New prototype neuronavigation system based on preoperative imaging and intraoperative freehand ultrasound: system description and validation

  • Laurence MercierEmail author
  • Rolando F. Del Maestro
  • Kevin Petrecca
  • Anna Kochanowska
  • Simon Drouin
  • Charles X. B. Yan
  • Andrew L. Janke
  • Sean Jy-Shyang Chen
  • D. Louis Collins
Original Article



The aim of this report is to present IBIS (Interactive Brain Imaging System) NeuroNav, a new prototype neuronavigation system that has been developed in our research laboratory over the past decade that uses tracked intraoperative ultrasound to address surgical navigation issues related to brain shift. The unique feature of the system is its ability, when needed, to improve the initial patient-to-preoperative image alignment based on the intraoperative ultrasound data. Parts of IBIS Neuronav source code are now publicly available on-line.


Four aspects of the system are characterized in this paper: the ultrasound probe calibration, the temporal calibration, the patient-to-image registration and the MRI-ultrasound registration. In order to characterize its real clinical precision and accuracy, the system was tested in a series of adult brain tumor cases.


Three metrics were computed to evaluate the precision and accuracy of the ultrasound calibration. 1) Reproducibility: 1.77 mm and 1.65 mm for the bottom corners of the ultrasound image, 2) point reconstruction precision 0.62–0.90 mm: and 3) point reconstruction accuracy: 0.49–0.74 mm. The temporal calibration error was estimated to be 0.82 ms. The mean fiducial registration error (FRE) of the homologous-point-based patient-to-MRI registration for our clinical data is 4.9 ± 1.1 mm. After the skin landmark-based registration, the mean misalignment between the ultrasound and MR images in the tumor region is 6.1 ± 3.4 mm.


The components and functionality of a new prototype system are described and its precision and accuracy evaluated. It was found to have an accuracy similar to other comparable systems in the literature.


Application accuracy Image-guided surgery Intraoperative imaging Intraoperative ultrasound Neuronavigation Registration 


