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Ultrasound-guided operations in unselected high-grade gliomas—overall results, impact of image quality and patient selection

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Abstract

Background

A number of tools, including intraoperative ultrasound, are reported to facilitate surgical resection of high-grade gliomas. However, results from selected surgical series do not necessarily reflect the effectiveness in common neurosurgical practice. Delineation of seemingly similar brain tumours vary in different ultrasound-guided operations, perhaps limiting usefulness in certain patients.

Methods

We explore and describe the results associated with use of the SonoWand system with intraoperative ultrasound in a population-based, unselected, high-grade glioma series. Surgeons filled out questionnaires about presumed extent of resection, use of ultrasound and ultrasound image quality just after surgery. We evaluate the impact of ultrasound image quality. We also explore the importance of patient selection for surgical results.

Results

Of 156 consecutive malignant glioma operations, 142 (91%) were resections whilst 14 (9%) were only biopsies. We achieved gross total resection (GTR) in 37% of all high-grade glioma resections, whilst worsening of functional status was seen in 13%. The risk of getting worse was significantly higher in reoperations, resections in eloquent locations, resections in cases with poor ultrasound image quality, resection when surgeons’ resection grade estimates were inaccurate and in cases with surgery-related complications. Aiming for GTR, unifocality of lesion, non-eloquent location and medium or good ultrasound image quality were identified as independent factors associated with achieving GTR.

Conclusion

We report good overall results, both in terms of resection grades and functional outcome in consecutive malignant glioma resections, in which intraoperative ultrasound was used in 95%. We observed a seeming dose–response relationship between ultrasound image quality and clinical and radiological results. This may suggest that better ultrasound facilitates better surgery. The study also clearly demonstrates that, in terms of surgical results, the selection of patients seems to be much more important than the selection of surgical tools.

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References

  1. Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34:45–60, discussion 60–41

    Article  CAS  PubMed  Google Scholar 

  2. Barker FG 2nd, Prados MD, Chang SM, Gutin PH, Lamborn KR, Larson DA, Malec MK, McDermott MW, Sneed PK, Wara WM, Wilson CB (1996) Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 84:442–448

    Article  PubMed  Google Scholar 

  3. Berger MS, Hadjipanayis CG (2007) Surgery of intrinsic cerebral tumors. Neurosurgery 61:279–304, discussion 304–275

    Article  PubMed  Google Scholar 

  4. Butowski N, Lamborn KR, Berger MS, Prados MD, Chang SM (2007) Historical controls for phase II surgically based trials requiring gross total resection of glioblastoma multiforme. J Neurooncol 85:87–94

    Article  PubMed  Google Scholar 

  5. Chang SM, Parney IF, McDermott M, Barker FG 2nd, Schmidt MH, Huang W, Laws ER Jr, Lillehei KO, Bernstein M, Brem H, Sloan AE, Berger M (2003) Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. J Neurosurg 98:1175–1181

    Article  PubMed  Google Scholar 

  6. Dowling C, Bollen AW, Noworolski SM, McDermott MW, Barbaro NM, Day MR, Henry RG, Chang SM, Dillon WP, Nelson SJ, Vigneron DB (2001) Preoperative proton MR spectroscopic imaging of brain tumors: correlation with histopathologic analysis of resection specimens. AJNR Am J Neuroradiol 22:604–612

    CAS  PubMed  Google Scholar 

  7. 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

    Article  PubMed  Google Scholar 

  8. Gerganov VM, Samii A, Akbarian A, Stieglitz L, Samii M, Fahlbusch R (2009) Reliability of intraoperative high-resolution 2D ultrasound as an alternative to high-field strength MR imaging for tumor resection control: a prospective comparative study. J Neurosurg 111:512–519

    Article  PubMed  Google Scholar 

  9. Gronningsaeter A, Kleven A, Ommedal S, Aarseth TE, Lie T, Lindseth F, Lango T, Unsgard G (2000) SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 47:1373–1379, discussion 1379–1380

    Article  CAS  PubMed  Google Scholar 

  10. Gulati S, Berntsen EM, Solheim O, Kvistad KA, Haberg A, Selbekk T, Torp SH, Unsgaard G (2009) Surgical resection of high-grade gliomas in eloquent regions guided by blood oxygenation level dependent functional magnetic resonance imaging, diffusion tensor tractography, and intraoperative navigated 3D ultrasound. Minim Invasive Neurosurg 52:17–24

