|
 
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| ORIGINAL ARTICLE |
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| Year : 2022 | Volume
: 13
| Issue : 2 | Page : 65-73 |
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A prospective study of outcome predictors of intramedullary spinal cord tumors
Ajay Choudhary1, Rajesh Kumar Sharma1, Suryanarayanan Bhaskar2, Minakshi Bhardwaj3, Shahina Bano4, Neetika Gupta5
1 Department of Neurosurgery, ABVIMS (Previously PGIMER), Dr. RML Hospital, New Delhi, India
2 Department of Neurosurgery, AIIMS, Jodhpur, Rajasthan, India
3 Department of Pathology, ABVIMS, Dr. RML Hospital, New Delhi, India
4 Department of Radiology, ABVIMS, Dr. RML Hospital, New Delhi, India
5 Department of Radiodiagnosis, VMMC and Safdarjung Hospital, New Delhi, India
| Date of Submission | 31-Oct-2021 |
| Date of Acceptance | 17-Jan-2022 |
| Date of Web Publication | 28-Feb-2022 |
Correspondence Address:
Dr. Rajesh Kumar Sharma
Department of Neurosurgery, ABVIMS (Previously PGIMER), Dr. RML Hospital, New Delhi
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/jrcr.jrcr_49_21
Objectives: The objective of this study was to evaluate the outcomes of intramedullary spinal cord tumor (IMSCT) and the predictive factors that affected the outcomes. We also assessed the change in the health-related quality of life (HRQOL) of the patient's postsurgery during the follow-up period. Methods: This prospective study was done on 57 patients of IMSCT for a period of 3 years. Details regarding demography, clinical symptoms, histopathology grades/types, surgery performed, and the HRQOL (the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire 30) were noted. The outcome measures included mortality, neurological status (McCormick scale), and change in the HRQOL over a period of 6 months of follow-up. The data were entered in MS Excel and analyzed with P < 0.05 as significant. Results: Among the 57 patients, 42 (73.68%) had low-grade, 12 (21.05%) had high-grade, and 3 (5.26%) had unclassified metastatic tumors. Postoperatively, outcomes according to McCormick grade were same in 30 (52.63%) patients, worse in 15 (26.32%), and better in 12 (21.05%) patients. One patient died due to recurring seizures after metastasis. Histopathological type and surgical resection showed a significant association with McCormick grade (P < 0.05). The symptoms of paresthesia, motor weakness, and bladder/bowel involvement were significant risk factors for adverse outcomes with an odds ratio of 28.488, 6.077, and 4.035, respectively (P < 0.05). There was a significant improvement in the global quality of life of the patients after the surgery with significant improvement in emotional function, symptoms, and pain scores but a decrease in the physical functions (P < 0.05). Conclusion: The outcomes of patients with IMSCT are significantly affected by histology type, preoperative functional grade, and presenting symptoms.
Keywords: Intramedullary spinal cord tumors, outcomes, predictors, quality of life
How to cite this article:
Choudhary A, Sharma RK, Bhaskar S, Bhardwaj M, Bano S, Gupta N. A prospective study of outcome predictors of intramedullary spinal cord tumors. J Radiat Cancer Res 2022;13:65-73 |
How to cite this URL:
Choudhary A, Sharma RK, Bhaskar S, Bhardwaj M, Bano S, Gupta N. A prospective study of outcome predictors of intramedullary spinal cord tumors. J Radiat Cancer Res [serial online] 2022 [cited 2023 Mar 23];13:65-73. Available from: https://www.journalrcr.org/text.asp?2022/13/2/65/338800 |
| Introduction | |  |
Intramedullary spinal cord tumors (IMSCTs) are rare tumors that originate from the spinal cord proper and result in the invasion as well as destruction of the gray and white matter.[1]
For planning of treatment, the preferred modality to characterize IMSCT is magnetic resonance imaging (MRI).[2] After diagnosis of IMSCT, surgical resection should be done at the earliest because outcomes correlate with preoperative neurologic condition, and observation can result in neurologic deficits.[2],[3] In 83%–92% of the patients, it is possible to perform complete excision where clinical improvements are found after resection in terms of better long-term neurological outcomes.[1],[2],[3] Better long-term outcomes are noted in patients who have less preoperative deficits, while recurrence is dependent on the extent of resection as well as tumor histology.[3]
However, in the current scenario, the outcomes for patients with IMSCTs are guarded[4] as several factors such as age, tumor biology, grade, and resection affect the surgical outcomes of the patients.[5] It has also been seen that the quality of life (QOL) of the patient's postsurgery also depends upon these factors and it still remains an enigma as to what level of improvement is achieved in it.[4],[5] The complicated surgery, the relatively guarded outcome, and an inconstant improvement in the QOL of the patients with IMSCT define the lacuna for which the current study was being planned. In this case series, we followed up the clinical and surgical details of the patients in an effort to determine the factors that may affect the outcomes of the operated IMSCT during the follow-up period.