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  1. 1.
    Dussik K, Dussik F, Wyt L (1947) Auf dem Wege zur Hyperphonographie des Gehirnes. Wien med Wschr 97: 425–429PubMedGoogle Scholar
  2. 2.
    French LA, Wild JJ, Neal D (1950) Detection of cerebral tumors by ultrasonic pulses; pilot studies on postmortem material. Cancer 3: 705–708PubMedCrossRefGoogle Scholar
  3. 3.
    Ballantine HT Jr, Bolt RH, Hueter TF, Ludwig GD (1950) On the detection of intracranial pathology by ultrasound, vol 112. Science, New York, pp 525–528Google Scholar
  4. 4.
    Ballantine HT Jr, Ludwig GD, Bolt RH, Hueter TF (1950) Ultrasonic localization of the cerebral ventricles. Trans Am Neurol Assoc 51: 38–41PubMedGoogle Scholar
  5. 5.
    Voorhies RM, Patterson RH (1980) Preliminary experience with intra-operative ultrasonographic localization of brain tumors. Radiol Nucl Med 10: 8–9Google Scholar
  6. 6.
    Rubin JM, Mirfakhraee M, Duda EE, Dohrmann GJ, Brown F (1980) Intraoperative ultrasound examination of the brain. Radiology 137: 831–832PubMedGoogle Scholar
  7. 7.
    Iseki H, Kawamura H, Tanikawa T, Kawabatake H, Taira T, Takakura K, Dohi T, Hata N (1994) An image-guided stereotactic system for neurosurgical operations. Stereotact Funct Neurosurg 63: 130–138PubMedCrossRefGoogle Scholar
  8. 8.
    Koivukangas J, Ylitalo J, Alasaarela E, Tauriainen A (1986) Three-dimensional ultrasound imaging of brain for neurosurgery. Ann Clin Res 18(47): 65–72PubMedGoogle Scholar
  9. 9.
    Koivukangas J, Louhisalmi Y, Alakuijala J, Oikarinen J (1993) Ultrasound-controlled neuronavigator-guided brain surgery. J Neurosurg 79: 36–42PubMedCrossRefGoogle Scholar
  10. 10.
    Trobaugh JW, Richard WD, Smith KR, Bucholz RD (1994) Frameless stereotactic ultrasonography: method and applications. Comput Med Imaging Graph 18: 235–246PubMedCrossRefGoogle Scholar
  11. 11.
    Oikarinen J, Jyrki A, Louhisalmi Y, Sallinen S, Helminen H, Koivukangas J (1993) The oulu neuronavigator system: intraoperative ultrasonography in the verification of neurosurgical localization and visualization. In: Maciunas RJ (eds) Interactive image-guided neurosurgery. AANS, USA, pp 233–246Google Scholar
  12. 12.
    Tirakotai W, Miller D, Heinze S, Benes L, Bertalanffy H, Sure U (2006) A novel platform for image-guided ultrasound. Neurosurgery 58: 710–718 discussion 710–718PubMedCrossRefGoogle Scholar
  13. 13.
    Gronningsaeter A, Kleven A, Ommedal S, Aarseth TE, Lie T, Lindseth F, Langø T, Unsgard G (2000) SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 47: 1373–1379 discussion 1379–1380PubMedCrossRefGoogle Scholar
  14. 14.
    Trantakis C, Meixensberger J, Lindner D, Strauss G, Grunst G, Schmidtgen A, Arnold S (2002) Iterative neuronavigation using 3D ultrasound. A feasibility study. Neurol Res 24: 666–670PubMedCrossRefGoogle Scholar
  15. 15.
    Engelhardt M, Hansen C, Brendel B, Hold S, Brenke C, Pechlivanis I, Harders A, Ermert H, Schmieder K (2007) Real time neuronavigation using 3-D ultrasound and MRI in patients with brain tumor. Advances in medical engineering. Springer, Berlin, pp 59–63Google Scholar
  16. 16.
    Hata N, Dohi T, Iseki H, Takakura K (1997) Development of a frameless and armless stereotactic neuronavigation system with ultrasonographic registration. Neurosurgery 41: 608–613 discussion 613–614PubMedGoogle Scholar
  17. 17.
    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: 1–5CrossRefGoogle Scholar
  18. 18.
    Gerganov VM, Akbarian A, Samii A, Samii M, Fahlbusch R (2008) Intraoperative visualization of tumor resection in patients with intracranial tumors—a comparison of two-dimensional ultrasound and high-field MRI. 59th annual meeting of the German society of neurosurgery (DGNC), WürzburgGoogle Scholar
  19. 19.
    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 60–61PubMedCrossRefGoogle Scholar
  20. 20.
    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 812PubMedCrossRefGoogle Scholar
  21. 21.
    Knauth M, Wirtz CR, Tronnier VM, Aras N, Kunze S, Sartor K (1999) Intraoperative MR imaging increases the extent of tumor resection in patients with high-grade gliomas. AJNR Am J Neuroradiol 20: 1642–1646PubMedGoogle Scholar
