Acta Neurochirurgica

, Volume 158, Issue 6, pp 1179–1185 | Cite as

The use of ultrasound in intracranial tumor surgery

Review Article - Brain Tumors
First Online:
Received:
Accepted:

Abstract

Background

As an intraoperative imaging modality, ultrasound is a user-friendly and cost-effective real-time imaging technique. Despite this, it is still not routinely employed for brain tumor surgery. This may be due to the poor image quality in inexperienced hands, and the well-documented learning curve. However, with regular use, the operator issues are addressed, and intraoperative ultrasound can provide valuable real-time information. The aim of this review is to provide an understanding for neurosurgeons of the development and use of ultrasound in intracranial tumor surgery, and possible future advances.

Methods

A systematic search of the electronic databases Embase, Medline OvidSP, PubMed, Cochrane, and Google Scholar regarding the use of ultrasound in intracranial tumor surgery was undertaken.

Results and discussion

Intraoperative ultrasound has been shown to be able to accurately account for brain shift and has potential for regular use in brain tumor surgery. Further developments in probe size, resolution, and image reconstruction techniques will ensure that intraoperative ultrasound is more accessible and attractive to the neuro-oncological surgeon.

Conclusions

This review has summarized the development of ultrasound and its uses with particular reference to brain tumor surgery, detailing the ongoing challenges in this area.

Keywords

Intra-operative imaging Ultrasound Glioma surgery Systematic review Neuronavigation 
This is a preview of subscription content, log in to check access.

Notes

Compliance with ethical standards

Funding

No funding was received for this research.

Conflict of interest

The author(s) declare that they have no competing interests.

