Top

Published in:

01-05-2017 | Clinical Study

Biopsy targeting with dynamic contrast-enhanced versus standard neuronavigation MRI in glioma: a prospective double-blinded evaluation of selection benefits

Authors: Vera C. Keil, Bogdan Pintea, Gerrit H. Gielen, Susanne Greschus, Rolf Fimmers, Jürgen Gieseke, Matthias Simon, Hans H. Schild, Dariusch R. Hadizadeh

Published in: Journal of Neuro-Oncology | Issue 1/2017

Abstract

Current biopsy planning based on contrast-enhanced T1W (CET1W) or FLAIR sequences frequently delivers biopsy samples that are not in concordance with the gross tumor diagnosis. This study investigates whether the quantitative information of transfer constant K^trans maps derived from T1W dynamic contrast-enhanced MRI (DCE-MRI) can help enhance the quality of biopsy target selection in glioma. 28 patients with suspected glioma received MRI including DCE-MRI and a standard neuronavigation protocol of 3D FLAIR- and CET1W data sets (0.1 mmol/kg gadobutrol) at 3.0 T. After exclusion of five cases with no K^trans-elevation, 2–6 biopsy targets were independently selected by a neurosurgeon (samples based on standard imaging) and a neuroradiologist (samples based on kinetic parameter K^trans) per case and tissue samples corresponding to these targets were collected by a separate independent neurosurgeon. Standard technique and K^trans-based samples were rated for diagnostic concordance with the gross tumor resection reference diagnosis (67 WHO IV; 24 WHO III and II) by a neuropathologist blinded for selection mode. K^trans-based sample targets differed from standard technique sample targets in 90/91 cases. More K^trans-based than standard imaging-based samples could be extracted. Diagnoses from K^trans-based samples were more frequently concordant with the reference gross tumor diagnoses than those from standard imaging-based samples (WHO IV: 30/39 vs. 11/20; p = 0.08; WHO III/II: 12/13 vs. 6/11; p = 0.06). In 4/5 non-contrast-enhancing gliomas, K^trans-based selection revealed significantly more accurate samples than standard technique sample-selection (10/12 vs. 2/8 samples; p = 0.02). If K^trans elevation is present, K^trans-based biopsy targeting provides significantly more diagnostic tissue samples in non-contrast-enhancing glioma than selection based on CET1W and FLAIR-weighted images alone.

Paulus W, Peiffer J (1989) Intratumoral histologic heterogeneity of gliomas. A quantitative study. Cancer 64:442–447CrossRefPubMed

Coons SW, Johnson PC, Scheithauer BW, Yates AJ, Pearl DK (1997) Improving diagnostic accuracy and interobserver concordance in the classification and grading of primary gliomas. Cancer 79:1381–1393CrossRefPubMed

Kunz M, Thon N, Eigenbrod S, Hartmann C, Egensperger R, Herms J, Geisler J, La Fougere C, Lutz J, Linn J, Kreth S, von Deimling A, Tonn JC, Kretzschmar HA, Popperl G, Kreth FW (2011) Hot spots in dynamic (18)FET-PET delineate malignant tumor parts within suspected WHO grade II gliomas. Neuro Oncol 13:307–316. doi:10.1093/neuonc/noq196 CrossRefPubMedPubMedCentral

Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, Curtis C, Watts C, Tavare S (2013) Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 110:4009–4014. doi:10.1073/pnas.1219747110 CrossRefPubMedPubMedCentral

Ganslandt O, Stadlbauer A, Fahlbusch R, Kamada K, Buslei R, Blumcke I, Moser E, Nimsky C (2005) Proton magnetic resonance spectroscopic imaging integrated into image-guided surgery: correlation to standard magnetic resonance imaging and tumor cell density. Neurosurgery 56:291–298 (discussion 291–298)PubMed

Muragaki Y, Chernov M, Maruyama T, Ochiai T, Taira T, Kubo O, Nakamura R, Iseki H, Hori T, Takakura K (2008) Low-grade glioma on stereotactic biopsy: how often is the diagnosis accurate? Minim Invasive Neurosurg 51:275–279. doi:10.1055/s-0028-1082322 CrossRefPubMed

Hermann EJ, Hattingen E, Krauss JK, Marquardt G, Pilatus U, Franz K, Setzer M, Gasser T, Tews DS, Zanella FE, Seifert V, Lanfermann H (2008) Stereotactic biopsy in gliomas guided by 3-tesla 1H-chemical-shift imaging of choline. Stereotact Funct Neurosurg 86:300–307. doi:10.1159/000155232 CrossRefPubMed

