Early Post-Operative MRI: Correlation with Progression-Free Survival and Overall Survival Time in Malignant Gliomas
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1 J. Exp. Clin. Cancer Res., 25, 2, 2006 Early Post-Operative MRI: Correlation with Progression-Free Survival and Overall Survival Time in Malignant Gliomas A. Vidiri 1, C. M. Carapella 2, A. Pace 3, A. Mirri 4, A. Fabi 5, M. Carosi 6, D. Giannarelli 7, A. Pompili 2, B. Jandolo 3, E. Occhipinti 2, S. Di Giovanni 1 and M. Crecco 1 Department of Diagnostic Imaging 1, Neurosurgery 2, Neurology 3, Radiotherapy 4, First Medical Oncology 5, Anatomo-Pathology 6 Statistical Unit 7, "Regina Elena" Cancer Institute, Rome - Italy and Forty-seven patients with Glioblastoma (42) and Anaplastic Astrocytoma (5) were studied with MR 24 hrs after surgery. In order to evaluate the role of early MR in defining the extent of surgical resection and its relation with the prognosis of malignant glioma patients, three categories of surgical resection were considered: gross total, sub-total and partial resection. The results were correlated with progression-free survival (PFS) and overall survival (ST). As demonstrated by early-mr, gross total resection was performed in 17 patients, sub-total and partial resection in 19 and 11 patients, respectively. The PFS was 6 months in gross total resection, 6 and 3 months in sub-total and in partial resection, respectively. The median survival time was 16 months in total resection patients, 13 months and 7 months in sub-total resection and partial resection patients, respectively. The study confirms that early-mr has to be considered an accurate technique for monitoring the extension of malignant glioma surgical resection and shows a good correlation between early-mr findings, PFS and ST. Key Words:MR, Early MR, Glioblastoma, Anaplastic astrocytoma The extension of tumor resection on the outcome of patients affected by malignant brain tumors is still discussed as reported in the literature, and there is modest evidence that aggressive surgical treatment prolongs overall survival time (1,2,3). As far as the extent of the resection is concerned, the reliability of the surgeon, without imaging confirmation, is rather poor. Early post-operative neuroimaging has clearly contributed to highlight the role of surgical resection utilizing post-operative CT or MRI with contrast medium administration in the first three days after surgical procedure (3,4,5) The purpose of this study was to define the role of early-mr in the evaluation of surgical resection in patients affected by malignant gliomas, comparing the observed results with the final outcome in terms of Progression Free Survival (PFS) and Survival Time (ST). Materials and Methods Forty-seven patients affected by malignant gliomas [42 Glioblastoma (GBM) and 5 Anaplastic Astrocytoma (AA)] were studied. The median age was 58 years (33-76 years); all patients were eligible for surgery; tumors of the basal ganglia, brain stem and corpus callosum were excluded. Multicenter tumors, or non-enhancing gliomas were not reported. Median Karnosfky Performance Status (KPS) was 80 (40-100): KPS > 80 in 35 patients and KPS < 50 in 3 patients. After surgery, the combined therapeutic strategy implied radiotherapy (55-60 Gray), followed by chemotherapy according to the Procarbazine, Carmustine and Vincristine combination regimen (PCV), and/or Temozolomide. Thirty-five patients received both radiotherapy and chemotherapy, 10 chemotherapy alone and two patients did not receive any complementary treatment due to old age and low KPS. MR imaging was performed within 24 hrs after surgery utilizing both 1.5 and 0.5 T superconductive scanners. A head-coil, matrix of 256 x 256 and 6-mm. tickness slices were used. Before the contrast medium injection, SE T1-weighted sequences (TR 560 ms, TE 15 ms) in the axial and coronal plane were obtained; in addition Turbo SE T2-weighted sequences in the coronal plane (TR 2500 ms, TE ms), and FLAIR in the axial plane (TR 6000 ms, TE 150 ms, TI 2000) were per- 177
2 A. Vidiri et al. formed. After contrast medium administration of 0,2 mmol/kg of gadolinium diethylemetriamine pentacetic acid (Gd-DTPA) SE T1-weighted sequences in the axial, coronal and sagittal planes were performed. In the pre-operative MRI, site and dimensions of the tumor were considered, referring the anterior-posterior, transversal and longitudinal diameters. Analysis of the early post-operative MR images was performed considering: 1. The areas of hyperintensity in T1 weighted sequences before c.m. injection were correlated with the presence of haemostatic agents. 2. The areas with nodular or mass-like shape enhancement after c.m. injection were correlated with the presence of residual tumor tissue. 3. TSE T2 and FLAIR sequences were used for the evaluation of the probable ischemic lesions linked to surgical maneuvers. The extent of tumor removal evaluated by early-mr was classified into three categories: 1. Gross total resection: complete or greater than 98% removal of contrast enhancing pre-operative lesion. 