| Methods | | |
This prospective study was performed at the Department of Neurosurgery over a period of 3 years from June 2014 to June 2017. Treatment records of all patients with spinal tumors were reviewed, and patients operated for spinal tumors were recognized and analyzed in detail. Written informed consent was obtained from all patients before enrolling them in the study. Any patients with conditions such as coronary heart disease, hypertension, diabetes mellitus, or coagulopathy and those with recurrence of the tumors were excluded from the study. The institutional ethical clearance was obtained before the start of the study (IEC/Thesis/PGIMER-RML-H/10338, dated November 16, 2013).
The sample size calculation was based on the study of Haq et al., who observed that ependymoma was the most common IMSCT – 20 patients (60%).[5] Taking this value as reference, the minimum required sample size with 13% margin of error and 5% level of significance is 55 patients. To reduce margin of error, total sample size taken is 57.
Data related to demography, clinical, radiological, and histological features were recorded in a predesigned pro forma. Neurological status of the patients was graded on the basis of the modified McCormick scale (MMS) before surgery, immediate postoperative, at discharge, at 1 month, and at 12 months.[6] Classification of the histological origins of IMSCTs was done according to the World Health Organization (WHO) classification into neuroepithelial and nonneuroepithelial tumors. Neuroepithelial tumors were further classified into low-grade tumors (i.e., grades I, II) and high-grade tumors (i.e., grades III, IV).[7] The health-related quality of life (HRQOL) of the patients was measured using the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire C30 scale at baseline and at 6 months postsurgery.[8]
X-ray, computed tomography (CT) scan, and MRI with MR myelogram were done in all patients to know the extent of the tumor. Preoperative preparation was done. Preoperative markers along with X-ray, image intensifier, and operative microscope were utilized for proper localization. When there was clinical evidence of neurological deterioration or radiological evidence of edema, potent steroid (dexamethasone 5 mg, i. v.) was administered in preoperative phase. Surgery was performed under general anesthesia in prone position, followed by laminectomy, durotomy, myelotomy, microsurgical resection of tumor, and wound closure.
The surgical resection was categorized into three types based on the size of the residual tumor as seen on postoperative MRI. Subtotal resection (STR): residual tumor measuring between 5% and 15% of the preoperative volume noted on postoperative imaging. Near-total resection (NTR): residual tumor may or may not be seen on postoperative imaging and if seen measures ≤5% of preoperative volume. Gross total resection (GTR): no residual tumor seen in the postoperative contrast CT brain.
Standard operative methods were used in hemostasis such as use of bone wax and uni- and bipolar cautery with oxidized cellulose and in case of excessive bleeding. Hemostat like combination of gelatin granules and human thrombin was used wherever necessary. For suspected cerebrospinal fluid (CSF) leak, dura was closed with fascia and fibrin glue. The patients were given oral dexamethasone 5 mg for 3–6 months postoperatively and weaned off with decreasing frequency. Any postoperative complication was recorded. On the day of the surgery, biopsy was taken, preserved in 10% formalin, and sent to laboratory for diagnosis of tissue.