    Article  CAS  PubMed  Google Scholar 

  11. Gupta DK, Chandra PS, Ojha BK, Sharma BS, Mahapatra AK, Mehta VS (2007) Awake craniotomy versus surgery under general anesthesia for resection of intrinsic lesions of eloquent cortex—a prospective randomised study. Clin Neurol Neurosurg 109:335–343

    Article  PubMed  Google Scholar 

  12. Hammoud MA, Ligon BL, ElSouki R, Shi WM, Schomer DF, Sawaya R (1996) Use of intraoperative ultrasound for localizing tumors and determining the extent of resection: a comparative study with magnetic resonance imaging. J Neurosurg 84:737–741

    Article  CAS  PubMed  Google Scholar 

  13. Hartov A, Roberts DW, Paulsen KD (2008) A comparative analysis of coregistered ultrasound and magnetic resonance imaging in neurosurgery. Neurosurgery 62:91–99, discussion 99–101

    Article  PubMed  Google Scholar 

  14. Hatiboglu MA, Weinberg JS, Suki D, Rao G, Prabhu SS, Shah K, Jackson E, Sawaya R (2009) Impact of intraoperative high-field magnetic resonance imaging guidance on glioma surgery: a prospective volumetric analysis. Neurosurgery 64:1073–1081, discussion 1081

    Article  PubMed  Google Scholar 

  15. Henegar MM, Moran CJ, Silbergeld DL (1996) Early postoperative magnetic resonance imaging following nonneoplastic cortical resection. J Neurosurg 84:174–179

    Article  CAS  PubMed  Google Scholar 

  16. Kamada K, Todo T, Ota T, Ino K, Masutani Y, Aoki S, Takeuchi F, Kawai K, Saito N (2009) The motor-evoked potential threshold evaluated by tractography and electrical stimulation. J Neurosurg 111:785–795

    Article  PubMed  Google Scholar 

  17. Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ (1987) Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg 66:865–874

    Article  CAS  PubMed  Google Scholar 

  18. Kim SS, McCutcheon IE, Suki D, Weinberg JS, Sawaya R, Lang FF, Ferson D, Heimberger AB, DeMonte F, Prabhu SS (2009) Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 64:836–845, discussion 345–836

    Article  PubMed  Google Scholar 

  19. Knauth M, Aras N, Wirtz CR, Dorfler A, Engelhorn T, Sartor K (1999) Surgically induced intracranial contrast enhancement: potential source of diagnostic error in intraoperative MR imaging. AJNR Am J Neuroradiol 20:1547–1553

    CAS  PubMed  Google Scholar 

  20. Kowalczuk A, Macdonald RL, Amidei C, Dohrmann G 3rd, Erickson RK, Hekmatpanah J, Krauss S, Krishnasamy S, Masters G, Mullan SF, Mundt AJ, Sweeney P, Vokes EE, Weir BK, Wollman RL (1997) Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery 41:1028–1036, discussion 1036–1028

    Article  CAS  PubMed  Google Scholar 

  21. Kurimoto M, Hayashi N, Kamiyama H, Nagai S, Shibata T, Asahi T, Matsumura N, Hirashima Y, Endo S (2004) Impact of neuronavigation and image-guided extensive resection for adult patients with supratentorial malignant astrocytomas: a single-institution retrospective study. Minim Invasive Neurosurg 47:278–283

    Article  CAS  PubMed  Google Scholar 

  22. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198

    Article  CAS  PubMed  Google Scholar 

  23. Laws ER, Parney IF, Huang W, Anderson F, Morris AM, Asher A, Lillehei KO, Bernstein M, Brem H, Sloan A, Berger MS, Chang S (2003) Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg 99:467–473

    Article  PubMed  Google Scholar 

  24. LeRoux PD, Winter TC, Berger MS, Mack LA, Wang K, Elliott JP (1994) A comparison between preoperative magnetic resonance and intraoperative ultrasound tumor volumes and margins. J Clin Ultrasound 22:29–36

    Article  CAS  PubMed  Google Scholar 

  25. Litofsky NS, Bauer AM, Kasper RS, Sullivan CM, Dabbous OH (2006) Image-guided resection of high-grade glioma: patient selection factors and outcome. Neurosurg Focus 20:E16

    Article  PubMed  Google Scholar 

  26. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109

    Article  PubMed  Google Scholar 

  27. Matsukado Y, Maccarty CS, Kernohan JW (1961) The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J Neurosurg 18:636–644

    Article  CAS  PubMed  Google Scholar 

  28. McGirt MJ, Chaichana KL, Gathinji M, Attenello FJ, Than K, Olivi A, Weingart JD, Brem H, Quinones-Hinojosa AR (2009) Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg 110:156–162

