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Sensitivity and specificity of linear array intraoperative ultrasound in glioblastoma surgery: a comparative study with high field intraoperative MRI and conventional sector array ultrasound

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Abstract

Introduction

Linear array intraoperative ultrasound (lioUS) is an emerging technology for intracranial use. We evaluated sensitivity and specificity of lioUS to detect residual tumor in patients harboring a glioblastoma.

Methods

After near total resection in 20 patients, residual tumor detection using lioUS, conventional intraoperative ultrasound (cioUS), and gadopentetic-diethylenetriamine penta-acetic acid (Gd-DTPA)-enhanced intraoperative MRI (iMRI) were compared. Sensitivity and specificity were calculated based on 68 navigated biopsies. Receiver operator characteristic (ROC) curves and correlation with histopathological findings of each imaging modality were calculated. Additionally, results were evaluated in the subgroup of recurrent disease (23 biopsies in 8 patients).

Results

Sensitivity of lioUS (76 %) was significantly higher compared with iMRI (55 %) and cioUS (24 %). Specificity of lioUS (58 %) was significantly lower than in cioUS (96 %), while there was no significant difference to iMRI (74 %). All imaging modalities correlated significantly with histopathological findings. In the subgroup of recurrent disease, sensitivity and specificity decreased in all modalities. However, cioUS showed significant lower values than iMRI and lioUS. In ROC curves, lioUS showed a higher area und the curve (AUC) in comparison with iMRI and cioUS. We found similar results in the subgroup of recurrent disease.

Conclusion

Tumor detection using a lioUS is significantly superior to cioUS. Overall test performance in lioUS is comparable with results of iMRI. While, the latter has a higher specificity and a significantly lower sensitivity in comparison with lioUS.

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References

  1. Bozinov O, Burkhardt JK (2012) Intra-operative computed-tomography-like real-time three-dimensional ultrasound in neurosurgery. World Neurosurg 78(1–2):5–7. doi:10.1016/j.wneu.2012.05.025

    Article  PubMed  Google Scholar 

  2. Bozinov O, Burkhardt JK, Woernle CM, Hagel V, Ulrich NH, Krayenbuhl N, Bertalanffy H (2012) Intra-operative high frequency ultrasound improves surgery of intramedullary cavernous malformations. Neurosurg Rev 35((2):269–275. doi:10.1007/s10143-011-0364-z, discussion 275

    Article  PubMed  Google Scholar 

  3. Chandler WF, Knake JE, McGillicuddy JE, Lillehei KO, Silver TM (1982) Intraoperative use of real-time ultrasonography in neurosurgery. J Neurosurg 57(2):157–163. doi:10.3171/jns.1982.57.2.0157

    Article  CAS  PubMed  Google Scholar 

  4. Coburger J, Engelke J, Scheuerle A, Thal DR, Hlavac M, Wirtz CR, Konig R (2014) 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 36(2):E3. doi:10.3171/2013.11.FOCUS13463

    Article  PubMed  Google Scholar 

  5. Coburger J, König RW, Scheuerle A, Engelke J, Hlavac M, Thal DR, Wirtz CR (2014) Navigated high frequency ultrasound: description of technique and first clinical comparison with conventional intracranial ultrasound. World Neurosurg

  6. Doyle TE, Factor RE, Ellefson CL, Sorensen KM, Ambrose BJ, Goodrich JB, Hart VP, Jensen SC, Patel H, Neumayer LA (2011) High-frequency ultrasound for intraoperative margin assessments in breast conservation surgery: a feasibility study. BMC Cancer 11:444. doi:10.1186/1471-2407-11-444

    Article  PubMed Central  PubMed  Google Scholar 

  7. 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(3):512–519

    Article  PubMed  Google Scholar 

  8. 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(6):1373–1379, discussion 1379–1380

    Article  CAS  PubMed  Google Scholar 

  9. Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143(1):29–36. doi:10.1148/radiology.143.1.7063747

    Article  CAS  PubMed  Google Scholar 

  10. Koenig RW, Schmidt TE, Heinen CP, Wirtz CR, Kretschmer T, Antoniadis G, Pedro MT (2011) Intraoperative high-resolution ultrasound: a new technique in the management of peripheral nerve disorders. J Neurosurg 114(2):514–521

