Management of patients with primary intramedullary spinal cord glioblastoma
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1 Accepted Manuscript Management of patients with primary intramedullary spinal cord glioblastoma Bedjan Behmanesh, MD, Matthias Setzer, MD, PhD, Juergen Konczalla, MD, Patrick Harter, MD, Johanna Quick-Weller, MD, Lioba Imoehl, MD, Kea Franz, MD, Florian Gessler, MD, Volker Seifert, MD, PhD, Gerhard Marquardt, MD, PhD PII: DOI: S (16) Reference: WNEU /j.wneu To appear in: World Neurosurgery Received Date: 29 June 2016 Revised Date: 12 October 2016 Accepted Date: 14 October 2016 Please cite this article as: Behmanesh B, Setzer M, Konczalla J, Harter P, Quick-Weller J, Imoehl L, Franz K, Gessler F, Seifert V, Marquardt G, Management of patients with primary intramedullary spinal cord glioblastoma, World Neurosurgery (2016), doi: /j.wneu This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
2 Behmanesh Management of patients with primary intramedullary spinal cord glioblastoma Bedjan Behmanesh, MD 1, Matthias Setzer, MD 1, PhD, Juergen Konczalla, MD 1, Patrick Harter, MD 2, Johanna Quick-Weller, MD 1, Lioba Imoehl, MD 1, Kea Franz, MD 1, Florian Gessler, MD 1, Volker Seifert, MD 1, PhD, Gerhard Marquardt, MD, PhD 1 Department of 1 Neurosurgery and 2 Neuropathology, University Hospital Frankfurt, Goethe-University, Frankfurt, Germany ABBREVIATIONS SC = spinal cord; SCGBM = intramedullary spinal cord glioblastoma; TMZ = temozolomide; CCNU = Chlorethyl-Cyclohexyl-Nitroso-Urea; McC = McCormick Grade; GBM = glioblastoma; ICGBM = intracranial glioblastoma, PFS = progression free survival
3 Behmanesh Correspondence Bedjan Behmanesh Department of Neurosurgery, University Hospital Frankfurt Schleusenweg 2-16, Frankfurt am Main, Germany Phone:
4 Abstract Behmanesh Background Primary intramedullary spinal cord glioblastoma are very rare tumors of the spinal cord. They imply a very poor prognosis since complete surgical resection is not possible due to the infiltrative growth of these tumors. The aim of this study is to present our data achieved with an aggressive multimodality treatment. Methods We retrospectively reviewed our clinical database. All patients with histologically proven intramedullary spinal cord glioblastoma treated in our department were included in this study. Results Four patients with intramedullary spinal cord glioblastoma were identified between 2006 and 2015, all of them were female. Mean age at the time of surgery was 33.5 years (range years). Tumors were located in the cervical region in two patients, and in the thoracic region in two patients. All four patients underwent microsurgical biopsy of the tumor. After surgery, all patients received radiation and temozolomide (TMZ) treatment. One patient underwent additional therapy with Bevacizumab, another patient received Rapamycin and Sunitinib, the third patient CCNU and Etoposide as additional therapy after tumor regrowth. Tumor progression occurred in a mean time of 18.2 months (6-32 months). In this series all patients died due to progression of the malignancy, median survival after diagnosis was 32.5 months.
