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Table of Contents
ORIGINAL ARTICLE
Year : 2018  |  Volume : 1  |  Issue : 3  |  Page : 111-116

Clinical and magnetic resonance imaging features of spinal cord glioblastoma multiforme in a series of 12 cases: A single-institutional experience


1 Department of Neurosurgery, Key Laboratory of Neurosurgical Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China
2 Department of Neurosurgery, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, China

Date of Web Publication29-Jun-2018

Correspondence Address:
Prof. Fuyou Guo
Department of Neurosurgery, Key Laboratory of Neurosurgical Diseases, The First Affiliated Hospital of Zhengzhou University, Jianshe East Road, No. 1, Zhengzhou 450052, Henan
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/glioma.glioma_25_18

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  Abstract 

Background: Spinal cord glioblastoma multiforme (SCGBM) is an extremely rare malignant tumor. The study aims to present the clinical and imaging features of SCGBM. Methods: The clinical and magnetic resonance imaging (MRI) characteristics of 12 pathologically proven SCBGM patients were retrospectively analyzed. Results: Three major MRI findings are as follows: (1) Mixed hypo-isointense signal on T1-weighted image (T1WI) and hyper-isointense signal on T2WI in all cases, (2) All except two patients demonstrated slight syringomyelia at upper or lower side of the lesion, and (3) Post-gadolinium-diethylenetriamine pentaacetic acid, a heterogeneously enhanced lesion with the crab foot-like shape on the map was seen in 11/12 cases. Clinically, pain in neck and waist was reported in 7 cases (58%) and progressive weakness of both lower extremities in 6 patients (50%). Gross total resection in 3 cases (25%) and subtotal resection in 9 cases (75%) were achieved. The most common postoperative complication was spinal instability, developed in 3 patients. The progress-free survival of surgery, surgery + temozolomide (TMZ), and surgery + TMZ + radiation treated patients was 2.50, 7.75, and 12.66 months, respectively. The overall survival of surgery, surgery + TMZ, and surgery + TMZ + radiation treated patients was 5.50, 15.25, and 24.00 months, respectively. Conclusion: The study reported MRI features in a large series of SCGBM. The trimodal therapy could provide longer survival for SCGBM patients.

Keywords: Clinical feature, magnetic resonance imaging, spinal cord glioblastoma multiforme


How to cite this article:
Guo F, Wang G, Suresh V, Xu D, Zhang X, Feng M, Wang F, Liu X, Song L. Clinical and magnetic resonance imaging features of spinal cord glioblastoma multiforme in a series of 12 cases: A single-institutional experience. Glioma 2018;1:111-6

How to cite this URL:
Guo F, Wang G, Suresh V, Xu D, Zhang X, Feng M, Wang F, Liu X, Song L. Clinical and magnetic resonance imaging features of spinal cord glioblastoma multiforme in a series of 12 cases: A single-institutional experience. Glioma [serial online] 2018 [cited 2022 Dec 7];1:111-6. Available from: http://www.jglioma.com/text.asp?2018/1/3/111/235651


  Introduction Top


The incidence of spinal cord glioblastoma multiforme (SCGBM) is extremely rare, which only accounts for 1.5% of all spinal tumors. Up to now, there have been fewer than 200 reported cases of SCGBM in literature.[1] Majority of SCGBM was described as solitary uncommon case,[2],[3],[4],[5],[6],[7] and only three studies enrolling >10 patients have been reported due to the rarity of SCGBM.[8],[9],[10] In view of the rarity of SCGBM, the optimal management of patients with SCGBM remains controversial. Ononiwu et al.[11] reported an average survival following gross total resection (GTR) and subtotal resection (STR) of SCGBM as 19.2 and 12.6 months, respectively. Their findings demonstrated that GTR was possible predictor of prolonged survival. Similar trend of better outcome on GTR followed by radiotherapy, than STR with radiotherapy, of SCBGM, was observed in systematic review.[12] However, Babu et al.[13] reported that the surgical intervention was associated with a higher rate of neurological complications and lacks a clear benefit for spinal cord astrocytomas, and thus, the resection should be reserved for selected cases and should be used sparingly.

There is no consensus on optimal management of SCGBM, by far. In addition, there is a lack of research regarding the clinical and magnetic resonance imaging (MRI) characteristics in a large series of SCGBM. The purpose of this study was to present our experience in a series of 12 SCGBM cases treated at our institution and briefly summarize the clinical and MRI features and management outcomes in these SCGBM cases.