Weber MA, Henze M, Tuttenberg J, Stieltjes B, Meissner M, Zimmer F, Burkholder I, Kroll A, Combs SE, Vogt-Schaden M, Giesel FL, Zoubaa S, Haberkorn U, Kauczor HU, Essig M (2010) Biopsy targeting gliomas: do functional imaging techniques identify similar target areas? Invest Radiol 45:755–768. doi:10.1097/RLI.0b013e3181ec9db0 CrossRefPubMed

Pafundi DH, Laack NN, Youland RS, Parney IF, Lowe VJ, Giannini C, Kemp BJ, Grams MP, Morris JM, Hoover JM, Hu LS, Sarkaria JN, Brinkmann DH (2013) Biopsy validation of 18F-DOPA PET and biodistribution in gliomas for neurosurgical planning and radiotherapy target delineation: results of a prospective pilot study. Neuro Oncol 15:1058–1067. doi:10.1093/neuonc/not002 CrossRefPubMedPubMedCentral

10.

Lopez WO, Cordeiro JG, Albicker U, Doostkam S, Nikkhah G, Kirch RD, Trippel M, Reithmeier T (2015) Correlation of (18)F-fluoroethyl tyrosine positron-emission tomography uptake values and histomorphological findings by stereotactic serial biopsy in newly diagnosed brain tumors using a refined software tool. Onco Targets Ther 8:3803–3815. doi:10.2147/OTT.S87126 CrossRefPubMedPubMedCentral

11.

Dammers R, Schouten JW, Haitsma IK, Vincent AJ, Kros JM, Dirven CM (2010) Towards improving the safety and diagnostic yield of stereotactic biopsy in a single centre. Acta Neurochir (Wien) 152:1915–1921. doi:10.1007/s00701-010-0752-0 CrossRef

12.

Roessler K, Gatterbauer B, Becherer A, Paul M, Kletter K, Prayer D, Hoeftberger R, Hainfellner J, Asenbaum S, Knosp E (2007) Surgical target selection in cerebral glioma surgery: linking methionine (MET) PET image fusion and neuronavigation. Minim Invasive Neurosurg 50:273–280. doi:10.1055/s-2007-991143 CrossRefPubMed

13.

Chaskis C, Stadnik T, Michotte A, Van Rompaey K, D’Haens J (2006) Prognostic value of perfusion-weighted imaging in brain glioma: a prospective study. Acta Neurochir (Wien) 148: 277–285. doi:10.1007/s00701-005-0718-9 (discussion 285)CrossRef

14.

Son BC, Kim MC, Choi BG, Kim EN, Baik HM, Choe BY, Naruse S, Kang JK (2001) Proton magnetic resonance chemical shift imaging (1H CSI)-directed stereotactic biopsy. Acta Neurochir (Wien) 143:45–49 (discussion 49–50)CrossRef

15.

Lefranc M, Monet P, Desenclos C, Peltier J, Fichten A, Toussaint P, Sevestre H, Deramond H, Le Gars D (2012) Perfusion MRI as a neurosurgical tool for improved targeting in stereotactic tumor biopsies. Stereotact Funct Neurosurg 90:240–247. doi:10.1159/000338092 CrossRefPubMed

16.

Knopp EA, Cha S, Johnson G, Mazumdar A, Golfinos JG, Zagzag D, Miller DC, Kelly PJ, Kricheff II (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798. doi:10.1148/radiology.211.3.r99jn46791 CrossRefPubMed

17.

Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, Larsson HB, Lee TY, Mayr NA, Parker GJ, Port RE, Taylor J, Weisskoff RM (1999) Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 10:223–232CrossRefPubMed

18.

Roberts HC, Roberts TP, Brasch RC, Dillon WP (2000) Quantitative measurement of microvascular permeability in human brain tumors achieved using dynamic contrast-enhanced MR imaging: correlation with histologic grade. AJNR Am J Neuroradiol 21:891–899PubMed

19.

Provenzale JM, Mukundan S, Dewhirst M (2005) The role of blood-brain barrier permeability in brain tumor imaging and therapeutics. AJR Am J Roentgenol 185:763–767. doi:10.2214/ajr.185.3.01850763 CrossRefPubMed

20.

Zhang N, Zhang L, Qiu B, Meng L, Wang X, Hou BL (2012) Correlation of volume transfer coefficient Ktrans with histopathologic grades of gliomas. J Magn Reson Imaging 36:355–363. doi:10.1002/jmri.23675 CrossRefPubMedPubMedCentral

21.

Dujardin MI, Sourbron SP, Chaskis C, Verellen D, Stadnik T, de Mey J, Luypaert R (2012) Quantification of cerebral tumour blood flow and permeability with T1-weighted dynamic contrast enhanced MRI: a feasibility study. J Neuroradiol 39:227–235. doi:10.1016/j.neurad.2011.07.001 CrossRefPubMed

22.