5 Conclusion Behmanesh The surgical outcome of intramedullary spinal cord glioblastoma still remains poor. Severe disability and amelioration of the neurological status lead to reduced quality of life. However, an aggressive multimodal and interdisciplinary treatment for the disease may be associated with longer survival. Key word: intramedullary glioblastoma, spinal cord, surgery, radiation, multimodal therapy
6 Introduction Behmanesh Primary spinal cord (SC) tumors are rare entities, accounting for 2 4% of all central nervous system tumors 6,5. Among these, astrocytoma represent only 6 8% of all intramedullary tumors, with 75 90% of them being low grade gliomas. Therefore, SC glioblastoma multiforme (GBM) is extremely rare, accounting for only 1.5% of all SC tumors 26,22,25,28. These highly malignant lesions occur mainly in the cervicothoracic segments and have a slight tendency to occur in the first decades of life. A short clinical history before diagnosis is mainly associated with the natural history of SC GBM 8,14. Overall survival of patients with SC GBM is approximately months, in contrast to a better prognosis of 14 months for its intracranial counterpart 1. SCGBM results in death due to complications related to progressive SC involvement, respiratory impairment and cerebral metastases 9,8. Only few data exist reporting current experience about survival and progression after introduction of TMZ and novel therapeutic strategies. The aim of this paper is also to highlight the effect of new drugs on survival and tumor control. Methods We retrospectively reviewed the medical history of all patients with intramedullary spinal cord tumors treated at our institution during a period of 36 years. Between 2006 and 2015 four patients with the diagnosis of intramedullary spinal cord glioblastoma were identified. The medical charts were reviewed, including surgical and histological data, treatment parameters, neurological outcome, progression free survival (PFS), and overall survival (OS). Histological grading of all tumors was done according to the World Health Organization (WHO) criteria. Pre- and postoperative
7 Behmanesh neurological status during follow-up was performed by the staff neurosurgeons using the McCormick Classification scheme (Tab.1). All patients underwent preoperative, postoperative and follow up MRI scans. Surgical therapy consisted of a standard posterior approach via a laminectomy or laminoplasty in cases of multilevel tumor involvement in all patients. All operations were performed using an intraoperative microscope and neuromonitoring. Postoperatively, frozen section analysis and final histological preparation confirmed the diagnosis of SCGBM in all cases. After surgery all patients underwent radiotherapy, with an average dose of 50 Gy in five weeks. Chemotherapy with TMZ was administered in all patients concomitantly during radiotherapy. MRI was performed within 72 hours after surgery and subsequently every three months thereafter. Tumor regrowth and progression were defined as clinical and/or radiographical progression on follow-up MRI. Additional chemotherapy was administered according to the decision of the neuro oncological conference. Overall survival was defined as the period from the initial surgery to the date of death. Survival and progression free survival (PFS) were analyzed using Kaplan- Meier curves. A matched pair analysis with 4 patients with intracranial GBM (ICGBM) treated in our department was performed for comparison and detection of differences focusing PFS and survival. This analysis included patients with identical demographic characteristics, such as age, sex, radiation therapy and TMZ. In addition, a review of the literature was performed to compare the OS, patient s characteristics and treatment modality. Study Approval The study was approved by the local ethics committee at the authors institution.
8 Results Behmanesh All patients were females, and their ages ranged from years at the time of surgery (mean 33.5 years). The follow-up period ranged from 10 to 46 months (mean 32.5 months). The presenting symptoms and signs were pain, hypesthesia or paresthesia in all cases. Two patients revealed motor weakness preoperatively and only one patient an improvement of the neurological status after surgery and postoperative therapy. The preoperative functional assessment, which was made in all patients, showed one patient with McCormick Grade I, one with McCormick Grade II and another with McCormick Grade III and one patient with McCormick Grade IV. After surgery 2 patients had a McCormick II Grade and two patients McCormick Grade III. In the follow-up period three patients revealed McCormick Grade IV and one patient with a neurological improvement from McCormick Grade IV to McCormick Grade III. Lesions were located in the cervical spinal cord in two patients, and in the thoracic region in another two patients (Tab.2). The O6-methylguanine-DNA methyltransferase (MGMT) promoter was methylated in 2/4 cases, TP53 mutation was detected in 2 patients. Molecular examination did not reveal IDH1- or ATRX-mutations. None of the patients with SCGBM underwent total resection. All patients showed progression of the tumor. In none of the patients, the tumor had disseminated to a different location in the spinal cord. In one case tumor dissemination within the brain was observed. Mean PFS was 18.2 months (range, 6-32 months) (Fig. 1). Mean overall survival was 32.5 months (range, months) (Fig. 2). Conventional radiation therapy (40 50 Gy in fractions) was performed in all patients and was combined with a concomitant chemotherapy consisting of TMZ. In
9 Behmanesh case of tumor progression, an additional chemotherapy or radiation was recommended. One patient underwent additional Bevacizumab therapy and survived 46 months after surgery. The second patient displayed a tumor regrowth after 6 months and died after 10 months without further therapy after tumor progression. Patient three had a PFS of 11 months and received additional Rapamycin and Sunitinib after tumor progression. She deceased after 24 months. Patient four had a PFS of 32 months and underwent additional CCNU and etoposide treatment. She underwent a second radiation therapy and died 41 months after the initial presentation. The cause of death was respiratory paralysis in two cases and a severe pneumonia in another two cases. No patient was lost in the follow-up (Tab.2). An additional matched pair analysis with patients with intracranial GBM revealed no significant difference in regard to overall survival and PFS (median survival 35 months in intracranial GBM group, 32.5 months in the SC GBM group; p>0.05). Discussion Due to the extremely rare occurrence of SC GBM the current literature is scarce. A review of the pertaining literature suggests that this entity shows a predilection in the earlier decades of life 11,29,25,3. In our series mean age was 33.5 years with one patient being younger than 18 years. Apparently, the most affected spinal areas are the cervical and thoracic region in line with the data presented here 4,13,28. Since complete resection of these tumors is not possible due to their infiltrative growth pattern, surgery is commonly limited to biopsy or subtotal resection. Particularly the benefit of a more aggressive surgical procedure is unproven. All measures have produced disappointing results inasmuch as mean survival amounts months after diagnosis 24,7,3,21,23,27,31.