  Materials and Methods Top


Patients

The study was approved by the Ethics Committee of Zhengzhou University. Consent forms were obtained from all patients. Between January 2011 and January 2018, a total of 12 SCGBM patients received microsurgical treatment at our neurosurgical center. The inclusion criteria of the current study were as follows: (1) Spinal tumor was pathologically proved to be GBM, which was consistent with the World Health Organization criteria; (2) All surgeries were performed at our institutional neurosurgical center; and (3) A complete MRI and neurological function follow-up report of the patient was available. Of the 12 included cases, there were 7 males and 5 females whose age ranged from 10 to 63 years (mean 34.4 years), with 2 patients <18 years of age. Pain in neck and waist was the chief complaint in 7 cases, followed by the progressive weakness of both lower extremities in six patients. Sensory disturbance occurred in 2 patients, incontinence of urine and feces in 2 patients, and dysuria was found in 1 patient. Tumors were located in the cervical region in 5 patients, in thoracic region in 5 patients, and in the lumbar region in 2 patients. Primary SCGBM was observed in 10 patients, while the remaining 2 patients were defined as secondary GBM due to metastasis from intracranial GBM [Table 1]. Of the metastasis cases, 1 metastasized from the GBM located in left temporal lobe 6 months after diagnosis, while in the other case, the metastasis occurred from GBM located in the right temporal-parietal lobe 2 years after diagnosis. The number of involved vertebral segments ranged from 2 to 8 segments, with the most common being 3 segments. The demographic data of 12 cases with SCGBM are presented in [Table 1] and [Figure 1]. All MRI examinations were performed on 3.0T clinical MR system (MAGNETOM Verio, SIEMENS Company, German). The images were reviewed by both an experienced neuroradiologist and a neurosurgeon.
Table 1: Demographic data on 12 cases with spinal cord glioblastoma

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Figure 1: Tumor location and involved segments of spinal cord glioblastoma multiforme

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Treatment

Therapeutic strategy was chosen based on surgeon' experience and patients' will after full doctor–patient communication. Some patient refused radiation therapy and chemotherapy due to anxiety of postoperative radiation and drug toxicity. Molecular profiles are essential to guide the precise treatment of patients. The molecular assay only conducted in our hospital since 2015, and it may cause economic burden to the family. Therefore, it has been only conducted in some of the cases.

Surgeries were performed using an intraoperative microscope and neuromonitoring. The tumors were removed at the maximal extent possible based on our goal of safe and precise surgery. No open biopsy was adopted in our surgical treatment. Extent of surgery was defined as GTR (≥95%), STR (≥50% and <95%), and partial resection (<50%).[8],[9],[10] Laminotomy or laminoplasty was carried out and the tumors were removed maximally following piecemeal resection technique, under the assistance of electrophysiology monitoring. Single operation was administrated in two patients without any adjuvant therapy, surgery plus temozolomide (TMZ) was used in four patients, and surgery + TMZ + radiation was adopted in six patients.

Pathology

Histological examination proved the tumor as GBM, with immunohistochemistry staining positive for glial fibrillary acidic protein, oligodendrocytes antigen 2, S-100, and vimentin. On an average, 40% of the cells were positive for Ki-67 marker. IDH1 and BRAF staining were negative. H3K27M were detected in two patients, with one being negative and the other being positive staining [Figure 2].
Figure 2: Histopathology of tumor showing (A) excessive atypical cells and microangiogenesis (H and E, ×200), (B) strong positive glial fibrillary acidic protein expression (×100), (C) positive S-100 expression (×100), ( D and E) IDH and K3M27 negative expression, respectively (×100), and (F) the percentage of Ki-67 expression was 40% (×100)

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Follow-up

Postoperative MRI was performed within 72 h after surgery. Thereafter, MRI and neurological function examination were performed at 3 months, 6 months, 1 year, and twice a year during the 2nd year. The overall survival (OS) was defined as the time from surgery to patient's death or the last follow-up. Progress-free survival (PFS) was defined as the time from the surgery to detection of disease progression, or patient's death or the last follow-up, as previously described.[9] The death of SCGBM was associated with the severe damage to respiratory center of cervical segment or multiple intracranial lesions from metastasis.