2. Sub-total resection: between 88 and 98% removal of contrast enhancing pre-operative lesion. 3. Partial resection: less than 88% removal of contrast enhancing pre-operative lesion. The follow-up scans were obtained 30 days after surgery and then every 2 to 4 months. The peripheral enhancement, eventually outlining tumor resection cavity, was considered benign when linear geometry was displayed or it disappeared after 6 months. Any nodular or mass-like enhancement related with the resection cavity was considered as tumor relapse or progression. All early-mrs were evaluated independently by two neuroradiologists; the experience of the surgeons in the treatment of high grade gliomas.was equivalent The data obtained with early-mr examinations have been confirmed by serial MR controls at follow-up. Patients outcome was considered evaluating PFS and ST, as well as post-surgical therapies (radiotherapy, chemotherapy or both), and these data were correlated with the results of early-mr. Progression-free survival was defined as the time between the date of histologic diagnosis and the date of first evidence of disease progression or death. Overall survival was defined as the time between the date of histologic diagnosis and the date of patient's death, or it was censored at the date of the last follow-up. Survival curves were estimated with the Kaplan- Meier method. Differences between curves were tested by log-rank test. The Cox model was used for multivariate analysis of survival data. Results All the tumors presented hypointensity on T1 weighted-sequences, hyperintensity in T2 and FLAIR sequences, and non-homogeneous enhancement after Gd-DTPA administration by evaluation of the pre-surgical MRI. In early-mr the hyperintensity areas on the T1 sequences, before c.m. injection, near the site of surgery were linked to the presence of haemostatic agents (surgicel), a strong oxidant agent that accelerates methemoglobin formation, and that is considered responsible for the hyperintensity areas on the T1 sequences. After Gd-DTPA infusion all the areas showing enhancement were classified as residual tumor tissue (Figs 1, 2, 3). The early dural and leptomeningeal enhancement usually near the craniotomy site was considered as postsurgical modification. In two cases the FLAIR and T2 weighted sequences showed ischemic infarction without gyral enhancement after contrast medium infusion On early-mr, gross total resection was observed in 17 patients; sub-total and partial resection in 19 and in 11 patients, respectively. The median PFS was 6 months in gross total resection, 6 months in sub-total resection, and 3 months in partial resection. These differences were statistically significant (p<0.0001). The median ST was 16 months in patients with total resection, 13 months and 7 months in patients with subtotal and partial resection, respectively (P=0.0002) The ST at one year was 65% in patients with gross resection, and 53% in subtotal resection; only two patients with partial removal were still alive at one year (p< ) (Fig. 4). The median PFS was 3 months in patients with KPS < 80 and 6 months for KPS > 80 (P = ), while the median ST was 7 months in patients with KPS < 80 and 15 months for KPS > 80 (P = 0.001). Considering only the patients submitted to both radiotherapy and chemotherapy (35 pts.; 6 with partial, 15 with subtotal and 14 with gross total resection), median survival time was 7 months after partial removal, 15 months and 16 months respectively after subtotal and gross total surgical resection (p=0.03). Median survival was 15 months in patients who received post-operative radiotherapy and chemotherapy, 7 months in patients who received only one or no 178
3 Early Post-Operative MRI in Malignant Gliomas A B C D Fig. 1 - Gross Total resection of Glioblastoma. A: SE T1 weighted sequence after Gd- DTPA infusion and after biopsy show a mass with strong enhancement in the parasagittal left frontal lobe. B: SE T1 sequence after surgery and before mdc infusion shows a millimetric area of the hyperintensity signal in relationship to the hemostatic agents in relationships to the inferior site of the resection cavity. C: SE T1 after mdc shows post-surgical dural enhancement in the absence of residual tumors. D: SE T1 after six months shows a benign linear post-surgical enhancement contouring the resection cavity A B C D Fig. 2 - Fig. 2: Gross Total resection of Glioblastoma A: SE T1 weighted sequence after Gd-DTPA infusion shown a mass with strong enhancement in parasagittal left parietal lobe. B: SE T1 weighted sequence after surgery and before mdc infusion shows the hyperintensity signal in relationship to the hemostatic agents in the resection cavity. C: SE T1 after mdc, in the same plane, shows enhancement of the falx in absence of relapse. D: SE T1 after ten months shows a mass with enhancement after mdc in relationship to the relapse. 179