10 Behmanesh The introduction of adjuvant temozolomide therapy, in addition and radiation therapy, has produced a considerable improvement in survival and clinical outcomes of patients with intracranial GBM 30, but its role in the management of SCGBM remains unclear. Contrary to published data the patients in our series revealed a longer survival (Tab3.). We believe, the reason therefore is an aggressive and multimodal therapy beside radiation and TMZ therapy. Based on the quality of life of patients each case was managed individually with additional chemotherapy, which was recommended after initial tumor regrowth despite radiation and TMZ by the neuro oncological tumor board to prolong the survival and defer the tumor regrowth. In all cases the inability of autonomous breathing, either caused by respiratory paralysis or severe pneumonia was the reason for therapy termination. Therefore, an individual and patient-centered approach should be advocated. But indeed an essential recommendation cannot be drawn based on this small series. In our series we found one case of brain dissemination of the tumor. Tumor dissemination is a known pattern of SCGBM, but the mechanism of dissemination is still unclear, surgical manipulation may facilitate tumor cell seeding to the subarachnoid space, resulting with an intracranial dissemination. All current therapeutic measures have produced disappointing results, with survival ranging between 6 and 16 months with a mean survival period of 12 months after diagnosis 24,7,3,7,15,19. We nevertheless advocate multimodal treatment to extend the patient's survival as long as possible with the best quality of life. Improvement in technical and surgical techniques has influenced the management of intramedullary spinal cord tumors. Numerous tools, such as intraoperative- MRI, intraoperative sonography and electrophysiological monitoring, as well as
11 Behmanesh angiography, have been implemented to achieve a good postoperative outcome. Nevertheless, all these improvements do not guarantee a favorable outcome after surgery 16,12,17,18,10. Numerous studies have been published since first description of resection of these tumors to improve the knowledge about this rare entity. Because of the rarity of these tumors patients should be managed in specific centers with high volume of cases. A pre- and postoperative MRI is necessary to evaluate the surgical planning and postoperative extent of resection. Although not proven by literature, surgery should be performed with intraoperative electrophysiological monitoring, such as SSEPs and MEPs to assure a good functional outcome after surgery. Surgery is suggested for confirmation of the diagnosis and for cytoreduction of the tumor. The initial symptoms are in most cases nonspecific and are often underestimated (hypesthesia, paresthesia, and sensory deficits) whereas later in the clinical course, the neurological status worsens dramatically, including sensory and motor disorders, paraplegia, tetraplegia, and sphincter disturbances 2,20,22,3,28. The prognosis for high-grade glioblastoma, as for their intracranial counterparts, is extremely poor, and virtually all patients die as a consequence of progressive disease. However, we showed in this series a doubled survival rate compared to the literature. Based on our data using the matched pair analysis with identical properties, such as age, sex and surgical procedure we were able to confirm an even longer median survival rate than in patients with intracranial GBM. But the quality of life in patients presented in this study remains disappointing. All patients suffered from progressive disability over time. The first three patients developed a severe weakness of the limbs and/ or respiratory paralysis. Patient 4 was introduced with a tetra paresis and had to be tracheal cannulated resulting from diaphragm paralysis. After surgery and additional chemo-radio therapy she recovered and was able to walk with an aid. But in the last follow up the grade of disability was increased due to