  22. 22.
    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: 1073–1081PubMedCrossRefGoogle Scholar
  23. 23.
    van Velthoven V (2003) Intraoperative ultrasound imaging: comparison of pathomorphological findings in US versus CT, MRI and intraoperative findings. Acta Neurochir Suppl 85: 95–99PubMedGoogle Scholar
  24. 24.
    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 1269CrossRefGoogle Scholar
  25. 25.
    Lindseth F, Ommedal S, Bang J, Unsgaard G, Nagelhus Hernes TA (2001) Image fusion of ultrasound and MRI as an aid for assessing anatomical shifts and improving overview and interpretation in ultrasound guided neurosurgery. CARS 2001: 247–252Google Scholar
  26. 26.
    Nabavi A, Black PM, Gering DT, Westin CF, Mehta V, Pergolizzi RS Jr, Ferrant M, Warfield SK, Hata N, Schwartz RB, Wells WM 3rd, Kikinis R, Jolesz FA (2001) Serial intraoperative magnetic resonance imaging of brain shift. Neurosurgery 48: 787–797 discussion 797–798PubMedGoogle Scholar
  27. 27.
    Clatz O, Delingette H, Talos IF, Golby AJ, Kikinis R, Jolesz FA, Ayache N, Warfield SK (2005) Robust nonrigid registration to capture brain shift from intraoperative MRI. IEEE Trans Med Imaging 24: 1417–1427PubMedCrossRefGoogle Scholar
  28. 28.
    Hartkens T, Hill DL, Castellano-Smith AD, Hawkes DJ, Maurer CR Jr, Martin AJ, Hall WA, Liu H, Truwit CL (2003) Measurement and analysis of brain deformation during neurosurgery. IEEE Trans Med Imaging 22: 82–92PubMedCrossRefGoogle Scholar
  29. 29.
    Maurer CR Jr, Hill DLG, Martin AJ, Liu H, McCue M, Rueckert D, Lloret D, Hall WA, Maxwell RE, Hawkes DJ, Truwit CL (1998) Investigation of intraoperative brain deformation using a 1.5T interventional MR system: preliminary results. IEEE Trans Med Imaging 17: 817–825PubMedCrossRefGoogle Scholar
  30. 30.
    Hastreiter P, Rezk-Salama C, Soza G, Bauer M, Greiner G, Fahlbusch R, Ganslandt O, Nimsky C (2004) Strategies for brain shift evaluation. Med Image Anal 8: 447–464PubMedCrossRefGoogle Scholar
  31. 31.
    Trantakis C, Tittgemeyer M, Schneider JP, Lindner D, Winkler D, Strauss G, Meixensberger J (2003) Investigation of time-dependency of intracranial brain shift and its relation to the extent of tumor removal using intra-operative MRI. Neurol Res 25: 9–12PubMedCrossRefGoogle Scholar
  32. 32.
    Comeau RM, Fenster A, Peters TM (1998) Intraoperative US in interactive image-guided neurosurgery. Radiographics 18: 1019–1027PubMedGoogle Scholar
  33. 33.
    Schroeder W, Martin K, Lorensen B (2003) The visualization toolkit an object oriented approach to 3D graphics, VTK version 4.2. 3, vol 4. Kitware, New YorkGoogle Scholar
  34. 34.
    Neelin P (1998) The MINC file format: from bytes to brains. NeuroImage 7: 786Google Scholar
  35. 35.
    Gobbi DG, Comeau RM, Peters TM (1999) Ultrasound probe tracking for real-time ultrasound/MRI overlay and visualization of brain shift. MICCAI 1999, vol 1679. Lecture Notes in Computer Science. Springer, Cambridge, UK, pp 920–927Google Scholar
  36. 36.
    Mercier L, Lango T, Lindseth F, Collins DL (2005) A review of calibration techniques for freehand 3-D ultrasound systems. Ultrasound Med Biol 31: 449–471PubMedCrossRefGoogle Scholar
  37. 37.
    Treece GM, Gee AH, Prager RW, Cash CJ, Berman LH (2003) High-definition freehand 3-D ultrasound. Ultrasound Med Biol 29: 529–546PubMedCrossRefGoogle Scholar
  38. 38.
    Prager RW, Gee A, Berman L (1998) Stradx: real-time acquisition and visualization of freehand three-dimensional ultrasound. Med Image Anal 3: 129–140CrossRefGoogle Scholar
  39. 39.
    Lindseth F, Tangen GA, Langø T, Bang J (2003) Probe calibration for freehand 3-D ultrasound. Ultrasound Med Biol 29: 1607– 1623PubMedCrossRefGoogle Scholar
  40. 40.
    Blackall JM, Rueckert D, Maurer CR, Penny GP, Hill DLG, Hawkes DJ (2000) An image registration approach to automated calibration for freehand 3D ultrasound. MICCAI 2000, vol 1935. Lecture Notes in Computer Science. Springer, Pittsburgh, USA, pp 462–471Google Scholar
  41. 41.
    Maurer CR Jr, Fitzpatrick JM, Wang MY, Galloway RL Jr, Maciunas RJ, Allen GS (1997) Registration of head volume images using implantable fiducial markers. IEEE Trans Med Imaging 16: 447–462PubMedCrossRefGoogle Scholar
