Abstract
Grade II gliomas grow slowly and linearly (at rates about 4 mm/year) before undergoing anaplastic transformation. In order to analyze how surgery may affect radiological grade II glioma kinetics, we restrospectively reviewed our national database searching for patients operated on for a supratentorial grade II glioma between 1997 and 2007. We selected patients with at least two postoperative MRI with a minimal delay of 6 months. For each patient, postoperative residues were segmented on successive MRIs. Velocities of diameter expansion were estimated by linear regression of mean diameter evolution for each patient. Fifty-four patients fulfilled inclusion criteria. Median postoperative follow-up was 1.6 years with, on average, 3.4 MRI examinations per patient. Postoperative growth rates of mean diameter were normally distributed, around a mean value of 4.3 mm/year (SD = 3.2 mm/year). Statistical analysis showed no difference between this distribution and the distribution of preoperative growth rates in a previous series of 143 grade II gliomas. For a subset of 23 patients, delay between first MRI and surgery made it possible to estimate also preoperative growth rates. Intrapatient comparison revealed that growth rates were grossly unchanged for 80% of cases. In summary, inter- and intrapatient comparison of pre- and postoperative growth rates proves that surgery does not change grade II glioma dynamics, thus, acting as a cytoreduction.
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Bynevelt M, Britton J, Seymour H, MacSweeney E, Thomas N, Sandhu K (2001) FLAIR imaging in the follow-up of low-grade gliomas: time to dispense with the dual-echo? Neuroradiology 43(2):129–133
Hofer SO, Shrayer D, Reichner JS, Hoekstra HJ, Wanebo HJ (1998) Wound-induced tumor progression: a probable role in recurrence after tumor resection. Arch Surg 133(4):383–389
Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S, Knopp EA, Zagzag D (2003) Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 24(10):1989–1998
Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord EC Jr, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53(4):524–528
Mandonnet E, Pallud J, Clatz O, Taillandier L, Konukoglu E, Duffau H, Capelle L (2008) Computational modeling of the WHO grade II glioma dynamics: principles and applications to management paradigm. Neurosurg Rev 31(3):263–269
Martins-Green M, Boudreau N, Bissell MJ (1994) Inflammation is responsible for the development of wound-induced tumors in chickens infected with Rous sarcoma virus. Cancer Res 54(16):4334–4341
McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, Olivi A, Brem H, Quinones-Hinojosa A (2008) Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 63(4):700–707 author reply, pp 707–708
Pallud J, Mandonnet E, Duffau H, Kujas M, Guillevin R, Galanaud D, Taillandier L, Capelle L (2006) Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas. Ann Neurol 60(3):380–383
Pallud J, Capelle L, Taillandier L, Fontaine D, Mandonnet E, Guillevin R, Bauchet L, Peruzzi P, Laigle-Donadey F, Kujas M, Guyotat J, Baron MH, Mokhtari K, Duffau H (2009) Prognostic significance of imaging contrast enhancement for WHO grade II gliomas. Neuro Oncol, 11:176–182
Pauleit D, Floeth F, Hamacher K, Riemenschneider MJ, Reifenberger G, Muller HW, Zilles K, Coenen HH, Langen KJ (2005) O-(2-[18F]fluoroethyl)-L-tyrosine PET combined with MRI improves the diagnostic assessment of cerebral gliomas. Brain 128(Pt 3):678–687
Pirotte B, Goldman S, Dewitte O, Massager N, Wikler D, Lefranc F, Ben Taib NO, Rorive S, David P, Brotchi J, Levivier M (2006) Integrated positron emission tomography and magnetic resonance imaging-guided resection of brain tumors: a report of 103 consecutive procedures. J Neurosurg 104(2):238–253
Rees J, Watt H, Jager HR, Benton C, Tozer D, Tofts P, Waldman A (2008) Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol
Ricard D, Kaloshi G, Amiel-Benouaich A, Lejeune J, Marie Y, Mandonnet E, Kujas M, Mokhtari K, Taillibert S, Laigle-Donadey F, Carpentier AF, Omuro A, Capelle L, Duffau H, Cornu P, Guillevin R, Sanson M, Hoang-Xuan K, Delattre JY (2007) Dynamic history of low-grade gliomas before and after temozolomide treatment. Ann Neurol 61(5):484–490