  Results Top


Magnetic resonance imaging findings

Three major MRI findings of SCGBM were identified. Mixed hypo-isointense signal on T1-weighted image (T1WI) and hyper-isointense signal on T2WI were found in all cases. All except two patients showed slight syringomyelia at upper or lower side of the lesion, with the incidence of syringomyelia being 83%. Post-gadolinium-diethylenetriamine pentaacetic acid (Gd-DTPA), a heterogeneously enhanced lesion with the crab foot-like shape on the map was seen in 11 cases, making it a striking characteristic of SCGBM found on MRI [Figure 3]. However, the lesion showed markedly homogeneous enhancement without necrosis, hemorrhage, or cyst formation in the remaining one patient.
Figure 3: (A) Preoperative sagittal T2 magnetic resonance imaging of spinal cord glioblastoma multiforme showing hyper-isointense signal with slight syringomyelia on the upper side, (B and C) sagittal and coronal gadolinium-enhanced magnetic resonance imaging scan showing the inhomogeneously enhanced lesion involved in the cervical 3–6, (D and E) postoperative sagittal magnetic resonance imaging scan showing tumor subtotal resection, developing spinal instability, (F) H and E staining showing atypical cells of glioblastoma multiforme. (G) Typical ependymoma in the cervical 3–4 showing obvious syringomyelia on the upper and lower side of the lesion. (H) Preoperative sagittal gadolinium-enhanced magnetic resonance imaging scan showing the homogeneously enhanced lesion, (I) postoperative sagittal gadolinium-enhanced magnetic resonance imaging scan showing total tumor resection

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Clinical features

Pain involved in neck and waist was the chief complaint in 7 cases (58%, 7/12), followed by the progressive weakness of both lower extremities in 6 patients (50%, 6/12). GTR was achieved in 3 cases (25%), and STR was performed in 9 cases (75%). There was no surgical mortality in this series. Following surgery, the complaint of pain was resolved in all patients, and the weakness of both lower extremities was improved in 4 patients, while the same deteriorated in 1 patient. The most common postoperative complication was spinal instability, developed in 3 patients, and cerebrospinal leakage occurred in 1 patient.

Therapeutic outcomes

PFS in surgery alone, surgery + TMZ, and surgery + TMZ + radiation was 2.50, 7.75, and 12.66 months, respectively, while the OS in surgery alone, surgery + TMZ, and surgery + TMZ + radiation was 5.50, 15.25, and 24.00 months, respectively.


  Discussion Top


GBM of spinal cord is considerably uncommon condition with poor prognosis due to highly aggressive biology. Unlike intracranial GBM, SCGBM has received little attention and lacks positive evidence to support treatment guidelines, due to its rarity. The optimal therapeutic strategy for SCGBM remains controversial and self-contradictory. The present study provided a comprehensive understanding of our neurosurgical experience, with the MRI characteristic analysis, clinical features, as well as surgical management outcomes in SCGBM. Several striking features were obtained from our series of 12 consecutive SCGBM patients: (1) SCGBM usually presents in younger patients with a mean age of 34.4 years, while the mean age of primary cerebral GBM and secondary cerebral GBM is 60 and 45 years, respectively; (2) The most common length of lesion corresponds to 3 vertebral segments; however, it may range from 2 to 8 vertebral segments; (3) The MRI finding of SCGBM demonstrated a heterogeneously enhanced lesion with the crab foot-like shape on the map after administrating Gd-DTPA, accounting for 83% of all patients; (4) Pain involved in neck and waist was the chief complaint in SCGBM, and the progressive weakness of both lower extremities was predominantly presented in our series; (5) The trimodal therapy, including surgery, chemotherapy, and radiation, could result in better survival outcomes for SCGBM patients, compared to surgery alone or surgery plus chemotherapy.