  42. 42.
    Fitzpatrick JM, West JB, Maurer CR Jr (1998) Predicting error in rigid-body point-based registration. IEEE Trans Med Imaging 17: 694–702PubMedCrossRefGoogle Scholar
  43. 43.
    Jannin P, Fitzpatrick JM, Hawkes DJ, Pennec X, Shahidi R, Vannier MW (2002) Validation of medical image processing in image-guided therapy. IEEE Trans Med Imaging 21: 1445–1449PubMedCrossRefGoogle Scholar
  44. 44.
    Comeau RM, Sadikot AF, Fenster A, Peters TM (2000) Intraoperative ultrasound for guidance and tissue shift correction in image-guided neurosurgery. Med Phys 27: 787–800PubMedCrossRefGoogle Scholar
  45. 45.
    Arbel T, Morandi X, Comeau RM, Collins DL (2001) Automatic non-linear MRI-ultrasound registration for the correction of intra-operative brain deformations. MICCAI 2001, vol 2208. LNCS. Springer, Utrecht, The Netherlands, pp 913–922Google Scholar
  46. 46.
    Arbel T, Morandi X, Comeau RM, Collins DL (2004) Automatic non-linear MRI-ultrasound registration for the correction of intra-operative brain deformations. Comput Aided Surg 9: 123–136PubMedGoogle Scholar
  47. 47.
    Klein D, Olivier A, Milner B, Zatorre RJ, Johnsrude I, Meyer E, Evans AC (1997) Obligatory role of the LIFG in synonym generation: evidence from PET and cortical stimulation. Neuroreport 8: 3275–3279PubMedCrossRefGoogle Scholar
  48. 48.
    Amiez C, Kostopoulos P, Champod AS, Collins DL, Doyon J, Del Maestro R, Petrides M (2008) Preoperative functional magnetic resonance imaging assessment of higher-order cognitive function in patients undergoing surgery for brain tumors. J Neurosurg 108: 258–268PubMedCrossRefGoogle Scholar
  49. 49.
    Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17: 87–97PubMedCrossRefGoogle Scholar
  50. 50.
    Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assis Tomogr 18: 192–205CrossRefGoogle Scholar
  51. 51.
    Zijdenbos AP, Dawant BM, Margolin RA, Palmer AC (1994) Morphometric analysis of white matter lesions in MR images: method and validation. IEEE Trans Med Imaging 13: 716–724PubMedCrossRefGoogle Scholar
  52. 52.
    MacDonald D, Kabani N, Avis D, Evans AC (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12: 340–356PubMedCrossRefGoogle Scholar
  53. 53.
    Bucholz RD, Yeh DD, Trobaugh JW, McDurmott LL (1997) The correction of stereotactic inaccuracy caused by brain shift using an intraoperative ultrasound device. CVRMed MRCAS’97, pp 459–466Google Scholar
  54. 54.
    Solberg OV, Lindseth F, Torp H, Blake RE, Nagelhus Hernes TA (2007) Freehand 3D ultrasound reconstruction algorithms—a review. Ultrasound Med Biol 33: 991–1009PubMedCrossRefGoogle Scholar
  55. 55.
    Coupe P, Hellier P, Morandi X, Barillot C (2007) A probabilistic objective function for 3d rigid registration of intraoperative us and preoperative MR brain images. ISBI, Arlington, pp 1320–1323Google Scholar
  56. 56.
    Ji S, Wu Z, Hartov A, Roberts DW, Paulsen KD (2008) Mutual-information-based image to patient re-registration using intraoperative ultrasound in image-guided neurosurgery. Med Phys 35: 4612–4624PubMedCrossRefGoogle Scholar
  57. 57.
    Reinertsen I, Descoteaux M, Drouin S, Siddiqi K, Collins DL (2004) Vessel driven correction of brain shift. MICCAI 2004, vol 3217, LNCS. Springer, Rennes, France, pp 208–216Google Scholar
  58. 58.
    Reinertsen I, Lindseth F, Unsgaard G, Collins DL (2007) Clinical validation of vessel-based registration for correction of brain-shift. Med Image Anal 11: 673–684PubMedCrossRefGoogle Scholar
  59. 59.
    Collignon A, Maes F, Delaere D, Vandermeulen D, Suetens P, Marchal G (1995) Automated multi-modality image registration based on information theory. IPMI’95 3: 263–274Google Scholar
  60. 60.
    Lindner D, Trantakis C, Renner C, Arnold S, Schmitgen A, Schneider J, Meixensberger J (2006) Application of intraoperative 3D ultrasound during navigated tumor resection. Minim Invasive Neurosurg 49: 197–202PubMedCrossRefGoogle Scholar
  61. 61.
    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 587–588PubMedCrossRefGoogle Scholar
  62. 62.
    Prager RW, Rohling RN, Gee AH, Berman L (1998) Rapid calibration for 3-D freehand ultrasound. Ultrasound Med Biol 24: 855–869PubMedCrossRefGoogle Scholar