4 A. Vidiri et al. A B C Fig. 3: Subtotal resection of Anaplastic Astrocitoma A: SE T1 weighted sequence after Gd-DTPA infusion shows a necrotic mass with peripheral enhancement in the right parasagittal parietal lobe. B: SE T1 weighted sequence without contrast medium after surgery: there are no post-surgical effects rendering the interpretation of the MRI difficult. C: SE T1 after Gd-DTPA shows an area of enhancement near the ventricle correlated to the residual neoplastic tissue. related to survival, a multivariate analysis was performed: when KPS, combined radio- and chemotherapy treatment, and type of resection were tested only these two latter variables entered the model meaning that independently influence overall survival (P = and P = 0.004, respectively), while PFS was influenced by the extent of resection (P = 0.003) and KPS (P = 0.001) (Tab.I). Fig. 4 - Overall survival according to type of resection on early- MR. treatment (P= ): such an outcome confirms the importance of well tailored combined therapeutic strategies. Age of patients and histotype (probably due to the very limited number of anaplastic astrocytomas) in the present series do not seem to influence overall survival. In order to identify independent prognostic factors Discussion The prognosis of the patients affected by malignant glioma is poor; the median survival time after diagnosis reported in literature is approximately 12 months, and notwithstanding new diagnostic and surgical techniques these data do not differ from the results of the last 20 years. Some Authors have reported a 3-year survival rate, in particular for young patients affected by malignant gliomas, with good performance status and submitted to radical surgery (2). As reported by several Authors, the elements that improve the prognosis of 180
5 Early Post-Operative MRI in Malignant Gliomas Table I - Time to event: multivariate analysis P.F.S. univariate P.F.S. multivariate O.S. univariate O.S. multivariate Type of resection P < P =0.003 P = P = Gross vs partial 0.17 ( ) 0.21 ( ) 0.19 ( ) 0.21 ( ) Subtotal vs partial 0.25 ( ) 0.27 ( ) 0.27 ( ) 0.28 ( ) Treatment received P = 0.02 P = n.s. P = P = None or only one vs 2.26 ( ) 3.54 ( ) 3.23 ( ) both CT and RT K.P.S. P < P = P = P = n.s. < 80% vs > 80% 4.81 ( ) 4.09 ( ) 3.20 ( ) these patients are different and include age, KPS score, tumor location and the characteristics of preoperative MRI such as the presence of necrosis (1,6,7,8,9,10). As stated by some authors, radical surgery as well as KPS score and patients age reperesent important prognostic factors (3), but on the contrary Kowalczuk et al. (6) demonstrated that aggressive surgical resection did not lead to a significant increase in survival time. The role of the aggressive surgical treatment has not yet been defined, due to the fact that in several studies the extent of the resection has been only quantified on the basis of the surgical reports without imaging confirmation (11-12). Usually patients with GBM or AA are submitted to MR post-operative evaluation before the radiation therapy; in most cases this examination shows post-contrast enhancement due to hypervascularization and the disruption of the blood-brain barrier, with difficult findings about any possible residual tumor tissue. In order to evaluate the extention of surgical removal current diagnostic methods are ecotomography or MR and early CT or MR performed hrs after surgery (5). Results on animal models with serial CT-scans after brain tumor removal showed that the enhancement at the borders of resection cavity is not evident before the fifth day after surgery. Some Authors demonstrated that before the fifth post-surgery day enhancement reflects the residual gliomas only (13-14); for this reason the early-mr could minimize interpretative difficulties caused by post-surgical artifacts due to scar tissue. The aim of our study was to evaluate the role of MR performed during the first 24 hrs after surgery in order to determine residual tumor and the extension of surgical removal. Few studies utilized early-mr after surgery in the evaluation of malignant gliomas, demonstrating that parenchimal enhancement after c.m. infusion showed by early MR was always correlated to the presence of residual cancer tissue (3, 13-14); the other possible causes of the enhancement in early-mr are the early dural and leptomeningeal enhancement near the craniotomy site, enhancement of the ependymal layer, the choroid plexus or dilated veins at the operative site. Further potential diagnostic inaccuracy derives from the presence in the resection cavity of haemostatic agents such as hydrogen peroxide; this agent is a strong oxidant that accelerates methemoglobin formation, determining hyperintensity areas on T1 sequences before c.m. administration. For these reasons, in early-mr, we generally used two scan planes in T1 sequences before contrast medium infusion, usually axial and coronal planes in relation to tumor site; these images must be compared with those after c.m. infusion in the same planes in order to better define the residual neoplastic tissue showing enhancement after Gd-DTPA. We prefer perform early-mr in the first 24 hrs after surgery for the absence of enhancement due to possible ischemic lesion correlate to surgery, but we think that there is no difference in the utility of the early-mr performed within the first day versus the first three days as advocated by previous studies (3). Despite the small patient cohort, our results suggest significant correlation between the evidence of early MR and the extent of surgical removal. In fact when early MR showed no evidence of residual tumor tissue (gross total resection) median PFS was 6 months and median ST was 16 months; while in patients with subtotal resection PFS was 6 months and median ST was