Sanai N, Berger MS (2008) Glioma extent of resection and its impact on patient outcome. Neurosurgery 62(4):753–764 discussion 264–266
Smith JS, Cha S, Mayo MC, McDermott MW, Parsa AT, Chang SM, Dillon WP, Berger MS (2005) Serial diffusion-weighted magnetic resonance imaging in cases of glioma: distinguishing tumor recurrence from postresection injury. J Neurosurg 103(3):428–438
Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26(8):1338–1345
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Marc Sindou, Lyon, France
This work is interesting as it deals with a subject only scarcely approached in the oncologic literature, namely the speed of tumor growth of gliomas grade II. In addition, it explains well the method of quantification: the velocity of diametric evolution (VDE); the main result of the study is that resective surgery is effective in delaying the volumetric—i.e., compressive—effects of the tumor. However, there no proof that resection delays anaplastic transformation. This has to be investigated through (randomized) prospective studies.
Benoit JM Pirotte, Brussels, Belgium
In this paper, Mandonnet and coauthors investigate whether surgical resection interferes or not on grade II glioma kinetics. The objective of that study might be surprising, and the conclusion that surgical resection should probably not act on tumor growth might appear as an evident statement to everyone. However, the idea deserved to be measured so far. Such study confirms once more the major role of surgery in the therapy of gliomas. The study design is very simple and accurate. The methodology used seems very appropriate and sustains the conclusion. Two limitations might, however, weaken the message of this very exciting work. First, the 54 cases studied by the authors represent less than 20% of all cases found in their initial database. We, therefore, need to extrapolate very carefully the current conclusion to the whole population. The selection bias, due to unavailability of Digital Imaging and Communications in Medicine images, should not alter significantly the data. Secondly, the FLAIR MRI signal used here for measuring tumor volumes might not exactly and accurately reflect the actual tumor boundaries in most cases. Indeed, in up to 80% of WHO grade II gliomas, FLAIR signal extent is found different (smaller in about two thirds of them or larger in about one third) than the volume of 18F-fluoroethyltyrosine or 11C-methionine uptake area on PET images (Pauleit D. et al., Brain 128:678–687, 2005; Pirotte B. et al., J Neurosurg 104:238–253, 2006). Different studies comparing MR and PET signals to local histology in stereotactic conditions have confirmed the higher specificity of methionine on MR signals as a marker of tumor tissue and as tool for tumor delineation. FLAIR MR signal, although being the best MRI signal to represent tumor boundaries, might, therefore, provide false-negative and false-positive signals for tumor tissue detection. In this paper, however, since the FLAIR imaging was used repeatedly for longitudinal comparison, its intrinsic limitations might not have consequence on the present results. We would strongly encourage the authors to keep on studying this issue in the future by using other detection tracers (metabolic or others) presenting higher specificity of tumor tissue.
Raimund Firsching, Magdeburg, Germany
Mandonnet and collaborators present an ambitious analysis of the biological activity of grade II gliomas. The data from preoperative MRI and postoperative repeat MRI indicate a mostly unchanged growth rate before and after partial surgical removal of the tumor. They concluded that the more tumor cells were removed, the less likely were an anaplastic malignant transformation. This appears reasonable, and as there is some uncertainty concerning the indication and extent of surgery of grade II gliomas in the neurosurgical community, this study is of great importance. The authors are to be congratulated on their work.
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Mandonnet, E., Pallud, J., Fontaine, D. et al. Inter- and intrapatients comparison of WHO grade II glioma kinetics before and after surgical resection. Neurosurg Rev 33, 91–96 (2010). https://doi.org/10.1007/s10143-009-0229-x
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DOI: https://doi.org/10.1007/s10143-009-0229-x