Jia ZZ, Geng DY, Liu Y, Chen XR, Zhang J (2013) Microvascular permeability of brain astrocytoma with contrast-enhanced magnetic resonance imaging: correlation analysis with histopathologic grade. Chin Med J (Engl) 126:1953–1956

23.

Tan CH, Hobbs BP, Wei W, Kundra V (2015) Dynamic contrast-enhanced MRI for the detection of prostate cancer: meta-analysis. AJR Am J Roentgenol 204:W439–W448. doi:10.2214/AJR.14.13373 CrossRefPubMedPubMedCentral

24.

An YS, Kang DK, Jung YS, Han S, Kim TH (2015) Tumor metabolism and perfusion ratio assessed by 18F-FDG PET/CT and DCE-MRI in breast cancer patients: correlation with tumor subtype and histologic prognostic factors. Eur J Radiol 84:1365–1370. doi:10.1016/j.ejrad.2015.03.026 CrossRefPubMed

25.

Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820. doi:10.1007/s00401-016-1545-1 CrossRefPubMed

26.

Wang HZ, Riederer SJ, Lee JN (1987) Optimizing the precision in T1 relaxation estimation using limited flip angles. Magn Reson Med 5:399–416CrossRefPubMed

27.

Rohrer M, Bauer H, Mintorovitch J, Requardt M, Weinmann HJ (2005) Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol 40:715–724CrossRefPubMed

28.

Della Puppa A, Persano L, Masi G, Rampazzo E, Sinigaglia A, Pistollato F, Denaro L, Barzon L, Palu G, Basso G, Scienza R, d’Avella D (2012) MGMT expression and promoter methylation status may depend on the site of surgical sample collection within glioblastoma: a possible pitfall in stratification of patients? J Neurooncol 106:33–41. doi:10.1007/s11060-011-0639-9 CrossRefPubMed

29.

Aker FV, Hakan T, Karadereler S, Erkan M (2005) Accuracy and diagnostic yield of stereotactic biopsy in the diagnosis of brain masses: comparison of results of biopsy and resected surgical specimens. Neuropathology 25:207–213CrossRefPubMed

30.

Pedeutour-Braccini Z, Burel-Vandenbos F, Goze C, Roger C, Bazin A, Costes-Martineau V, Duffau H, Rigau V (2015) Microfoci of malignant progression in diffuse low-grade gliomas: towards the creation of an intermediate grade in glioma classification? Virchows Arch 466:433–444. doi:10.1007/s00428-014-1712-5 CrossRefPubMed

31.

Widhalm G, Kiesel B, Woehrer A, Traub-Weidinger T, Preusser M, Marosi C, Prayer D, Hainfellner JA, Knosp E, Wolfsberger S (2013) 5-Aminolevulinic acid induced fluorescence is a powerful intraoperative marker for precise histopathological grading of gliomas with non-significant contrast-enhancement. PLoS ONE 8:e76988. doi:10.1371/journal.pone.0076988 CrossRefPubMedPubMedCentral

32.

Cordova JS, Shu HK, Liang Z, Gurbani SS, Cooper LA, Holder CA, Olson JJ, Kairdolf B, Schreibmann E, Neill SG, Hadjipanayis CG, Shim H (2016) Whole-brain spectroscopic MRI biomarkers identify infiltrating margins in glioblastoma patients. Neuro Oncol 18:1180–1189. doi:10.1093/neuonc/now036 CrossRefPubMed

33.

Jia ZZ, Gu HM, Zhou XJ, Shi JL, Li MD, Zhou GF, Wu XH (2015) The assessment of immature microvascular density in brain gliomas with dynamic contrast-enhanced magnetic resonance imaging. Eur J Radiol 84:1805–1809. doi:10.1016/j.ejrad.2015.05.035 CrossRefPubMed

34.

van Osch MJ, van der Grond J, Bakker CJ (2005) Partial volume effects on arterial input functions: shape and amplitude distortions and their correction. J Magn Reson Imaging 22:704–709. doi:10.1002/jmri.20455 CrossRefPubMed

35.

van der Schaaf I, Vonken EJ, Waaijer A, Velthuis B, Quist M, van Osch T (2006) Influence of partial volume on venous output and arterial input function. AJNR Am J Neuroradiol 27:46–50PubMed

36.

Calamante F (2013) Arterial input function in perfusion MRI: a comprehensive review. Prog Nucl Magn Reson Spectrosc 74:1–32. doi:10.1016/j.pnmrs.2013.04.002 CrossRefPubMed

37.