Human and animal consent

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Newman PG, Rozycki GS (1998) The history of ultrasound. Surg Clin North Am 78:179–195CrossRefPubMedGoogle Scholar
  2. 2.
    Leksell L (1956) Echo-encephalography I. Detection of intracranial complications following head injury. Acta Chir Scand 110:301–315PubMedGoogle Scholar
  3. 3.
    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 95:190–198CrossRefPubMedGoogle Scholar
  4. 4.
    Simpson JR, Horton J, Scott C, Curran WJ, Rubin P, Fischbach J, Isaacson S, Rotman M, Asbell SO, Nelson JS (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 26:239–244CrossRefPubMedGoogle Scholar
  5. 5.
    Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C, Franz K, Pietsch T, ALA-Glioma Study Group (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62(3):564–576, discussion 564-76CrossRefPubMedGoogle Scholar
  6. 6.
    Dorward NL, Alberti O, Velani B, Gerritsen FA, Harkness WF, Kitchen ND, Thomas DG (1998) Postimaging brain distortion: magnitude, correlates, and impact on neuronavigation. J Neurosurg 88:656–662CrossRefPubMedGoogle Scholar
  7. 7.
    Coburger J, Scheuerle A, Thal DR, Engelke J, Hlavac M, Wirtz CR, König R (2015) Linear array ultrasound in low-grade glioma surgery: histology-based assessment of accuracy in comparison to conventional intraoperative ultrasound and intraoperative MRI. Acta Neurochir 157:195–206CrossRefPubMedGoogle Scholar
  8. 8.
    Burkhardt JK, Serra C, Neidert MC, Woernle CM, Fierstra J, Regli L, Bozinov O (2014) High-frequency intra-operative ultrasound-guided surgery of superficial intra-cerebral lesions via a single-burr-hole approach. Ultrasound Med Biol 40:1469–1475CrossRefPubMedGoogle Scholar
  9. 9.
    Müns A, Meixensberger J, Arnold S, Schmitgen A, Arlt F, Chalopin C, Lindner D (2011) Integration of a 3D ultrasound probe into neuronavigation. Acta Neurochir (Wien) 153:1529–1533CrossRefGoogle Scholar
  10. 10.
    Mair R, Heald J, Poeata I, Ivanov M (2013) A practical grading system of ultrasonographic visibility for intracerebral lesions. Acta Neurochir 155:2293–2298CrossRefPubMedGoogle Scholar
  11. 11.
    Hill DLG, Maurer CR, Maciunas RJ, Barwise JA, Fitzpatrick JM, Wang MY (1998) Measurement of intraoperative brain surface deformation under a craniotomy. Neurosurgery 43:514–528CrossRefPubMedGoogle Scholar
  12. 12.
    Roberts DW, Hartov A, Kennedy FE, Miga MI, Paulsen KD (1998) Intraoperative brain shift and deformation: a quantitative analysis of cortical displacement in 28 cases. Neurosurgery 43:749–760CrossRefPubMedGoogle Scholar
  13. 13.
    Ivanov M, Wilkins S, Poeata I, Brodbelt A (2010) Intraoperative ultrasound in neurosurgery—a practical guide. Br J Neurosurg 24:510–517CrossRefPubMedGoogle Scholar
  14. 14.
    Gronningsaeter A, Kleven A, Ommedal S, Aarseth TE, Lie T, Lindseth F, Langø T, Unsgård G (2000) SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 47:1373–1379, discussion 1379-80CrossRefPubMedGoogle Scholar
  15. 15.
    Roche A, Pennec X, Malandin G, Ayache N (2001) Rigid registration of 3D ultrasound with MR images: a new approach combining intensity and gradient information. IEEE Trans Med Imaging 20:1038–1049Google Scholar
  16. 16.
    Prada F, Del Bene M, Mattei L, Casali C, Filippini A, Legnani F, Mangraviti A, Saladino A, Perin A, Richetta C, Vetrano I, Moiraghi A, Saini M, DiMeco F (2014) Fusion imaging for intra-operative ultrasound-based navigation in neurosurgery. J Ultrasound 17:243–251CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Prada F, Del Bene M, Mattei L, Lodigiani L, DeBeni S, Kolev V, Vetrano I, Solbiati L, Sakas G, DiMeco F (2015) Preoperative magnetic resonance and intraoperative ultrasound fusion imaging for real-time neuronavigation in brain tumor surgery. Ultraschall Med 36:174–186PubMedGoogle Scholar
  18. 18.
    Berntsen EM, Gulati S, Solheim O, Kvistad KA, Torp SH, Selbekk T, Unsgård G, Håberg AK (2010) Functional magnetic resonance imaging and diffusion tensor tractography incorporated into an intraoperative 3-dimensional ultrasound-based neuronavigation system: impact on therapeutic strategies, extent of resection, and clinical outcome. Neurosurgery 67:251–264CrossRefPubMedGoogle Scholar
  19. 19.
    Rasmussen IA Jr, Lindseth F, Rygh OM, Berntsen EM, Selbekk T, Xu J, Nagelhus Hernes TA, Harg E, Håberg 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 149:365–378CrossRefPubMedGoogle Scholar
  20. 20.
    Elias WJ, Fu K-M, Frysinger RC (2007) Cortical and subcortical brain shift during stereotactic procedures. J Neurosurg 107:983–988CrossRefPubMedGoogle Scholar
  21. 21.
    Coupé P, Hellier P, Morandi X, Barillot C (2012) 3D rigid registration of intraoperative ultrasound and preoperative MR brain images based on hyperechogenic structures. Int J Biomed Imaging 2012:531–539CrossRefGoogle Scholar
  22. 22.
    Nigris D, Collins DL, Arbel T (2012) Fast and robust registration based on gradient orientations: case study matching intra- operative ultrasound to pre-operative MRI in neurosurgery. In: Abolmaesumi P, Joskowicz L, Navab N, Jannin P (eds) Information processing in computer-assisted interventions, vol 7330. Springer, Berlin, pp 125–134, Lecture Notes in Computer ScienceGoogle Scholar
  23. 23.
    Reinertsen I, Lindseth F, Askeland C, Iversen DH, Unsgård G (2014) Intra-operative correction of brain-shift. Acta Neurochir 156:1301–1310CrossRefPubMedGoogle Scholar