    Article  PubMed  Google Scholar 

  29. McGirt MJ, Mukherjee D, Chaichana KL, Than KD, Weingart JD, Quinones-Hinojosa A (2009) Association of surgically acquired motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery 65:463–469, discussion 469–470

    Article  PubMed  Google Scholar 

  30. Miller D, Heinze S, Tirakotai W, Bozinov O, Surucu O, Benes L, Bertalanffy H, Sure U (2007) Is the image guidance of ultrasonography beneficial for neurosurgical routine? Surg Neurol 67:579–587, discussion 587–578

    Article  PubMed  Google Scholar 

  31. Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R (2006) Intraoperative visualization for resection of gliomas: the role of functional neuronavigation and intraoperative 1.5 T MRI. Neurol Res 28:482–487

    Article  PubMed  Google Scholar 

  32. Nimsky C, Ganslandt O, Fahlbusch R (2005) Comparing 0.2 Tesla with 1.5 Tesla intraoperative magnetic resonance imaging analysis of setup, workflow, and efficiency. Acad Radiol 12:1065–1079

    Article  PubMed  Google Scholar 

  33. Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56:130–137, discussion 138

    PubMed  Google Scholar 

  34. Nimsky C, Ganslandt O, Tomandl B, Buchfelder M, Fahlbusch R (2002) Low-field magnetic resonance imaging for intraoperative use in neurosurgery: a 5-year experience. Eur Radiol 12:2690–2703

    PubMed  Google Scholar 

  35. Oser AB, Moran CJ, Kaufman BA, Park TS (1997) Intracranial tumor in children: MR imaging findings within 24 hours of craniotomy. Radiology 205:807–812

    CAS  PubMed  Google Scholar 

  36. Pronin IN, McManus KA, Holodny AI, Peck KK, Kornienko VN (2009) Quantification of dispersion of Gd-DTPA from the initial area of enhancement into the peritumoral zone of edema in brain tumors. J Neurooncol 94:399–408

    Article  PubMed  Google Scholar 

  37. Rasmussen IA Jr, Lindseth F, Rygh OM, Berntsen EM, Selbekk T, Xu J, Nagelhus Hernes TA, Harg E, Haberg A, Unsgaard G (2007) Functional neuronavigation combined with intra-operative 3D ultrasound: initial experiences during surgical resections close to eloquent brain areas and future directions in automatic brain shift compensation of preoperative data. Acta Neurochir (Wien) 149:365–378

    Article  Google Scholar 

  38. Roth J, Biyani N, Beni-Adani L, Constantini S (2007) Real-time neuronavigation with high-quality 3D ultrasound SonoWand in pediatric neurosurgery. Pediatr Neurosurg 43:185–191

    Article  PubMed  Google Scholar 

  39. Rygh OM, Nagelhus Hernes TA, Lindseth F, Selbekk T, Brostrup Muller T, Unsgaard G (2006) Intraoperative navigated 3-dimensional ultrasound angiography in tumor surgery. Surg Neurol 66:581–592, discussion 592

    Article  PubMed  Google Scholar 

  40. Rygh OM, Selbekk T, Torp SH, Lydersen S, Hernes TA, Unsgaard G (2008) Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection. Acta Neurochir (Wien) 150:1033–1041, discussion 1042

    Article  Google Scholar 

  41. Scherer H (1940) The forms of growth in gliomas and their practical significance. Brain 63:1–35

    Article  Google Scholar 

  42. Senft C, Seifert V, Hermann E, Franz K, Gasser T (2008) Usefulness of intraoperative ultra low-field magnetic resonance imaging in glioma surgery. Neurosurgery 63:257–266, discussion 266–257

    Article  PubMed  Google Scholar 

  43. Shinoura N, Takahashi M, Yamada R (2006) Delineation of brain tumor margins using intraoperative sononavigation: implications for tumor resection. J Clin Ultrasound 34:177–183

    Article  PubMed  Google Scholar 

  44. Simpson JR, Horton J, Scott C, Curran WJ, Rubin P, Fischbach J, Isaacson S, Rotman M, Asbell SO, Nelson JS et al (1993) Influence of location and extent of surgical resection on survival of patients with glioblastoma multiforme: results of three consecutive Radiation Therapy Oncology Group (RTOG) clinical trials. Int J Radiat Oncol Biol Phys 26:239–244

    CAS  PubMed  Google Scholar 

  45. Solheim O, Selbekk T, Lindseth F, Unsgard G (2009) Navigated resection of giant intracranial meningiomas based on intraoperative 3D ultrasound. Acta Neurochir (Wien) 151:1143–1151