12 Behmanesh tumor progression. A tetra paresis as initially introduced and disability of breathing led to death. All patients needed external aid and suffered from severe paralysis and pain. The reduced quality of life, especially the inability of autonomous breathing was the main reason for refusal of any further therapy. Conclusion The surgical outcome of intramedullary spinal cord glioblastoma still remains poor. Severe disability and amelioration of the neurological status lead to reduced quality of life. However, an aggressive multimodal and interdisciplinary treatment for the disease may be associated with longer survival. Limitation The retrospective design based on experience of a single center and the limited number of patients. Acknowledgements We thank Marina Heibel for her excellent technical support Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
13 Behmanesh Fig.1 Kaplan-Meier analysis of tumor progression for intramedullary spinal cord glioblastoma (SCGBM) compared to progression free survival of intracranial glioblastoma (ICGBM). No significant difference was obtained in this analysis. Fig.2 Kaplan- Meier analysis of overall survival (OAS) of SCGBM in comparison with its intracranial counterpart (ICGBM). Fig.3 Illustrative Case of intramedullary spinal cord glioblastoma A: before surgery B: after surgery and radiation C: progression of the tumor at last follow up before death
14 References: Behmanesh 1. Adams H, Avendaño J, Raza SM, Gokaslan ZL, Jallo GI, Quiñones-Hinojosa A: Prognostic factors and survival in primary malignant astrocytomas of the spinal cord: a population-based analysis from 1973 to Spine (Phila Pa 1976) 37:E727-35, Aghakhani N, David P, Parker F, Lacroix C, Benoudiba F, Tadie M: Intramedullary spinal ependymomas: analysis of a consecutive series of 82 adult cases with particular attention to patients with no preoperative neurological deficit. Neurosurgery 62: , Alvisi C, Cerisoli M, Giulioni M: Intramedullary spinal gliomas: long-term results of surgical treatments. Acta Neurochir (Wien) 70:169 79, Balériaux DL: Spinal cord tumors. Eur Radiol 9:1252 8, Barker DJ, Weller RO, Garfield JS: Epidemiology of primary tumours of the brain and spinal cord: a regional survey in southern England. J Neurol Neurosurg Psychiatry 39:290 6, Benes V, Barsa P, Benes V, Suchomel P: Prognostic factors in intramedullary astrocytomas: a literature review. Eur Spine J 18: , Chamberlain MC, Johnston SK: Recurrent spinal cord glioblastoma: salvage therapy with bevacizumab. J Neurooncol 102:427 32, Ciappetta P, Salvati M, Capoccia G, Artico M, Raco A, Fortuna A: Spinal glioblastomas: report of seven cases and review of the literature. Neurosurgery 28:302 6, Cohen AR, Wisoff JH, Allen JC, Epstein F: Malignant astrocytomas of the spinal cord. J Neurosurg 70:50 4, 1989
15 Behmanesh 10. Eroes CA, Zausinger S, Kreth F-W, Goldbrunner R, Tonn J-C: Intramedullary low grade astrocytoma and ependymoma. Surgical results and predicting factors for clinical outcome. Acta Neurochir (Wien) 152:611 8, Fortuna A, Giuffré R: Intramedullary glioblastomas. Neurochirurgia (Stuttg) 14:14 23, Garcés-Ambrossi GL, McGirt MJ, Mehta VA, Sciubba DM, Witham TF, Bydon A, et al.: Factors associated with progression-free survival and long-term neurological outcome after resection of intramedullary spinal cord tumors: analysis of 101 consecutive cases. J Neurosurg Spine 11:591 9, Guidetti B, Mercuri S, Vagnozzi R: Long-term results of the surgical treatment of 129 intramedullary spinal gliomas. J Neurosurg 54:323 30, Henson JW: Spinal cord gliomas. Curr Opin Neurol 14:679 82, Kaley TJ, Mondesire-Crump I, Gavrilovic IT: Temozolomide or bevacizumab for spinal cord high-grade gliomas. J Neurooncol 109:385 9, Klekamp J: Treatment of intramedullary tumors: analysis of surgical morbidity and long-term results. J Neurosurg Spine 19:12 26, Kothbauer KF, Deletis V, Epstein FJ: Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus 4:e1, Manzano G, Green BA, Vanni S, Levi AD: Contemporary management of adult intramedullary spinal tumors-pathology and neurological outcomes related to surgical resection. Spinal Cord 46:540 6, McGirt MJ, Goldstein IM, Chaichana KL, Tobias ME, Kothbauer KF, Jallo GI: Extent of surgical resection of malignant astrocytomas of the spinal cord: outcome analysis of 35 patients. Neurosurgery 63: , 2008