  24. 24.
    El Mouaaouv A, Gawlowski J, Schrot G, Arlt R (1986) Intraoperative ultrasound diagnosis in neurosurgery. Ultraschall Med 7:235–238CrossRefGoogle Scholar
  25. 25.
    Le Roux PD, Berger MS, Wang K, Mack LA, Ojemann GA (1992) Low-grade gliomas: comparison of intraoperative ultrasound characteristic with preoperative imaging studies. J Neurooncol 13:189–198CrossRefPubMedGoogle Scholar
  26. 26.
    Unsgaard G, Gronningsaeter A, Ommedal S, Nagelhus Hernes TA (2002) Brain operations guided by real-time two-dimensional ultrasound: new possibilities as a result of improved image quality. Neurosurgery 51:402–411PubMedGoogle Scholar
  27. 27.
    Unsgaard G, Ommedal S, Muller T, Gronningsaeter A, Nagelhus Hernes TA (2002) Neuronavigation by intraoperative three-dimensional ultrasound: initial experience during brain tumour resection. Neurosurgery 50:804–812CrossRefPubMedGoogle Scholar
  28. 28.
    Unsgaard G, Rygh OM, Selbekk T, Müller TB, Kolstad F, Lindseth F, Hernes TA (2006) Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir 148:235–253CrossRefPubMedGoogle Scholar
  29. 29.
    Sæther CA, Torsteinsen M, Torp SH, Sundstrøm S, Unsgård G, Solheim O (2012) 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 Cen Eur Neurosurg 73:73–78CrossRefGoogle Scholar
  30. 30.
    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 33:306–312CrossRefGoogle Scholar
  31. 31.
    Woydt M, Krone A, Becker G, Schmidt K, Roggendorf W, Roosen K (1996) Correlation of intra-operative ultrasound with histopathologic findings after tumour resection in supratentorial gliomas. A method to improve gross total resection. Acta Neurochir 57:129–135Google Scholar
  32. 32.
    Chacko AG, Kumar NK, Chacko G, Athyal R, Rajshekhar V (2003) Intraoperative ultrasound in determining the extent of resection of parenchymal brain tumours—a comparative study with computed tomography and histopathology. Act Neurochir 145:743–748CrossRefGoogle Scholar
  33. 33.
    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. Act Neurochir 150:1033–1041CrossRefGoogle Scholar
  34. 34.
    Shah AJ, Callaway M, Thomas MG, Finch-Jones MD (2010) Contrast-enhanced intraoperative ultrasound improves detection of liver metastases during surgery for primary colorectal cancer. HPB 12:181–187CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Malhi H, Grant EG, Duddalwar V (2014) Contrast-enhanced ultrasound of the liver and kidney. Radiol Clin N Am 52:1177–1190CrossRefPubMedGoogle Scholar
  36. 36.
    Prada F, Perin A, Martegani A, Aiani L, Solbiati L, Lamperti M, Casali C, Legnani F, Mattei L, Saladino A, Saini M, DiMeco F (2014) Intraoperative contrast-enhanced ultrasound for brain tumor surgery. Neurosurgery 74:542–552, discussion 552CrossRefPubMedGoogle Scholar
  37. 37.
    He W, Jiang X, Wang S, Zhang M, Zhao J, Lui H, Ma J, Xiang D, Wang L (2008) Intraoperative contrast-enhanced ultrasound for brain tumours. Clin Imaging 32:419–424CrossRefPubMedGoogle Scholar
  38. 38.
    Engelhardt M, Hansen C, Eyding J, Wilkening W, Brenke C, Krogias C, Scholz M, Harders A, Ermert H, Schmieder K (2007) Feasibility of contrast-enhanced sonography during resection of cerebral tumours: initial results of a prospective study. Ultrasound Med Biol 33:571–575CrossRefPubMedGoogle Scholar
  39. 39.
    Chan HW, Pressler R, Uff C, Gunny R, St Piers K, Cross H, Bamber J, Dorward N, Harkness W, Chakraborty A (2014) A novel technique of detecting MRI-negative lesion in focal symptomatic epilepsy: intraoperative ShearWave elastography. Epilepsia 55:e30–e33CrossRefPubMedGoogle Scholar
  40. 40.
    Selbekk T, Brekken R, Indergaard M, Solheim O, Unsgård G (2012) Comparison of contrast in brightness mode and strain ultrasonography of glial brain tumours. BMC Med Imaging 12:11CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Chakraborty A, Bamber JC, Dorward NL (2012) Preliminary investigation into the use of ultrasound elastography during brain tumour resection. Ultrasound 20:33–40CrossRefGoogle Scholar
  42. 42.
    Sebag F, Vaillant-Lombard J, Berbis J, Griset V, Henry JF, Petit P, Oliver C (2010) Shear wave elastography: a new ultrasound imaging mode for the differential diagnosis of benign and malignant thyroid nodules. J Clin Endocrinol Metab 95:5281–5288CrossRefPubMedGoogle Scholar
  43. 43.
    Ferraioli G, Parekh P, Levitov AB, Filice C (2014) Shear wave elastography for evaluation of liver fibrosis. J Ultrasound Med 33:197–203CrossRefPubMedGoogle Scholar
  44. 44.
    Chauvet D, Imbault M, Capelle L, Demene C, Mossad M, Karachi C, Boch AL, Gennisson JL, Tanter M (2015) In vivo measurement of brain tumour elasticity using intraoperative shear wave elastography. Ultraschall Med. doi: 10.1055/s-0034-1399152 PubMedGoogle Scholar
  45. 45.
    Hervey-Jumper SL, Berger MS (2014) Role of surgical resection in low- and high- grade gliomas. Curr Treat Neurol 16:284CrossRefGoogle Scholar
  46. 46.
    Selbekk T, Jakola AS, Solheim O, Johansen TF, Lindseth F, Reinertsen I, Unsgård G (2013) Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improving resection control. Act Neurochir 155:973–980CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Department of NeurosurgeryThe Royal London HospitalLondonEngland
  2. 2.Department of NeurosurgeryCharing Cross HospitalLondonEngland

Personalised recommendations