seven patients. J Spinal Disord Tech 19:43472006

  • 49

    Weissman DEGrossman SA: Simultaneous leptomeningeal and intramedullary spinal metastases in small cell lung carcinoma. Med Pediatr Oncol 14:54561986

  • 50

    Wiedemayer HFauser BSandalcioglu IESchäfer HStolke D: The impact of neurophysiological intraoperative monitoring on surgical decisions: a critical analysis of 423 cases. J Neurosurg 96:2552622002

  • 51

    Wilson DAFusco DJUschold TDSpetzler RFChang SW: Survival and functional outcome after surgical resection of intramedullary spinal cord metastases. World Neurosurg 77:3703742012

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

Article Information

Correspondence Sven O. Eicker, Department of Neurosurgery, University Hospital Hamburg-Eppendorf, Martinistr. 52, Hamburg 20246, Germany. email: eicker.s@mac.com.

INCLUDE WHEN CITING DOI: 10.3171/2015.5.FOCUS15149.

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

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Left: Typical enhancement in the gadolinium-enhanced T1 sequence of an intramedullary metastasis originating from an ovarian carcinoma at the level of C4–6. Right: The tumor extending in a transversal slice is shown.

  • View in gallery

    Patient 1 with a space-occupying lesion in the conus medullaris in sagittal (A and C) and transversal (B and D) T2 and T1 sequences with contrast enhancement. The postsurgical results with remaining edema (E) and the small approach (F) are shown.

  • View in gallery

    T2 FLAIR sequence of an intramedullary metastasis of a known anaplastic astrocytoma WHO Grade III in the cervical spine. There was no enhancement in the T1-enhanced sequence. Sagittal T2 FLAIR sequence (left) and transversal MRI (right) are shown, with good visualization of the tumor.

  • View in gallery

    Number of publications in PubMed including case reports, series of up to 19 cases, and review of the literature concerning intramedullary metastasis.

References

1

Abdulazim ABackhaus MStienen MNCitak MBrokinkel BKuhlmann T: Intramedullary spinal cord metastasis and multiple brain metastases from urothelial carcinoma. J Clin Neurosci 18:140514072011

2

Ateaque AMartin JLO’Brien C: Intramedullary spinal cord metastases from a hypernephroma 11 years following the diagnosis and treatment of the primary lesion. Br J Neurosurg 14:4744762000

3

Chi JHParsa AT: Intramedullary spinal cord metastasis: clinical management and surgical considerations. Neurosurg Clin N Am 17:45502006

4

Conill CMarruecos JVerger EBerenguer JLomeña FDomingo-Domènech J: Clinical outcome in patients with intramedullary spinal cord metastases from lung cancer. Clin Transl Oncol 9:1721762007

5

Connolly ES JrWinfree CJMcCormick PCCruz MStein BM: Intramedullary spinal cord metastasis: report of three cases and review of the literature. Surg Neurol 46:3293381996

6

Constantini SMiller DCAllen JCRorke LBFreed DEpstein FJ: Radical excision of intramedullary spinal cord tumors: surgical morbidity and long-term follow-up evaluation in 164 children and young adults. J Neurosurg 93:2 Suppl1831932000

7

Crowley RWSherman JHLe BHJane JA: Intramedullary spinal cord metastasis from bladder carcinoma: case report. Neurosurgery 63:E611E6122008

8

Dam-Hieu PSeizeur RMineo J-FMetges J-PMeriot PSimon H: Retrospective study of 19 patients with intramedullary spinal cord metastasis. Clin Neurol Neurosurg 111:10172009

9

Donovan DJFreeman JH: Solitary intramedullary spinal cord tumor presenting as the initial manifestation of metastatic renal cell carcinoma: case report. Spine (Phila Pa 1976) 31:E460E4632006

10

Eicker SOFloeth FWKamp MSteiger HJHänggi D: The impact of fluorescence guidance on spinal intradural tumour surgery. Eur Spine J 22:139414012013

