Rofo 2017; 189(06): 519-526
DOI: 10.1055/s-0043-106189
Neuroradiology
© Georg Thieme Verlag KG Stuttgart · New York

Accuracy of High-Field Intraoperative MRI in the Detectability of Residual Tumor in Glioma Grade IV Resections

Treffsicherheit der Intraoperativen MR-Bildgebung (ioMRI)in der Nachweisbarkeit von Resttumorgewebe zur Resektion hochgradiger (Grad IV) Gliome
Volker Heßelmann
1   Radiology/Neurologie, Asklepios-Klinik Hamburg-Nord, Hamburg, Germany
,
Ann-Kathrin Mager
1   Radiology/Neurologie, Asklepios-Klinik Hamburg-Nord, Hamburg, Germany
,
Claudia Goetz
2   Department of Neurosurgery, Asklepios Klinik Nord, Hamburg, Germany
,
Oliver Detsch
3   Department of Anaesthesiology and Intensive Care Medicine, Asklepios Klinik Nord, Hamburg, Germany
,
Hannah-Katharina Theisgen
4   Department of Neurosurgery, Universitatsklinikum Schleswig-Holstein Campus Kiel, Germany
,
Michael Friese
5   Department of Pathology and Neuropahthology, Asklepios Klinik Nord, Hamburg, Germany
,
Wolfram Schwindt
6   Department of Clinical Radiology, University Hospital Münster, Münster, Germany
,
Joachim Gottschalk
5   Department of Pathology and Neuropahthology, Asklepios Klinik Nord, Hamburg, Germany
,
Paul Kremer
2   Department of Neurosurgery, Asklepios Klinik Nord, Hamburg, Germany
› Institutsangaben
Weitere Informationen

Publikationsverlauf

17. Oktober 2016

01. März 2017

Publikationsdatum:
07. Juni 2017 (online)

Abstract

Objective To assess the sensitivity/specificity of tumor detection by T1 contrast enhancement in intraoperative MRI (ioMRI) in comparison to histopathological assessment as the gold standard in patients receiving surgical resection of grade IV glioblastoma.

Materials and Methods 68 patients with a primary or a recurrent glioblastoma scheduled for surgery including fluorescence guidance and neuronavigation were included (mean age: 59 years, 26 female, 42 male patients). The ioMRI after the first resection included transverse FLAIR, DWI, T2-FFE and T1 – 3 d FFE +/- GD-DPTA. The second resection was performed whenever residual contrast-enhancing tissue was detected on ioMRI. Resected tissue samples were histopathologically evaluated (gold standard). Additionally, we evaluated the early postoperative MRI scan acquired within 48 h post-OP for remaining enhancing tissue and compared them with the ioMRI scan.

Results In 43 patients ioMRI indicated residual tumorous tissue, which could be confirmed in the histological specimens of the second resection. In 16 (4 with recurrent, 12 with primary glioblastoma) cases, ioMRI revealed truly negative results without residual tumor and follow-up MRI confirmed complete resection. In 7 cases (3 with recurrent, 4 with primary glioblastoma) ioMRI revealed a suspicious result without tumorous tissue in the histopathological workup. In 2 (1 for each group) patients, residual tumorous tissue was detected in spite of negative ioMRI. IoMRI had a sensitivity of 95 % (94 % recurrent and 96 % for primary glioblastoma) and a specificity of 69.5 % (57 % and 75 %, respectively). The positive predictive value was 86 % (84 % for recurrent and 87 % for primary glioblastoma), and the negative predictive value was 88 % (80 % and 92 %, respectively).

Conclusion ioMRI is effective for detecting remaining tumorous tissue after glioma resection. However, scars and leakage of contrast agent can be misleading and limit specificity.

Key points

  • Intraoperative MRI (ioMRI) presents with a high sensitivity for residual contrast-enhancing tumorous tissue during glioma resection.

  • Contrast leakage due to bleeding and scars with reactive contrast enhancement can cause possible misleading artifacts in ioMRI, leading to a limited specificity of ioMRI.

  • Bleeding control in glioma resection is crucial for successful usage of ioMRO for glioma resection.

Citation Format

  • Heßelmann V, Mager A, Goetz C et al. Accuracy of High-Field Intraoperative MRI in the Detectability of Residual Tumor in Glioma Grade IV Resections. Fortschr Röntgenstr 2017; 189: 519 – 526

Zusammenfassung

Einleitung Ziel der Studie ist die Untersuchung der Sensitivität und Spezifität der intraoperativen MRT (ioMRI) zum Nachweis von Resttumorgewebe auf der Basis der T1-Wichtung nach GD-DPTA im Vergleich zur Histopathologie (Goldstandard) bei neurochirurgischen Operationen von WHO Grad IV Gliomen.