The patients with GTR and NTR were further treated with radiotherapy (RT) with a total of 60 Gy dose, in daily 2 Gy fractions, and patients with STR were followed with RT 60 Gy dose, in daily 2 Gy fractions as well as with chemotherapy with temozolomide with a dose of 75 mg/m2 on a cyclical pattern.
Patients were followed up at 1 month and 6 months telephonically. Patients were advised yearly MRI scans, irrespective of the adjuvant treatment.
The primary outcomes were McCormick grades, QOL, and risk factors affecting the postoperative outcomes. The secondary outcomes were mortality and length of hospital stay.
Statistical analysis
Categorical variables were presented in number and percentage (%), and continuous variables were presented as mean ± standard deviation and median. Normality of data was tested by Kolmogorov–Smirnov test. If the normality was rejected, then nonparametric test was used.
Quantitative variables were associated using Kruskal–Wallis test (as the data sets were not normally distributed) with histopathology and extent of resection, and Mann–Whitney test was used for association between high and low grades. Paired t-test was used for comparison between pre- and post-QOL. Qualitative variables were associated using Chi-square test/Fisher's exact test. Univariate and multivariate logistic regression was used to find out significant factors responsible for worst/same outcome. P < 0.05 was considered statistically significant.
The data were entered in MS Excel spreadsheet, and analysis was done using the Statistical Package for the Social Sciences, IBM manufacturer, Chicago, USA, version 21.0.
| Results | | |
The mean age of the patients was 33 ± 18.4 years, with 52.63% of the patients being ≤30 years of age. Females constituted 52.63% of the patients. The complaints of the patients were motor weakness (78.95%), loss of bladder/bowel involvement (52.63%), pain (52.63%), paresthesia (42.11%), spasticity (47.37%), and wasting (47.37%). The mean duration of the presence of tumor was 10.06 ± 14.09 months [Table 1]. | Table 1: Distribution of demographic and clinical characteristics of study subjects
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Most of the tumors were thoracolumbar (31.58%), followed by thoracic (26.32%) and cervicothoracic (21.05%). Astrocytoma was the most common IMSCT (36.84%), while 31.58% of the patients had ependymoma, and 15.79% had hemangioblastoma. As per the WHO grade, 42 (73.68%) were low grade (I/II), 12 (21.05%) were high grade (III/IV), and 3 (5.26%) were metastatic unclassified. GTR and NTR were done in 36.84% of the patients each and STR in 26.32% of the patients [Table 2]. | Table 2: Distribution of tumor characteristics and its management of study subjects
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The most common postoperative complications were urinary tract infection (UTI, 78.95%), bedsore (52.63%), and upper respiratory infection (URI, 42.11%). Outcomes according to McCormick grade were same in 30 (52.63%) patients, worse in 15 (26.32%), and better in 12 (21.05%) patients. The mean length of hospital stay was 35.89 days. There was a single mortality where the patient had metastatic lesions in brain leading to status epilepticus, and could not survive because of seizures [Table 3].
McCormick grades (1–4) were significantly different preoperatively, immediate postoperatively, at the time of discharge, and after 1 month and 6 months (P < 0.05). McCormick grades 2 and 3 were present in significantly less patients in immediate postoperatively and returned to preoperative values at 1 and 6 months. McCormick grade 4 was present in significantly less patients at 3 months postoperatively. McCormick grade 5 was comparable preoperatively, immediate postoperatively, at the time of discharge, and after 1 month and 6 months (P > 0.05) [Table 4].