MRI plays a vital role in the diagnosis of spinal tumors, allowing tumors to be classified as extradural, intradural-extramedullary, or intradural-intramedullary, which is very useful and helpful in tumor characterization.[14] A recent study demonstrated that seven of the 12 spinal meningiomas were positive for the ginkgo leaf sign, which was not present in the control group tumors.[15] Unfortunately, there is still no study reporting the image analysis of SCGBM, due to the exceedingly rarity. From the results of our study, one can suspect SCGBM in the following conditions: (1) Young patients with typical MRI features exhibiting heterogeneously enhanced spinal lesions with crab foot-like shape on the map, after administrating Gd-DTPA. Such typical presentation is due to necrosis, hemorrhage, and cyst formation in the lesion. (2) Presence of syringomyelia on MRI for SCGBM. It is well known that the astrocytomas and ependymomas comprise the majority of the intramedullary tumors, and ependymomas occur with about double the frequency of astrocytomas. Based on our clinical experience on MRI, it is the feature of ependymomas to show high incidence of syringomyelia and homogeneously enhanced solid tumor section [Figure 3]G,[Figure 3]H,[Figure 3]I. As for low-grade astrocytomas, it usually lacks obvious enhancement on MRI, after administrating Gd-DTPA. However, currently, it is very difficult to differentiate between the anaplastic astrocytomas and GBM based on neuroimaging alone. Consequently, the difference between the anaplastic astrocytomas and GBM on MRI remains to be elucidated in the future. Our study is the first to report the unique findings of MRI features of SCGBM from a large series of cases. SCGBM should be highlighted in the differential diagnosis of the spinal cord malignant tumors.

There are still debates regarding the best therapeutic strategy for treating SCGBM currently. A meta-analysis by Hernández-Durán et al.[16] showed that at least 12 different treatment modalities have been adopted in the management of SCGBM. Furthermore, the study noted no significant difference in the median OS rate between TMZ group and non-TMZ group although a little long survival was observed in TMZ group compared to non-TMZ group. In our study, poor survival was observed in patients when treated with surgery alone. Conversely, longer PFS and OS were achieved when the surgery was combined with TMZ therapy. Another controversy in therapeutic outcome of SCGBM is the extent of resection during surgery; whether the total or STR results in better outcome compared to partial resection or biopsy? Viljoen et al.[17] suggested that the aggressive surgery, such as cordectomy, may delay intracranial extension and prolong survival of SCGBM patients. However, Shastin et al.[18] proposed that biopsy may be beneficial in given circumstances as cervical spinal GBM carries a better prognosis. In our opinion, the goal of surgery for SCGBM should be to resect as much tumor as possible, simultaneously preserving motor function. Thus, a high rate of STR (75%) was observed in our series, compared to total resection (25%). Our reasons for why the tumor should be resected as much as possible in SCGBM are as follows: (1) Chief complaint in our study population is pain due to the giant tumor, the maximal removal of which can only ameliorate the symptom dramatically; (2) In the current era of precise surgery, it is possible to preserve motor function under the assistance of electrophysiology monitoring and intraoperative MRI guidance; (3) The senior surgeon's experience also contribute to maximal resection of tumor, at the cost of less eloquent area damage to spinal cord; (4) With minimal postsurgical complications in our large series of 12 cases, the maximal resection of tumor in SCGBM can be reasoned to be reliable and safe. Another controversy in SCGBM is whether postoperative radiation can contribute to the long survival for patients? Sgouros et al.[19] reported that the 10-year survival rate in ependymomas patients receiving postoperative radiotherapy was 48%, compared to 96% in those who did not receive radiotherapy. Their findings demonstrated that radiotherapy did not offer any significant protection against recurrence or progression of spinal ependymomas. However, a study by Liu et al.[20] showed that postoperative radiation therapy was the only factor associated with prolonged survival in high-grade spinal gliomas. From our limited data, the postoperative radiotherapy as an adjuvant to surgery is found beneficial to SCGBM patients. Consequently, we advocate the safety and efficacy of not only maximal tumor resection but also the combination of chemo- and radio-therapy used in treating SCGBM. In fact, in our study, the longest survival was observed in SCGBM patients who received triple modal treatment, compared to single or double treatment.

The most common postoperative complication was spinal instability, which was seen in 3 patients. Based on our clinical experience, we closely associate this complication to the pediatric and long spinal segments of the lesion. Merlot et al.[21] reported that 10 of 21 spinal cord tumor patients developed secondary spinal deformity after surgery, with the incidence rate of 47.6%. Thus, it is urgent and necessary to develop an effective strategy to avoid this common complication of spinal instability in the future.

This study reported MRI features in a large series of SCGBM patients. Rare SCGBM cases with unique homogenous enhancement and without syringomyelia should be reported further. The trimodal therapy including surgery, chemotherapy, and radiation may result in prolonged survival of SCGBM patients, compared to surgery alone or surgery plus chemotherapy.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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