Material und Methoden 68 Patienten (Durchschnittsalter 59 Jahre, 26 weiblich, 42 männlich mit primären oder rezidivierenden WHO Grad IV Gliomen erhielten gleichzeitig eine floureszenz-, eine neuronavigations- und ein ioMRI-gestützte Resektion. Bei Nachweis von KM-Anreicherungen in T1-Wichtung in der ioMRI erfolgte eine Nachresektion, deren histopathologischen Proben (Goldstandard) von einem Neuropathologen bewertet wurde. Nach kompletter Entfernung des flouresziierenden oder MR-tomografisch nachweisbaren Resttumorgewebes wurde die OP beendet. Zusätzlich wurde die postoperative MRT zum Nachweis residueller KM-Anreicherungen mit der ioMRI verglichen und als in die Auswertung mit einbezogen.

Ergebnisse Bei 43 Patienten wurde in der ioMRI Resttumorgewebe nachgewiesen und histopathologisch bestätigt. In 16 Fällen war die zweite ioMRI ohne histopathologischen Nachweis von Resttumor richtig negativ (4 Rezidive, 12 Primärtumore). In 7 Fällen (3 Rezidive, 4 Primärtumore) war der ioMRT Befund falsch positiv, in zwei Patienten (1 Rezidiv, 1 Primärtumor) falsch negativ. Für alle Patienten betrug die Sensitivität 95 %, die Spezifität 69,5 %, für die Rezidive 94 % und 57 % und für die Primärtumore 96 % und 75 %. Der positive Vorhersagewert war 86 %, der negative Vorhersagewert 88 % für alle Patienten, 84 % und 80 % für die Rezidive und 87 und 92 % für die Primärtumore.

Schlussfolgerung Die ioMRI ist sensitiv im Nachweis von kontrastmittelanreicherndem Resttumorgewebes nach Gliomresektion. Narbengewebe und Kontrastmittelleckagen durch Blutaustritt führen zu Fehlinterpretationen und reduzieren die Spezifität.

Kernaussagen

  • Die ioMRI ist hochsensitiv im Nachweis residueller, kontrastmittelanreichender Resttumoranteile in der Gliomresektion

  • Artefakte durch blutungsbedingte Kontrastmittelaustritte und reaktive Kontrastmittelanreicherungen durch Narbengewebe limitieren die Spezifität der ioMRI

  • Eine suffiziente Blutungsstillung ist entscheidend für eine hohe Aussagekraft der ioMRI