    Article  Google Scholar 

  46. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401

    Article  CAS  PubMed  Google Scholar 

  47. Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C, Franz K, Pietsch T (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62:564–576, discussion 564–576

    Article  PubMed  Google Scholar 

  48. Stummer W, Tonn JC, Mehdorn HM, Nestler U, Franz K, Goetz C, Bink A, Pichlmeier U (2010) Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. J Neurosurg (in press)

  49. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant Temozolomide for glioblastoma. N Engl J Med 352:987–996

    Article  CAS  PubMed  Google Scholar 

  50. Tovi M, Hartman M, Lilja A, Ericsson A (1994) MR imaging in cerebral gliomas. Tissue component analysis in correlation with histopathology of whole-brain specimens. Acta Radiol 35:495–505

    CAS  PubMed  Google Scholar 

  51. Tronnier VM, Bonsanto MM, Staubert A, Knauth M, Kunze S, Wirtz CR (2001) Comparison of intraoperative MR imaging and 3D-navigated ultrasonography in the detection and resection control of lesions. Neurosurg Focus 10:E3

    Article  CAS  PubMed  Google Scholar 

  52. Unsgaard G, Ommedal S, Muller T, Gronningsaeter A, Nagelhus Hernes TA (2002) Neuronavigation by intraoperative three-dimensional ultrasound: initial experience during brain tumor resection. Neurosurgery 50:804–812, discussion 812

    Article  PubMed  Google Scholar 

  53. Unsgaard G, Selbekk T, Brostrup Muller T, Ommedal S, Torp SH, Myhr G, Bang J, Nagelhus Hernes TA (2005) Ability of navigated 3D ultrasound to delineate gliomas and metastases—comparison of image interpretations with histopathology. Acta Neurochir (Wien) 147:1259–1269, discussion 1269

    Article  CAS  Google Scholar 

  54. van Genugten JA, Leffers P, Baumert BG, Tjon AFH, Twijnstra A (2010) Effectiveness of Temozolomide for primary glioblastoma multiforme in routine clinical practice. J Neurooncol 96:249–257

    Article  CAS  PubMed  Google Scholar 

  55. Vecht CJ, Avezaat CJ, van Putten WL, Eijkenboom WM, Stefanko SZ (1990) The influence of the extent of surgery on the neurological function and survival in malignant glioma. A retrospective analysis in 243 patients. J Neurol Neurosurg Psychiatry 53:466–471

    Article  CAS  PubMed  Google Scholar 

  56. Vuorinen V, Hinkka S, Farkkila M, Jaaskelainen J (2003) Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir (Wien) 145:5–10

    Article  CAS  Google Scholar 

  57. Willems PW, Taphoorn MJ, Burger H, Berkelbach van der Sprenkel JW, Tulleken CA (2006) Effectiveness of neuronavigation in resecting solitary intracerebral contrast-enhancing tumors: a randomized controlled trial. J Neurosurg 104:360–368

    Article  PubMed  Google Scholar 

  58. Wirtz CR, Albert FK, Schwaderer M, Heuer C, Staubert A, Tronnier VM, Knauth M, Kunze S (2000) The benefit of neuronavigation for neurosurgery analyzed by its impact on glioblastoma surgery. Neurol Res 22:354–360

    CAS  PubMed  Google Scholar 

  59. Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, Tronnier VM (2000) Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery 46:1112–1120, discussion 1120–1112

    Article  CAS  PubMed  Google Scholar 

  60. Yoshimoto Y (2003) Publication bias in neurosurgery: lessons from series of unruptured aneurysms. Acta Neurochir (Wien) 145:45–48

    Article  CAS  Google Scholar 

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Acknowledgements

The neuroradiologists Kjell A. Kvistad, Mari Folvik and Jana Rydland helped with size measurement of lesions, and Eirik Magnus Berntsen did manual segmentation of some lesions. The project was supported by the Norwegian Ministry of Health and Social Affairs through the National Centre for 3D Ultrasound in Surgery, the Norwegian University of Science and Technology (NTNU) and Helse Midt-Norge (the regional health authorities of Central Norway).

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Correspondence to Ole Solheim.

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Solheim, O., Selbekk, T., Jakola, A.S. et al. Ultrasound-guided operations in unselected high-grade gliomas—overall results, impact of image quality and patient selection. Acta Neurochir 152, 1873–1886 (2010). https://doi.org/10.1007/s00701-010-0731-5

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