Hansen AE, Pedersen H, Rostrup E, Larsson HB (2009) Partial volume effect (PVE) on the arterial input function (AIF) in T1-weighted perfusion imaging and limitations of the multiplicative rescaling approach. Magn Reson Med 62:1055–1059. doi:10.1002/mrm.22098 CrossRefPubMed

38.

Haroon HA, Buckley DL, Patankar TA, Dow GR, Rutherford SA, Baleriaux D, Jackson A (2004) A comparison of Ktrans measurements obtained with conventional and first pass pharmacokinetic models in human gliomas. J Magn Reson Imaging 19:527–536. doi:10.1002/jmri.20045 CrossRefPubMed

39.

Heisen M, Fan X, Buurman J, van Riel NA, Karczmar GS, ter Haar Romeny BM (2010) The influence of temporal resolution in determining pharmacokinetic parameters from DCE-MRI data. Magn Reson Med 63:811–816. doi:10.1002/mrm.22171 CrossRefPubMedPubMedCentral

40.

Lavini C, Verhoeff JJ (2010) Reproducibility of the gadolinium concentration measurements and of the fitting parameters of the vascular input function in the superior sagittal sinus in a patient population. Magn Reson Imaging 28:1420–1430. doi:10.1016/j.mri.2010.06.017 CrossRefPubMed

41.

Sourbron SP, Buckley DL (2013) Classic models for dynamic contrast-enhanced MRI. NMR Biomed 26:1004–1027. doi:10.1002/nbm.2940 CrossRefPubMed

42.

van Niekerk CG, van der Laak JA, Hambrock T, Huisman HJ, Witjes JA, Barentsz JO, Hulsbergen-van de Kaa CA (2014) Correlation between dynamic contrast-enhanced MRI and quantitative histopathologic microvascular parameters in organ-confined prostate cancer. Eur Radiol 24:2597–2605. doi:10.1007/s00330-014-3301-z CrossRefPubMed

43.

Jia Z, Geng D, Xie T, Zhang J, Liu Y (2012) Quantitative analysis of neovascular permeability in glioma by dynamic contrast-enhanced MR imaging. J Clin Neurosci 19:820–823. doi:10.1016/j.jocn.2011.08.030 CrossRefPubMed

44.

Jackson A, Jayson GC, Li KL, Zhu XP, Checkley DR, Tessier JJ, Waterton JC (2003) Reproducibility of quantitative dynamic contrast-enhanced MRI in newly presenting glioma. Br J Radiol 76:153–162. doi:10.1259/bjr/70653746 CrossRefPubMed

45.

Lavini C, Verhoeff JJ, Majoie CB, Stalpers LJ, Richel DJ, Maas M (2011) Model-based, semiquantitative and time intensity curve shape analysis of dynamic contrast-enhanced MRI: a comparison in patients undergoing antiangiogenic treatment for recurrent glioma. J Magn Reson Imaging 34:1303–1312. doi:10.1002/jmri.22742 CrossRefPubMed

46.

Weber MA, Zoubaa S, Schlieter M, Juttler E, Huttner HB, Geletneky K, Ittrich C, Lichy MP, Kroll A, Debus J, Giesel FL, Hartmann M, Essig M (2006) Diagnostic performance of spectroscopic and perfusion MRI for distinction of brain tumors. Neurology 66:1899–1906. doi:10.1212/01.wnl.0000219767.49705.9c CrossRefPubMed

Title: Biopsy targeting with dynamic contrast-enhanced versus standard neuronavigation MRI in glioma: a prospective double-blinded evaluation of selection benefits
Authors: Vera C. Keil
Bogdan Pintea
Gerrit H. Gielen
Susanne Greschus
Rolf Fimmers
Jürgen Gieseke
Matthias Simon
Hans H. Schild
Dariusch R. Hadizadeh
Publication date: 01-05-2017
Publisher: Springer US
Published in: Journal of Neuro-Oncology / Issue 1/2017
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-017-2424-x

At a glance: The STEP trials

Springer Medicine

Biopsy targeting with dynamic contrast-enhanced versus standard neuronavigation MRI in glioma: a prospective double-blinded evaluation of selection benefits

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2017

Primary cranial sarcomatoid carcinoma

Cerebrospinal fluid dissemination of high-grade gliomas following boron neutron capture therapy occurs more frequently in the small cell subtype of IDH1R132H mutation-negative glioblastoma

IDH mutation and 1p19q codeletion distinguish two radiological patterns of diffuse low-grade gliomas

Long-term neuropsychological follow-up of young children with medulloblastoma treated with sequential high-dose chemotherapy and irradiation sparing approach

Flow arrest intra-arterial delivery of small TAT-decorated and neutral micelles to gliomas

Does early resection of presumed low-grade glioma improve survival? A clinical perspective