  63. 63.
    Kowal J, Amstutz CA, Caversaccio M, Nolte L-P (2003) On the development and comparative evaluation of an ultrasuond B-mode probe calibration method. Comput Aided Surg 8: 107–119PubMedCrossRefGoogle Scholar
  64. 64.
    Rousseau F, Hellier P, Barillot C (2006) A novel temporal calibration method for 3-D ultrasound. IEEE Trans Med Imaging 25: 1108–1112PubMedCrossRefGoogle Scholar
  65. 65.
    Mascott CR, Sol JC, Bousquet P, Lagarrigue J, Lazorthes Y, Lauwers-Cances V (2006) Quantification of true in vivo (application) accuracy in cranial image-guided surgery: influence of mode of patient registration. Neurosurgery 59: 146–155CrossRefGoogle Scholar
  66. 66.
    Pfisterer WK, Papadopoulos S, Drumm DA, Smith K, Preul MC (2008) Fiducial versus nonfiducial neuronavigation registration assessment and considerations of accuracy. Neurosurgery 62: 201–207 discussion 207–208PubMedCrossRefGoogle Scholar
  67. 67.
    Villalobos H, Germano IM (1999) Clinical evaluation of multimodality registration in frameless stereotaxy. Comput Aided Surg 4: 45–49PubMedCrossRefGoogle Scholar
  68. 68.
    Woerdeman PA, Willems PWA, Noordmans HJ, Berkelbachvander Sprenkel JW (2006) Clinical accuracy of neuronavigation using registration methods based on point-pairs or surface matching. Int J CARS 1: 297–298Google Scholar
  69. 69.
    Dorward NL, Alberti O, Palmer JD, Kitchen ND, Thomas DG (1999) Accuracy of true frameless stereotaxy: in vivo measurement and laboratory phantom studies. Technical note. J Neurosurg 90: 160–168PubMedCrossRefGoogle Scholar
  70. 70.
    Shamir RR, Joskowicz L, Spektor S, Shoshan Y (2008) Localization and registration accuracy in image-guided neurosurgery: a clinical study. Int J CARS 3: S289Google Scholar
  71. 71.
    Fitzpatrick JM (2009) Fiducial registration error and target registration error are uncorrelated. SPIE Med Imaging 2009: 7261Google Scholar
  72. 72.
    Shamir RR, Joskowicz L (2009) Worst-case analysis of target localization errors in fiducial-based rigid body registration. In: Josien PWP, Benoit MD (eds) vol 7259. SPIE 725938Google Scholar
  73. 73.
    Fitzpatrick JM (2010) The role of registration in accurate surgical guidance. J Eng Med 224: 607–622CrossRefGoogle Scholar
  74. 74.
    Letteboer MM, Willems PW, Viergever MA, Niessen WJ (2005) Brain shift estimation in image-guided neurosurgery using 3-D ultrasound. IEEE Trans Biomed Eng 52: 268–276PubMedCrossRefGoogle Scholar
  75. 75.
    Keles GE, Lamborn KR, Berger MS (2003) Coregistration accuracy and detection of brain shift using intraoperative sononavigation during resection of hemispheric tumors. Neurosurgery 53: 556–562 discussion 562–564PubMedCrossRefGoogle Scholar
  76. 76.
    Ji S, Liu F, Hartov A, Roberts DW, Paulsen KD (2007) Brain–skull boundary conditions in a computational deformation model. In: Proceedings of SPIE, vol 6509, San Diego, USA 65092JGoogle Scholar
  77. 77.
    Lindseth F, Bang J, Langø T (2003) A robust and automatic method for evaluating accuracy in 3-D ultrasound-based navigation. Ultrasound Med Biol 29: 1439–1452PubMedCrossRefGoogle Scholar
  78. 78.
    Wiles A, Peters T (2008) Interactive software tool for IGS performance evaluation. Int J CARS 3: S314Google Scholar
  79. 79.
    Weiler F, Hahn HK, Koehn A, Friman O, Klein J, Peitgen H-O (2008) Dealing with inaccuracies in multimodal neurosurgical planning—a preliminary concept. Int J CARS 3: S77–S78Google Scholar

Copyright information

© CARS 2010

Authors and Affiliations

  • Laurence Mercier
    • 1
    Email author
  • Rolando F. Del Maestro
    • 2
  • Kevin Petrecca
    • 2
  • Anna Kochanowska
    • 1
  • Simon Drouin
    • 1
  • Charles X. B. Yan
    • 1
  • Andrew L. Janke
    • 3
  • Sean Jy-Shyang Chen
    • 1
  • D. Louis Collins
    • 1
  1. 1.McConnell Brain Imaging Center, Montreal Neurological InstituteMcGill UniversityMontrealCanada
  2. 2.Brain Tumour Research Centre, Montreal Neurological Institute and HospitalMcGill UniversityMontrealCanada
  3. 3.Department of Geriatric MedicineThe Australian National UniversityCanberraAustralia

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