There was a significant association of outcome with histopathology (P = 0.009). Postoperatively, lipoma had 100% better McCormick grades, while metastatic tumors had 100% worse McCormick grades. Other tumor types (astrocytoma, ependymoma, ganglioglioma, and hemangioblastoma) achieved varied McCormick grades, with majority of the patients showing the same McCormick grades even after 6 months of surgery. The median length of hospital stay was significantly highest in ganglioglioma, followed by metastatic, hemangioblastoma, ependymoma, astrocytoma, and lipoma (90 vs. 64 vs. 41 vs. 26 vs. 22 vs. 21) (P = 0.003) [Table 5].
There was a significant association of outcome with extent of resection. Significantly more patients with GTR had better outcomes (42.86%), with NTR (57.14%) and STR (80%) having majority of the patients with the same outcome (P = 0.009). The median length of hospital stay was similar in GTR, NTR, and STR (35 vs. 24 vs. 21, P = 0.197) [Table 6]. One representative case with preoperative and postoperative scans is shown in [Figure 1] and [Figure 2]. | Figure 1: Preoperative sagittal T2 weighted image (a) showing a large elongated intramedullary mass lesion involving the thoracic cord from T4–T10 level with cord expansion. Sagittal postcontrast T2 weighted image (b) demonstrating mildly heterogeneous and intense enhancement of this intramedullary mass
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 | Figure 2: Postoperative scan on day 1, T2W image (a) showing interval removal of the mass lesion with heterogeneously hyperintense changes and few hypointense areas likely representing postsurgical changes (edema and hemorrhage). The postcontrast T1W (b) images showing subtle postcontrast peripheral enhancement that could be reactive rather than residual mass. Postsurgical changes noted in the paraspinal region associated with deficient posterior elements at the same level
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The risk assessment of adverse outcomes showed that males (odds ratio [OR]: 3.093, P = 0.109), thoracic location (OR: 16.12, P = 0.076), high-grade tumors (OR: 10.246, P = 0.131), and symptoms carried an increased risk of adverse outcomes. Statistically, only the symptoms of paresthesia, motor weakness, and bladder/bowel involvement were significant risk factors for adverse outcomes with OR of 28.488, 6.077, and 4.035, respectively (P < 0.05). After adjusting for the confounders, only paresthesia was found as a significant adverse predictor with an adjusted odds ratio of 27.55 (P = 0.029) [Table 7]. | Table 7: Predictive factors of outcome of Intramedullary spinal cord tumors
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Compared to preoperative QOL, the postoperative QOL showed a significant improvement in the global QOL (61.5 vs. 53.2, P < 0.0001). Among the various parameters of QOL, the improvement was significant in the emotional function (73.6 vs. 69.3, P = 0.024), nausea and vomiting (6.6 vs. 11.7, P < 0.0001), and pain scores (18.3 vs. 22.2, P = 0.047). The physical functions showed a decrease in the mean score from 78.4 to 75.1, P = 0.01 [Table 8]. | Table 8: Changes in the health-related quality of life after surgery for Intramedullary spinal cord tumors
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| Discussion | | |
Spinal tumors (extradural, intradural-extramedullary, and intramedullary) are some of the rare central nervous system (CNS) tumors among which IMSCTs are the least common (2%–5%).[1] IMSCTs constitute about 2%–4% of all CNS tumors and 5%–10% of the spinal cord tumors. In a recent Indian study, 15% of the cases had IMSCT.[9]
The index study determined the outcome predictors for this rare category of tumors (IMSCT) and found that the histology type, preoperative functional grade, and presenting symptoms may adversely affect the outcomes of the patients.