    Article  PubMed  Google Scholar 

  11. Krekel NM, Zonderhuis BM, Schreurs HW, Cardozo AM, Rijna H, van der Veen H, Muller S, Poortman P, de Widt L, de Roos WK, Bosch AM, van Taets AAH, Bergers E, van der Linden MH, de DeLange Klerk ES, Winters HA, Meijer S, van den Tol PM (2011) Ultrasound-guided breast-sparing surgery to improve cosmetic outcomes and quality of life. A prospective multicentre randomised controlled clinical trial comparing ultrasound-guided surgery to traditional palpation-guided surgery (COBALT trial). BMC Surg 11:8. doi:10.1186/1471-2482-11-8

    Article  PubMed Central  PubMed  Google Scholar 

  12. Kubben PL, Wesseling P, Lammens M, Schijns OE, Ter Laak-Poort MP, van Overbeeke JJ, van Santbrink H (2012) Correlation between contrast enhancement on intraoperative magnetic resonance imaging and histopathology in glioblastoma. Surg Neurol Int 3:158

    Article  PubMed Central  PubMed  Google Scholar 

  13. 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(2):190–198. doi:10.3171/jns.2001.95.2.0190

    Article  CAS  PubMed  Google Scholar 

  14. 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(2):97–109

    Article  PubMed Central  PubMed  Google Scholar 

  15. Marko NF, Weil RJ, Schroeder JL, Lang FF, Suki D, Sawaya RE et al (2014) Extent of resection of glioblastoma revisited: personalized survival modeling facilitates more accurate survival prediction and supports a maximum-safe-resection approach to surgery. J Clin Oncol: Off J Am Soc Clin Oncol 32(8):774–782. doi:10.1200/jco.2013.51.8886

    Article  Google Scholar 

  16. Marko NF, Weil RJ, Schroeder JL, Lang FF, Suki D, Sawaya RE (2014) Extent of resection of glioblastoma revisited: personalized survival modeling facilitates more accurate survival prediction and supports a maximum-safe-resection approach to surgery. J Clin Oncol. doi:10.1200/jco.2013.51.8886

    PubMed  Google Scholar 

  17. Moiyadi A, Shetty P, Mahajan A, Udare A, Sridhar E (2013) Usefulness of three-dimensional navigable intraoperative ultrasound in resection of brain tumors with a special emphasis on malignant gliomas. Acta Neurochir 155(12):2217–2225. doi:10.1007/s00701-013-1881-z

    Article  PubMed  Google Scholar 

  18. Moran CM, Pye SD, Ellis W, Janeczko A, Morris KD, McNeilly AS, Fraser HM (2011) A comparison of the imaging performance of high resolution ultrasound scanners for preclinical imaging. Ultrasound Med Biol 37(3):493–501. doi:10.1016/j.ultrasmedbio.2010.11.010

    Article  PubMed Central  PubMed  Google Scholar 

  19. 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 149(4):365–378

    Article  PubMed  Google Scholar 

  20. Renovanz M, Hickmann AK, Henkel C, Nadji-Ohl M, Hopf NJ (2014) Navigated versus non-navigated intraoperative ultrasound: is there any impact on the extent of resection of high-grade gliomas? A retrospective clinical analysis. J Neurol Surg A Cent Eur Neurosurg. doi:10.1055/s-0033-1356486

    PubMed  Google Scholar 

  21. 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 150(10):1033–1041, discussion 1042

    Article  PubMed  Google Scholar 

  22. Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115(1):3–8. doi:10.3171/2011.2.jns10998

    Article  PubMed  Google Scholar 

  23. Selbekk T, Jakola AS, Solheim O, Johansen TF, Lindseth F, Reinertsen I, Unsgard G (2013) Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochirurgica

  24. Serra C, Stauffer A, Actor B, Burkhardt JK, Ulrich NH, Bernays RL, Bozinov O (2012) Intraoperative high frequency ultrasound in intracerebral high-grade tumors. Ultraschall Med 33(7):E306–E312. doi:10.1055/s-0032-1325369, Stuttgart, Germany : 1980