11

Eicker SOLangen KJGalldiks NStoffels GHerdmann JSteiger HJ: Clinical value of 2-deoxy-[18F]fluoro-D-glu-cose positron emission tomography in patients with cervical spondylotic myelopathy. Neurosurg Focus 35:1E22013

12

Epstein FJFarmer JPSchneider SJ: Intraoperative ultraso-nography: an important surgical adjunct for intramedullary tumors. J Neurosurg 74:7297331991

13

Fakih MSchiff DErlich RLogan TF: Intramedullary spinal cord metastasis (ISCM) in renal cell carcinoma: a series of six cases. Ann Oncol 12:117311772001

14

Gao JLi YYang ZWang R: Intramedullary spinal cord metastasis of renal cell carcinoma 6 years following the nephrectomy. Turk Neurosurg 24:2942962014

15

Gasser TSandalcioglu IEEl Hamalawi Bvan de Nes JAStolke DWiedemayer H: Surgical treatment of intramedullary spinal cord metastases of systemic cancer: functional outcome and prognosis. J Neurooncol 73:1631682005

16

Guo LZhong CJiang JQiu Y: A rare intramedullary spinal cord metastasis from prostate carcinoma. Neurol India 61:4444462013

17

Hashii HMizumoto MKanemoto AHarada HAsakura HHashimoto T: Radiotherapy for patients with symptomatic intramedullary spinal cord metastasis. J Radiat Res (Tokyo) 52:6416452011

18

Holoye PLibnoch JCox JKun LByhardt RAlmagro U: Spinal cord metastasis in small cell carcinoma of the lung. Int J Radiat Oncol Biol Phys 10:3493561984

19

Inoue TKumabe TTakahashi TNakajima TWatanabe MTominaga T: Spinal intramedullary metastasis of medulloblastoma at initial diagnosis. Childs Nerv Syst 23:1131162007

20

Ishii TTerao TKomine KAbe T: Intramedullary spinal cord metastases of malignant melanoma: an autopsy case report and review of the literature. Clin Neuropathol 29:3343402010

21

Isoya ESaruhash YKatsuura ATakahashi SMatsusue YHukuda S: Intramedullary spinal cord metastasis of ovarian tumor. Spinal Cord 42:4854872004

22

Kalayci MCağavi FGül SYenidünya SAçikgöz B: Intramedullary spinal cord metastases: diagnosis and treatment - an illustrated review. Acta Neurochir (Wien) 146:134713542004

23

Kalita O: Current insights into surgery for intramedullary spinal cord metastases: a literature review. Int J Surg Oncol 2011:9895062011

24

Kamp MADibué MSantacroce AZella SMNiemann LSteiger HJRapp MSabel M: The tumour is not enough or is it? Problems and new concepts in the surgery of cerebral metastases. Ecancermedicalscience 7:3062013

25

Kothbauer KDeletis VEpstein FJ: Intraoperative spinal cord monitoring for intramedullary surgery: an essential adjunct. Pediatr Neurosurg 26:2472541997

26

Lee SSKim MKSym SJKim SWKim WKKim S-B: Intramedullary spinal cord metastases: a single-institution experience. J Neurooncol 84:85892007

27

Madhugiri VSPandey PIndira Devi BSantosh VYasha TC: Intramedullary metastasis in a case of vermian medulloblastoma. Br J Neurosurg 26:2782802012

28

Miranpuri ASRajpal SSalamat MSKuo JS: Upper cervical intramedullary spinal metastasis of ovarian carcinoma: a case report and review of the literature. J Med Case Reports 5:3112011

29

Mortimer NHughes DO’Byrne KJ: Intramedullary spinal cord metastasis. Lancet Oncol 2:6072001

30

Mut MSchiff DShaffrey ME: Metastasis to nervous system: spinal epidural and intramedullary metastases. J Neurooncol 75:43562005

31

Nieder CGrosu ALAndratschke NHMolls M: Update of human spinal cord reirradiation tolerance based on additional data from 38 patients. Int J Radiat Oncol Biol Phys 66:144614492006

