J Neurol Surg A Cent Eur Neurosurg 2014; 75(06): 434-441
DOI: 10.1055/s-0034-1372436
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Navigable Intraoperative Ultrasound and Fluorescence-Guided Resections Are Complementary in Resection Control of Malignant Gliomas: One Size Does Not Fit All

Aliasgar Moiyadi
1   Department of Neurosurgery, Tata Memorial Centre, Mumbai, India
,
Prakash Shetty
1   Department of Neurosurgery, Tata Memorial Centre, Mumbai, India
› Author Affiliations
Further Information

Publication History

09 November 2013

03 January 2014

Publication Date:
27 June 2014 (online)

Abstract

Introduction Conventional imaging (intraoperative ultrasound and intraoperative magnetic resonance imaging) as well as enhanced visualization (aminolevulinic acid [ALA]-based fluorescence-guided resection) have both been used to improve the resection of malignant gliomas. Each modality has its pros and cons and may not be suitable for all cases. We describe our experience with these two complementary techniques.

Methods Eight patients underwent resection for malignant gliomas using combined navigable three-dimensional ultrasound (3D-US) and ALA-induced fluorescence. These were analyzed for magnetic resonance imaging characteristics, resectability, and extent of resection. The utility of navigable 3D-US and the fluorescence were assessed for each case to stratify cases that may benefit from either or both of these techniques.

Results Four subjects had predominant contrast-enhancing potentially resectable gliomas. Intraoperative strong fluorescence was seen, which was the primary guide for resection control. Navigable 3D-US was additionally useful for planning the craniotomy and localizing the subcortical lesions. All four tumors were gross-totally excised. Four other tumors were minimally enhancing and diffuse. Fluorescence was patchy and not used for resection control; instead, navigable 3D-US was the primary guide for resection. However, the fluorescence helped locating the focally higher grade parts within the tumors. Gross-total resection could be achieved in one patient.

Conclusions Navigable 3D-US and ALA-induced fluorescence provide information regarding different aspects of tumor extent and combined together enhance the extent of resection. Fluorescence-guided resection may be sufficient for enhancing tumors, but nonenhancing tumors are better resected with navigable 3D-US.

Notes

The results of this analysis were presented in part at the annual meeting of the Dandy Society held in Milan, Italy in June 2013.


Funding Source

None.


 
  • References

  • 1 Sæther CA, Torsteinsen M, Torp SH, Sundstrøm S, Unsgård G, Solheim O. Did survival improve after the implementation of intraoperative neuronavigation and 3D ultrasound in glioblastoma surgery? A retrospective analysis of 192 primary operations. J Neurol Surg A Cent Eur Neurosurg 2012; 73 (2) 73-78
  • 2 Solheim O, Selbekk T, Jakola AS, Unsgård G. Ultrasound-guided operations in unselected high-grade gliomas—overall results, impact of image quality and patient selection. Acta Neurochir (Wien) 2010; 152 (11) 1873-1886
  • 3 Senft CBA, Bink A, Franz K, Vatter H, Gasser T, Seifert V. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 2011; 12 (11) 997-1003
  • 4 Kubben PL, ter Meulen KJ, Schijns OE, ter Laak-Poort MP, van Overbeeke JJ, van Santbrink H. Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review. Lancet Oncol 2011; 12 (11) 1062-1070
  • 5 Unsgaard G, Rygh OM, Selbekk T , et al. Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 2006; 148 (3) 235-253 ; discussion 253
  • 6 Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ ; ALA-Glioma Study Group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006; 7 (5) 392-401
  • 7 Rygh OM, Selbekk T, Torp SH, Lydersen S, Hernes TA, Unsgaard G. Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection. Acta Neurochir (Wien) 2008; 150 (10) 1033-1041 ; discussion 1042
  • 8 Tsugu A, Ishizaka H, Mizokami Y , et al. Impact of the combination of 5-aminolevulinic acid-induced fluorescence with intraoperative magnetic resonance imaging-guided surgery for glioma. World Neurosurg 2011; 76 (1–2) 120-127
  • 9 Eyüpoglu IY, Hore N, Savaskan NE , et al. Improving the extent of malignant glioma resection by dual intraoperative visualization approach. PLoS ONE 2012; 7 (9) e44885
  • 10 Díez Valle R, Tejada Solis S, Idoate Gastearena MA, García de Eulate R, Domínguez Echávarri P, Aristu Mendiroz J. Surgery guided by 5-aminolevulinic fluorescence in glioblastoma: volumetric analysis of extent of resection in single-center experience. J Neurooncol 2011; 102 (1) 105-113
  • 11 Della Puppa A, De Pellegrin S, d'Avella E , et al. 5-aminolevulinic acid (5-ALA) fluorescence guided surgery of high-grade gliomas in eloquent areas assisted by functional mapping. Our experience and review of the literature. Acta Neurochir (Wien) 2013; 155 (6) 965-972 ; discussion 972
  • 12 Vogelbaum MA, Jost S, Aghi MK , et al. Application of novel response/progression measures for surgically delivered therapies for gliomas: Response Assessment in Neuro-Oncology (RANO) Working Group. Neurosurgery 2012; 70 (1) 234-243 ; discussion 243–244
  • 13 Aldave G, Tejada S, Pay E , et al. Prognostic value of residual fluorescent tissue in glioblastoma patients after gross total resection in 5-aminolevulinic acid-guided surgery. Neurosurgery 2013; 72 (6) 915-920 ; discussion 920–921
  • 14 Roberts DW, Valdés PA, Harris BT , et al. Coregistered fluorescence-enhanced tumor resection of malignant glioma: relationships between δ-aminolevulinic acid-induced protoporphyrin IX fluorescence, magnetic resonance imaging enhancement, and neuropathological parameters. Clinical article. J Neurosurg 2011; 114 (3) 595-603
  • 15 Unsgaard G, Selbekk T, Brostrup Müller T , et al. Ability of navigated 3D ultrasound to delineate gliomas and metastases—comparison of image interpretations with histopathology. Acta Neurochir (Wien) 2005; 147 (12) 1259-1269 ; discussion 1269
  • 16 Selbekk T, Jakola AS, Solheim O , et al. Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochir (Wien) 2013; 155 (6) 973-980
  • 17 Moiyadi AV, Shetty PM, Mahajan A, Udare A, Sridhar E. Usefulness of three-dimensional navigable intraoperative ultrasound in resection of brain tumors with a special emphasis on malignant gliomas. Acta Neurochir (Wien) 2013; 155 (12) 2217-2225
  • 18 Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 2011; 115 (1) 3-8
  • 19 Pichlmeier U, Bink A, Schackert G, Stummer W ; ALA Glioma Study Group. Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients. Neuro-oncol 2008; 10 (6) 1025-1034
  • 20 Panciani PP, Fontanella M, Schatlo B , et al. Fluorescence and image guided resection in high grade glioma. Clin Neurol Neurosurg 2012; 114 (1) 37-41
  • 21 Sanai N, Snyder LA, Honea NJ , et al. Intraoperative confocal microscopy in the visualization of 5-aminolevulinic acid fluorescence in low-grade gliomas. J Neurosurg 2011; 115 (4) 740-748
  • 22 Widhalm G, Kiesel B, Woehrer A , et al. 5-Aminolevulinic acid induced fluorescence is a powerful intraoperative marker for precise histopathological grading of gliomas with non-significant contrast-enhancement. PLoS ONE 2013; 8 (10) e76988