    Article  CAS  PubMed  Google Scholar 

  25. Solheim O, Selbekk T, Jakola A, Unsgård G (2010) Ultrasound-guided operations in unselected high-grade gliomas—overall results, impact of image quality and patient selection. Acta Neurochir 152(11):1873–1886. doi:10.1007/s00701-010-0731-5

    Article  PubMed  Google Scholar 

  26. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen H-J (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7(5):392–401. doi:10.1016/s1470-2045(06)70665-9

    Article  CAS  PubMed  Google Scholar 

  27. Tirakotai W, Miller D, Heinze S, Benes L, Bertalanffy H, Sure U (2006) A novel platform for image-guided ultrasound. Neurosurgery 58(4):710–718, discussion 710–718. d

    Article  PubMed  Google Scholar 

  28. Ulrich NH, Burkhardt JK, Serra C, Bernays RL, Bozinov O (2012) Resection of pediatric intracerebral tumors with the aid of intraoperative real-time 3-D ultrasound. Childs Nerv Syst 28(1):101–109. doi:10.1007/s00381-011-1571-1

    Article  PubMed  Google Scholar 

  29. Unsgard G, Solheim O, Lindseth F, Selbekk T (2011) Intra-operative imaging with 3D ultrasound in neurosurgery. Acta Neurochir Suppl 109:181–186

    PubMed  Google Scholar 

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Conflict of interest

The Department of Neurosurgery was provided with a software plug-in and the hardware to integrate ioUS in the neuronavigation software for scientific use by Brainlab AG (Feldkirchen, Germany). RK has worked as a medical consultant for Brainlab AG (Feldkirchen, Germany). DRT received consultancies from Simon-Kucher and Partners (Germany), Covance Laboratories (UK), and GE-Healthcare (UK), received a speaker honorarium from GE-Healthcare (UK) and collaborated with Novartis Pharma Basel (Switzerland).

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Authors and Affiliations

  1. Department of Neurosurgery, University of Ulm, Ludwig Heilmeyerstr. 2, 89312, Günzburg, Germany

    Jan Coburger, Thomas Kapapa, Jens Engelke, Christian R. Wirtz & Ralph König

  2. Institute of Pathology, Laboratory of Neuropathology, Center for biomedical Research, University of Ulm, Ludwig Heilmeyerstr. 2, 89312, Günzburg, Germany

    Angelika Scheuerle & Dietmar Rudolf Thal

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  1. Jan Coburger
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  2. Angelika Scheuerle
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  4. Jens Engelke
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  6. Christian R. Wirtz
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  7. Ralph König
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Correspondence to Jan Coburger.

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Comments

Marian Neidert, Oliver Bozinov, Zurich, Switzerland

Coburger and colleagues present a prospective non-randomized single-center study (class IV) on the usefulness of intraoperative linear array ultrasound (lioUS) in glioblastoma surgery. In this study, lioUS was compared (first time) to high field ioMRI and to conventional ioUS. The authors conclude that lioUS is superior to cioUS in glioblastoma surgery and comparable with ioMRI (lioUS has a better sensitivity, but worse specificity).

Intraoperative ultrasound (ioUS) is often considered an “old” technology introduced in the 1960s that was not used frequently in neurosurgical practice over a long period of time due to suboptimal image quality. However, in recent years, ioUS had a comeback mainly because of technical improvements (reduced probe size allowing intracavital scanning, improved resolution with high-frequency probes, the option of 3D imaging and the option of linking ioUS to neuronavigation). Most importantly, ioUS offers true repetetive real time information, which is not the case with pure neuronavigation or in a delayed way with ioMRI or ioCT.

Regarding glioblastoma surgery, good evidence supports not only the idea of the extent of resection and the volume of residual disease but also new focal-neurological deficits following resection have a strong impact on patient outcome. As ioUS helps to differentiate between tumor and healthy brain tissue, ioUS can help in the balancing act of achieving a maximum resection while providing safety. Hence, the data provided in this manuscript are valuable to the neurosurgical community.

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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 38, 499–509 (2015). https://doi.org/10.1007/s10143-015-0627-1

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  • DOI: https://doi.org/10.1007/s10143-015-0627-1

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