In the present study on 57 patients with IMSCT, the mean age was 33 years with slight female predominance (52.63%). The most common presenting symptoms were motor weakness, pain, and loss of B/B involvement, with some patients having spasticity, wasting, and paresthesia, which is in accordance with the common presenting symptoms reported in the literature.[1],[10],[11],[12],[13],[14],[15]
In a study by Haq et al., the mean age was 36 years, with 56% of males, and common presenting complaints were loss of sensation in 80% patients, paresis in 66%, altered sensation in 40%, back pain in 36%, and sphincteric disturbances in 30% of the patients.[5] In a study by Persson et al., the median age of the patients was 45 years, with more males than females. The median time between the onset of symptoms and surgery was 12 months which was comparable to 10.06 months in the present study. The most common symptoms in their study included pain, sensory deficit, and motor deficit.[15] Zhang et al. reported a mean age of 35.5 years with slightly more females.[14] In a study by Khalid et al., the mean age of the patients was 47.63 years, with 62.6% of males.[1] Sharma et al. reported that the mean age was 29.7 years with slight male preponderance. The mean duration of symptom was 11.5 months which included motor weakness and sensory impairment.[10]
Overall, the most commonly encountered IMSCTs are astrocytoma, ependymomas, and hemangioblastomas. Gliomas (astrocytoma and ependymomas) constitute nearly 80% of the intramedullary tumors. Astrocytomas are found in majority of the patients in 30–40 years of age, are usually low grade, and located at the thoracic level, while ependymomas are reported to be present mostly in 30–60 years of age, with slight male predominance, and are located at the lower cord, conus, and filum. Besides these two, the third most common IMSCT is hemangioblastoma (in nearly 2%–15% of the cases). Rarely, metastatic intramedullary tumors are found which arise commonly from breast and lung tumors.[11],[12],[13],[14],[15]
Histopathologically, the most common tumors found in the present study were astrocytoma, ependymoma, and hemangioblastoma. The findings were in line with Haq et al., Zhang et al., Fathy et al., and Sharma et al. who found gliomas as the most common group of IMSCT (astrocytoma and ependymoma).[1],[5],[10],[14] Even the tumor location and the type of tumor resection were similar in our study and other previous studies.[11],[12],[13],[14],[16]
In our study, all the cases of IMSCT were surgically managed. Patients experienced certain complications such as UTI (78.95%), bedsore, URI, CSF leak, and deep vein thrombosis. We report a single case of death after recurrent seizures. Among other studies, pain was the most common postoperative complication (50%), sensory deficit (49%), motor deficit (42%), decreased bladder function (22%), and decreased gastrointestinal function (8%) with a mortality rate of 8.4%.[15] Fathy et al. found that common complications included CSF leak occurred in two cases in which dural grafts were used, postoperative hematoma in one case, tumor recurrence in two cases at last follow-up, and UTI in one case.[17] Haq et al. reported that superficial wound infection was present in 6.66% of the patients, CSF leak in 10% of the cases, and worsening of neurodeficit in 10% of the patients. Compared to the preoperative neurological condition, the overall postoperative state at last follow-up was improved or unchanged in 65% of the patients and worse in 34% of the patients.[5]
Surgical outcomes for IMSCT are affected by several variables such as tumor histology and preoperative neurological function, therefore, it is important to be aware of these parameters for predicting the outcome.[11] High-grade tumors are found to be associated with poor neurological outcomes. Reason behind this is that high-grade tumors infiltrate the normal spinal cord; this leads to an obscure surgical plane. Furthermore, pre- or postoperative RT is required in the high-grade tumors which can lead to poor functional outcomes.[5]
According to NCCN guidelines, several asymptomatic primary tumors of the spinal cord, particularly grade 1 meningiomas and peripheral nerve sheath tumors, follow an indolent course and can be followed by observation without immediate intervention.[18]
In symptomatic tumors, the preferred treatment is surgery. In the case of radiographically well-defined lesions (like ependymoma, WHO grade I astrocytoma, hemangioblastoma, schwannoma, and WHO grade I meningioma), the goal is maximal, safe resection. Where possible, maximal safe resection is attempted. GTR is seldom feasible with grade II or higher astrocytoma.
Radiation therapy is not recommended as primary therapy. Postoperative RT is recommended when symptoms persist after incomplete resection or biopsy. Chemotherapy is recommended when surgery and radiation therapy fail. We followed a regimen of postoperative RT for GTR and NTR, with STR cases being given radiochemotherapy.