 
  • References

  • 1 Coburger J. Engelke J. Scheuerle A. et al. Tumor detection with 5-aminolevulinic acid fluorescence and Gd-DTPA-enhanced intraoperative MRI at the border of contrast-enhancing lesions: a prospective study based on histopathological assessment. Neurosurg Focus 2014; 36: E3
  • 2 Coburger J. Hagel V. Wirtz CR. et al. Surgery for Glioblastoma: Impact of the Combined Use of 5-Aminolevulinic Acid and Intraoperative MRI on Extent of Resection and Survival. PLoS One 2015; 10: e0131872
  • 3 Stummer W. Novotny A. Stepp H. et al. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. Journal of Neurosurgery 2000; 93: 1003-1013
  • 4 Wirtz CR. Albert FK. Schwaderer M. et al. The benefit of neuronavigation for neurosurgery analyzed by its impact on glioblastoma surgery. Neurol Res 2000; 22: 354-360
  • 5 Eyupoglu IY. Hore N. Savaskan NE. et al. Improving the extent of malignant glioma resection by dual intraoperative visualization approach. PLoS One 2012; 7: e44885
  • 6 Kreth FW. Berlis A. Spiropoulou V. et al. The role of tumor resection in the treatment of glioblastoma multiforme in adults. Cancer 1999; 86: 2117-2123
  • 7 Schucht P. Beck J. Abu-Isa J. et al. Gross total resection rates in contemporary glioblastoma surgery: results of an institutional protocol combining 5-aminolevulinic acid intraoperative fluorescence imaging and brain mapping. Neurosurgery 2012; 71: 927-935 ; discussion 935–926
  • 8 Stummer W. Pichlmeier U. Meinel T. et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006; 7: 392-401
  • 9 Neidert MC. Hostettler IC. Burkhardt JK. et al. The influence of intraoperative resection control modalities on survival following gross total resection of glioblastoma. Neurosurg Rev 2016; 39: 401-409
  • 10 Stummer W. Novotny A. Stepp H. et al. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. Journal of neurosurgery 2000; 93: 1003-1013
  • 11 Roberts DW. Valdes PA. Harris BT. et al. Coregistered fluorescence-enhanced tumor resection of malignant glioma: relationships between delta-aminolevulinic acid-induced protoporphyrin IX fluorescence, magnetic resonance imaging enhancement, and neuropathological parameters. Clinical article. Journal of neurosurgery 2011; 114: 595-603
  • 12 Kubben PL. van Santbrink H. Intraoperative magnetic resonance imaging for high grade glioma resection: Evidence-based or wishful thinking?. Surg Neurol Int 2013; 4: 1
  • 13 Tronnier VM. Wirtz CR. Knauth M. et al. Intraoperative diagnostic and interventional magnetic resonance imaging in neurosurgery. Neurosurgery 1997; 40: 891-900 ; discussion 900–892
  • 14 Steinmeier R. Fahlbusch R. Ganslandt O. et al. Intraoperative magnetic resonance imaging with the magnetom open scanner: concepts, neurosurgical indications, and procedures: a preliminary report. Neurosurgery 1998; 43: 739-747 ; discussion 747–738
  • 15 Martin AJ. Hall WA. Liu H. et al. Brain tumor resection: intraoperative monitoring with high-field-strength MR imaging-initial results. Radiology 2000; 215: 221-228
  • 16 Senft C. Bink A. Franz K. et al. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 2011; 12: 997-1003
  • 17 Gessler F. Forster MT. Duetzmann S. et al. Combination of Intraoperative Magnetic Resonance Imaging and Intraoperative Fluorescence to Enhance the Resection of Contrast Enhancing Gliomas. Neurosurgery 2015; 77: 16-22 ; discussion 22
  • 18 Coburger J. Scheuerle A. Kapapa T. et al. Sensitivity and specificity of linear array intraoperative ultrasound in glioblastoma surgery: a comparative study with high field intraoperative MRI and conventional sector array ultrasound. Neurosurg Rev 2015; 38: 499-509 ; discussion 509
  • 19 Liang D. Schulder M. The role of intraoperative magnetic resonance imaging in glioma surgery. Surg Neurol Int 2012; 3: S320-S327
  • 20 Kubben PL. Scholtes F. Schijns OE. et al. Intraoperative magnetic resonance imaging versus standard neuronavigation for the neurosurgical treatment of glioblastoma: A randomized controlled trial. Surg Neurol Int 2014; 5: 70
  • 21 Stummer W. Commentary: Combining 5-Aminolevulinic Acid Fluorescence and Intraoperative Magnetic Resonance Imaging in Glioblastoma Surgery: A Histology-Based Evaluation. Neurosurgery 2016; 78: 484-486
  • 22 Lacroix M. Abi-Said D. Fourney DR. et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001; 95: 190-198
  • 23 Albert FK. Forsting M. Sartor K. et al. Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 1994; 34: 45-60 ; discussion 60–41
  • 24 Mager AK. Theisgen H. Götz C. et al. Treffsicherheit der intraoperativen MR-Bildgebung in der Nachweisbarkeit von Resttumorgewebe zur Resektion hochgradiger (Grad IV) Gliome. Clinical neuroradiology 2014; 24 (Suppl. 01) 1-106
  • 25 Stummer W. Stepp H. Moller G. et al. Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue. Acta Neurochir (Wien) 1998; 140: 995-1000
  • 26 van den Bent MJ. Wefel JS. Schiff D. et al. Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol 2011; 12: 583-593
  • 27 Ozduman K. Yildiz E. Dincer A. et al. Using intraoperative dynamic contrast-enhanced T1-weighted MRI to identify residual tumor in glioblastoma surgery. Journal of neurosurgery 2014; 120: 60-66
  • 28 Engelhorn T. Schwarz MA. Hess A. et al. Definition of K(trans) and FA thresholds for better assessment of experimental glioma using high-field MRI: a feasibility study. Clinical neuroradiology 2014; 24: 337-345
  • 29 Akbari H. Macyszyn L. Da X. et al. Imaging Surrogates of Infiltration Obtained Via Multiparametric Imaging Pattern Analysis Predict Subsequent Location of Recurrence of Glioblastoma. Neurosurgery 2016; 78: 572-580
  • 30 Heckl S. Feigl GC. Honegger J. et al. [Intraoperative MRI (iMRI) in neurosurgery: a radiological point of view]. Rofo 2012; 184: 1-5