32

Nikolaou MKoumpou MMylonakis NKarabelis APectasides DKosmas C: Intramedullary spinal cord metastases from atypical small cell lung cancer: a case report and literature review. Cancer Invest 24:46492006

33

Nishihara MSasayama TKondoh TTanaka KKohmura EKudo H: Long-term survival after surgical resection of primary spinal malignant melanoma. Neurol Med Chir (Tokyo) 49:5465482009

34

Okamoto HShinkai TMatsuno YSaijo N: Intradural parenchymal involvement in the spinal subarachnoid space associated with primary lung cancer. Cancer 72:258325881993

35

Park JChung SWKim KTCho DCHwang JHSung JK: Intramedullary spinal cord metastasis in renal cell carcinoma: a case report of the surgical experience. J Korean Med Sci 28:125312562013

36

Poggi MMPatronas NButtman JAHewitt SMFuller B: Intramedullary spinal cord metastasis from renal cell carcinoma: detection by positron emission tomography. Clin Nucl Med 26:8378392001

37

Potti AAbdel-Raheem MLevitt RSchell DAMehdi SA: Intramedullary spinal cord metastases (ISCM) and non-small cell lung carcinoma (NSCLC): clinical patterns, diagnosis and therapeutic considerations. Lung Cancer 31:3193232001

38

Rades DRudat VVeninga TStalpers LJAHoskin PJSchild SE: Prognostic factors for functional outcome and survival after reirradiation for in-field recurrences of metastatic spinal cord compression. Cancer 113:109010962008

39

Rostami RSafarpour DTavassoli FAJabbari B: Intramedullary metastasis in breast cancer-a comprehensive literature review. J Neurol Sci 332:16202013

40

Rykken JBDiehn FEHunt CHSchwartz KMEckel LJWood CP: Intramedullary spinal cord metastases: MRI and relevant clinical features from a 13-year institutional case series. AJNR Am J Neuroradiol 34:204320492013

41

Samandouras G: Oxford Medicine Online: The Neurosurgeon’s Handbook (http://www.oxfordmedicine.com/view/10.1093/med/9780198570677.001.0001/med-9780198570677)Accessed June 24 2015

42

Sandalcioglu IEGasser TAsgari SLazorisak AEngelhorn TEgelhof T: Functional outcome after surgical treatment of intramedullary spinal cord tumors: experience with 78 patients. Spinal Cord 43:34412005

43

Schiff DO’Neill BP: Intramedullary spinal cord metastases: clinical features and treatment outcome. Neurology 47:9069121996

44

Shin DAHuh RChung SSRock JRyu S: Stereotactic spine radiosurgery for intradural and intramedullary metastasis. Neurosurg Focus 27:6E102009

45

Sung WSSung MJChan JHManion BSong JDubey A: Intramedullary spinal cord metastases: a 20-year institutional experience with a comprehensive literature review. World Neurosurg 79:5765842013

46

Sutter BArthur ALaurent JChadduck JFriehs GClarici G: Treatment options and time course for intramedullary spinal cord metastasis. Report of three cases and review of the literature. Neurosurg Focus 4:5e31998

47

Veeravagu ALieberson REMener AChen Y-RSoltys SGGibbs IC: CyberKnife stereotactic radiosurgery for the treatment of intramedullary spinal cord metastases. J Clin Neurosci 19:127312772012

48

Watanabe MNomura TToh ESato MMochida J: Intramedullary spinal cord metastasis: a clinical and imaging study of seven patients. J Spinal Disord Tech 19:43472006

49

Weissman DEGrossman SA: Simultaneous leptomeningeal and intramedullary spinal metastases in small cell lung carcinoma. Med Pediatr Oncol 14:54561986

50

Wiedemayer HFauser BSandalcioglu IESchäfer HStolke D: The impact of neurophysiological intraoperative monitoring on surgical decisions: a critical analysis of 423 cases. J Neurosurg 96:2552622002

51

Wilson DAFusco DJUschold TDSpetzler RFChang SW: Survival and functional outcome after surgical resection of intramedullary spinal cord metastases. World Neurosurg 77:3703742012

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