We observed that high-grade tumors carried an increased risk (OR: 10.246) of adverse outcome though the risk association failed to cross statistical boundaries which might be due to a small number of high-grade tumors during the prospective study. In comparison, Fathy et al., Han et al., and Nakamura et al. found that high-grade tumors such as astrocytoma correlated with poor surgical outcomes.[4],[17],[19]
Besides grade of the tumors, we found that tumor histology significantly affected the McCormick grade. The findings were consistent with Karikari et al., who found that tumor histology (P = 0.005) was predictive of functional neurological outcomes.[20]
We observed that there was a significant association of outcome with extent of resection (P = 0.009). Worse outcome was present in 28.57%, 28.57%, and 20% of the patients, respectively, in GTR, NTR, and STR. Similar to our study, Karikari et al. found that extent of resection (P < 0.0001) was predictive of functional neurological outcomes.[20] Fathy et al. found that postoperatively, there was an improvement in the MMS scores in all the patients of the total resection (TR) group (100%) (MMS score ≤3), whereas scores improved in only two patients (33.3%) in the STR group (P = 0.008). It was also found that at the last follow-up, MMS score improvement was clinically and statistically significant in the TR group (P = 0.003).[17] As reported by Wong et al., in patients with malignant IMSCT who were treated with gross TR, there was a significantly lower mortality as well as improved prognosis than patients who were treated with biopsy, STR, or nonsurgical measures.[21] Kothbauer mentioned that advancement in microsurgical skills as well as intraoperative neurophysiological monitoring resulted in more aggressive efforts for TR and NTR of IMSCTs.[22]
As found in a study by Minehan et al., TR had good outcome, with complete tumor removal as well as good postoperative functional outcome.[23] It is suggested that in cases where total removal is not possible and high-grade tumors, partial resection or biopsy with RT and chemotherapy must be done.[17] A comparative evaluation of factors affecting neurological outcomes and the mortality rate among various studies conducted on patients with IMSCT is shown in [Table 9]. | Table 9: Studies evaluating factors affecting outcomes among patients with intramedullary spinal cord tumors
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Besides a good surgery, the QOL of the patients becomes important for the doctor. Any improvement in the HRQOL of the patients over time may indicate that the surgery was beneficial for the patient. Despite survival, there are various components that decide the QOL of the patients such as emotional, social, pain, vomiting, and financial components. In our study, it was clearly seen that the global QOL was significantly improved with better emotional component since they were relieved that they had undergone surgery. It was also seen that the symptom score was significantly reduced, and the improvement reflected upon their physical component as well. Among previous studies, Xiao et al. evaluated QOL outcomes after IMSCT resection, and found that patients with better preoperative neurological status or ependymoma experienced QOL improvement, whereas postoperative complications negatively impacted long-term QOL.[24] Nakanishi et al. reported no significant improvement of mean total HRQOL (431.1 before surgery and 434.2 at 6–12 months postoperatively, P > 0.05); however, the study showed a strong correlation between postoperative functional conditions and preservation of HRQOL.[25] As opposed to the adult population undergoing IMSCT surgery, aa per a pediatric study by Schneider et al., including children who underwent surgery for IMSCTs, QOL scores in terms of PedsQL 4.0 instrument showed no difference from those in a normal sample population.[26] This could be because of the difference in the patterns an adult, and a child assessed the QOL after a tumor.
Overall, the improvement in the QOL among adult patients undergoing surgery for IMSCT shows that the patients must be counseled about the effects of the surgery not only pertaining to the surgical outcomes and the complications but also in relation to the overall HRQOL of the patients.
Limitations
The study had certain limitations. First, the blood loss during the surgery was not estimated. Second, the adjuvant therapy was not adjusted as a confounding factor for assessing the improvement in the QOL of the patients.
| Conclusion | | |
The outcomes of patients with IMSCT are significantly affected by histology type, preoperative functional grade, and presenting symptoms. With an appropriate surgical approach, the functional abilities and QOL of the patients with IMSCT may be significantly improved over a period of time.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]
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