6 A. Vidiri et al. months, and respectively 3 and 7 months for patients submitted to partial resection, with significant statistical correlation. Multivariate analysis confirms that the extent of tumor resection, as documented by the early-mr, and adjuvant treatment significantly influence survival time, being longer in patients submitted to gross-total removal and chemo-radiotherapy. Furthermore, gross total surgical removal and KPS > 80 positively influence progression free survival. Conclusion: Present data show, in accordance with other Authors (18,19,20), that early post-operative MR is a valuable method in determining residual tumor tissue, or gross total surgical removal; this technique minimizes interpretative inaccuracy caused by surgical artifacts and represents a necessary baseline measure to assess the activity of multimodality treatment of malignant gliomas. Acknowledgments: We thank Maurizio Abrugia for his technical assistance, Ivana Zardin and Mauro Di Giovanni for the photography support and P. Franke for assistance with the English version. References 1. Lacroix M., Abi-Said D., Fourney D.R., Gokaslan Z.L., Shi W., De Monte F. et al.: A multivariate analysis of 416 patients with glioblastomas multiforme: prognosis, extent of resection, and survival. J. Neurosur. 95: , Stupp R., Dietrich P.Y., Ostermann Kraljievic S.: Promising survival for patients with newly diagnosed glioblastoma multiforme with concomitant radiation plus temozolomide followed by adjuvant temozolomide. J. Clin. Oncol. 20: , Albert F.K., Forsting M., Sartor K. : Early postoperative magnetic resonance imaging after resection of malignant gliomas: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34: 45-61, Forsyth P.A.J., Petrov E., Mahallati H., Cairncross J.G., Brasher P., MacRae M.E. et al.: Prospective study of postoperative magnetic resonance imaging in patients with malignant gliomas. J Clin Oncol 15: , Becker G., Hofmann E., Woydt M., Huslsmann U., Maurer M., Lindner A. et al.: Postoperative neuroimaging of high-grade gliomas: comparison of transcranial sonography, magnetic resonance imaging, and computed tomography. Neurosurgery 44: , Kowalczuk A., Macdonald L., Amidei C., Dohrmann G., Erickson R.K., Hekmatpanah J. et al.: Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery 41: , Burger P.C., Green S.B.: Patients age, histological features and length of survival in patients with Glioblastoma Multiforme. Cancer 59: , Gilbert H., Kagan A.R., Cassidy K.: Glioblastoma Multiforme is not a uniform disease. Cancer 4:87-89, Hammoud M.A., Sawaya R., Shi W.: Prognostic significance of preoperative MRI scans in Glioblastoma Multiforme. J. Neuroncol. 27: 65-73, Nitta T., Sato K.: Prognostic implications of the extent of surgical resection in patients with intracranial malignant gliomas. Cancer 5: , Kreeth F.W., Warnke P.C., Scherenet R.: Surgical resection and radiation therapy versus biopsy and radiation therapy in treatment of Glioblastoma Multiforme. J. Neurosur. 78: , Curran W.J. Jr., Scott C.B., Horton J.: Does extent of surgery influence outcome for astrocytoma with atypical or anaplastic foci. A report from three Radiation Therapy Oncology Group (RTOG) trials. J. Neuroncol. 12: , Cairncross J.G., Pexman J.H.W., Rathbone M.P., Delmaestro R.F.: Postoperative contrast enhancement in patients with brain tumors. Ann. Neurol. 17: , Jeffries B.F., Kishore P.R.S., Singh K.S., Ghatak N.R., Krempa J.: Contrast enhancement in the postoperative brain. Radiology 139: , Ringe J.G., Clanton J.A., Price A.C., Herzer W.A., Allen J.H., Partain C.L. et al.: Evaluation of contrast enhanced MR imaging in a brain abscess model. A.J.N.R. 6: , Sze G.: New aplications of MR contrast agents in neuroradiology. Neuroradiology 32: , Elster A.D., Dipersio D.A.: Cranial post-operative site: assessment with contrast-enhanced MR imaging. Radiology 174:93-98, Ammirati M., Vick N.A., Liao Y., Ciric I., Mikhael M.A.: Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocitoma. Neurosurgery 21:21-26, Ciric I., Ammirati M., Vick N.A., Mikhael M.A.: Supratentorial gliomas: surgical consideration s and immediate postoperative results. Neurosurgery 21: , Ciric I., Vick N.A., Mikhael M.A., Cozzens J., Eller T., Walsh A.: Aggressive surgery for malignant supratentorial gliomas. Clin. Neurosurg. 36: , Received: February 20, 2006 Accepted after revision: March 1, 2006 Antonello Vidiri Department of Diagnostic Imaging, "Regina Elena" Cancer Insitute Via Elio Chianesi 53, Rome, Italy. vidiri@ifo.it Phone number:
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