16 Behmanesh 20. Nakamura M, Ishii K, Watanabe K, Tsuji T, Takaishi H, Matsumoto M, et al.: Surgical treatment of intramedullary spinal cord tumors: prognosis and complications. Spinal Cord 46:282 6, Ononiwu C, Mehta V, Bettegowda C, Jallo G: Pediatric spinal glioblastoma multiforme: current treatment strategies and possible predictors of survival. Childs Nerv Syst 28:715 20, Raco A, Esposito V, Lenzi J, Piccirilli M, Delfini R, Cantore G: Long-term follow-up of intramedullary spinal cord tumors: a series of 202 cases. Neurosurgery 56: , Ryu SJ, Kim JY, Kim KH, Park JY, Kuh SU, Chin DK, et al.: A retrospective observational study on the treatment outcomes of 26 patients with spinal cord astrocytoma including two cases of malignant transformation. Eur Spine J: Santi M, Mena H, Wong K, Koeller K, Olsen C, Rushing EJ: Spinal cord malignant astrocytomas. Clinicopathologic features in 36 cases. Cancer 98:554 61, Scarrow AM, Rajendran P, Welch WC: Glioblastoma multiforme of the conus medullaris. Clin Neurol Neurosurg 102:166 7, Schwartz TH, McCormick PC: Intramedullary ependymomas: clinical presentation, surgical treatment strategies and prognosis. J Neurooncol 47:211 8, Seki T, Hida K, Yano S, Aoyama T, Koyanagi I, Houkin K: Surgical Outcomes of High-Grade Spinal Cord Gliomas. Asian Spine J 9:935 41, Shrivastava RK, Epstein FJ, Perin NI, Post KD, Jallo GI: Intramedullary spinal cord tumors in patients older than 50 years of age: management and outcome analysis. J Neurosurg Spine 2:249 55, 2005
17 Behmanesh 29. Stecco A, Quirico C, Giampietro A, Sessa G, Boldorini R, Carriero A: Glioblastoma multiforme of the conus medullaris in a child: description of a case and literature review. AJNR Am J Neuroradiol 26: , Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, et al.: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987 96, Yanamadala V, Koffie RM, Shankar GM, Kumar JI, Buchlak QD, Puthenpura V, et al.: Spinal cord glioblastoma: 25years of experience from a single institution. J Clin Neurosci 27:138 41, 2016
18 Tab.1. Modified McCormick score Grade I II III IV Clinical definition Neurologically normal Moderate deficit, limitation of function, independent without external aid Severe motor or sensory deficit, limited function, dependent in external aid Severe deficit, paraplegia or quadriplegia, dependent
19 Tab.2. Patient s characteristics Sex Age Tumor location Treatment Survival (months) Postop Status Pat.1 f 43 thoracic Bx+ RT+ TMZ+ Avastin 46 worsened Pat. 2 f 26 cervical Bx+RT+TMZ 10 worsened Pat.3 f 14 thoracic Bx+ RT+ TMZ+ Rapamycin+ Sunitinib Pat.4 f 50 cervical Bx + RT + TMZ + CCNU + Etoposid + RT Bx = biopsy, f = female, RT = radiation therapy, TMZ = temozolomide. 24 worsened 41 improved
20 Tab.3: Characteristics and outcomes of patients with spinal cord glioblastoma in the recent literature and in our series Age (years) No. of patients (SCGBM) Tumor Location C/T GTR Sex m/f Chemo TMZ McGirt et al /8 4/5 7/8 8/8 9 RT Median OS (mon) Raco et al /5 3/12 7/5 5/12 8/12 17 Chamberlain et al /4 0/6 5/1 6/6 6/6 9 Ononiwu et al /4 4/8 15 Median PFS (mon) Kaley et al /6 5/1 6/6 6/ Seki et al /3 0/4 3/1 2/2 4/ Yanamadala et al /3 2/4 3/6 3/6 18 Ryu et al /6 3/3 0/6 3/ Our series /2 0/4 0/4 4/4 4/ SCGBM: spinal cord glioblastoma; C: cervical; T: thoracic; GTR: gross total resection; m: male; f: female; TMZ: temozolomide; RT: radiation; OS: overall survival; mon: months; PFS: progression free survival
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23 AC C EP TE D M AN U SC RI PT
24 Highlights - This paper provides an additional multimodal therapy approach of intramedullary spinal cord glioblastoma - We show the double survival time compared to the literature - With interdisciplinary approach we improved patients survival - The quality of life remains still poor
25 ABBREVIATIONS SC = spinal cord SCGBM = intramedullary spinal cord glioblastoma TMZ = temozolomide CCNU = Chlorethyl-Cyclohexyl-Nitroso-Urea = Lomustin McC = McCormick Grade SC = spinal cord GBM = glioblastoma ICGBM = intracranial glioblastoma PFS = progression free survival
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