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Table of Contents
Vol. 88, No. 1, 2010
Issue release date: January 2010
Section title: Technology Report
Free Access
Stereotact Funct Neurosurg 2010;88:1–10
(DOI:10.1159/000258143)

Estimation of Brain Deformation for Volumetric Image Updating in Protoporphyrin IX Fluorescence-Guided Resection

Valdés P.A.a, b · Fan X.b · Ji S.b · Harris B.T.a, c · Paulsen K.D.a, b, d · Roberts D.W.a, d, e
aDartmouth Medical School and bThayer School of Engineering, Dartmouth College, Hanover, N.H., cDepartment of Pathology, dNorris Cotton Cancer Center, and eSection of Neurosurgery, Dartmouth-Hitchcock Medical Center, Lebanon, N.H., USA
email Corresponding Author

Abstract

Introduction: Fluorescence-guided resection (FGR) of brain tumors is an intuitive, practical and emerging technology for visually delineating neoplastic tissue exposed intraoperatively. Image guidance is the standard technique for producing 3-dimensional spatially coregistered information for surgical decision making. Both technologies together are synergistic: the former detects surface fluorescence as a biomarker of the current surgical margin while the latter shows coregistered volumetric neuroanatomy but can be degraded by intraoperative brain shift. We present the implementation of deformation modeling for brain shift compensation in protoporphyrin IX FGR, integrating these two sources of information for maximum surgical benefit. Methods: Two patients underwent FGR coregistered with conventional image guidance. Histopathological analysis, intraoperative fluorescence and image space coordinates were recorded for biopsy specimens acquired during surgery. A biomechanical brain deformation model driven by intraoperative ultrasound data was used to generate updated MR images. Results: Combined use of fluorescence signatures and updated MR image information showed substantially improved accuracy compared to fluorescence or the original (i.e., nonupdated) MR images, detecting only true positives and true negatives, and no instances of false positives or false negatives. Conclusion: Implementation of brain deformation modeling in FGR shows promise for increasing the accuracy of neurosurgical guidance in the delineation and resection of brain tumors.

© 2009 S. Karger AG, Basel


  

Key Words

  • Fluorescence-guided resection
  • Brain shift
  • Protoporphyrin IX
  • Aminolevulinic acid
  • Deformation modeling
  • Brain tumor

References

  1. Utsuki S, Miyoshi N, Oka H, Miyajima Y, Shimizu S, Suzuki S, Fujii K: Fluorescence-guided resection of metastatic brain tumors using a 5-aminolevulinic acid-induced protoporphyrin IX: pathological study. Brain Tumor Pathol 2007;24:53–55.
  2. Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, Goetz AE, Kiefmann R, Reulen HJ: Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 1998;42:518–525.
  3. Stummer W, Stepp H, Moller G, Ehrhardt A, Leonhard M, Reulen HJ: Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue. Acta Neurochir (Wien) 1998;140:995–1000.
  4. Stummer W, Reulen HJ, Novotny A, Stepp H, Tonn JC: Fluorescence-guided resections of malignant gliomas – An overview. Acta Neurochir Suppl 2003;88:9–12.
  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: Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 2008;62:564–576.
  6. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ: Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006;7:392–401.
  7. Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ: Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 2000;93:1003–1013.
  8. Pichlmeier U, Bink A, Schackert G, Stummer W: Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients. Neuro Oncol 2008;10:1025–1034.
  9. Hefti M, von Campe G, Moschopulos M, Siegner A, Looser H, Landolt H: 5-Aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: a one-year experience at a single institution. Swiss Med Wkly 2008;138:180–185.
  10. Sun H, Roberts DW, Farid H, Wu Z, Hartov A, Paulsen KD: Cortical surface tracking using a stereoscopic operating microscope. Neurosurgery 2005;56:86–97.
  11. Sun H, Lunn KE, Farid H, Wu Z, Roberts DW, Hartov A, Paulsen KD: Stereopsis-guided brain shift compensation. IEEE Trans Med Imaging 2005;24:1039–1052.
  12. Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R: Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 2000;47:1070–1079.
  13. Lunn KE, Paulsen KD, Liu F, Kennedy FE, Hartov A, Roberts DW: Data-guided brain deformation modeling: evaluation of a 3-D adjoint inversion method in porcine studies. IEEE Trans Biomed Eng 2006;53:1893–1900.
  14. Hill DL, Maurer CR Jr, Maciunas RJ, Barwise JA, Fitzpatrick JM, Wang MY: Measurement of intraoperative brain surface deformation under a craniotomy. Neurosurgery 1998;43:514–526.
  15. Utsuki S, Oka H, Sato S, Shimizu S, Suzuki S, Tanizaki Y, Kondo K, Miyajima Y, Fujii K: Histological examination of false positive tissue resection using 5-aminolevulinic acid-induced fluorescence guidance. Neurol Med Chir (Tokyo) 2007;47:210–213.
  16. Toms SA, Lin WC, Weil RJ, Johnson MD, Jansen ED, Mahadevan-Jansen A: Intraoperative optical spectroscopy identifies infiltrating glioma margins with high sensitivity. Neurosurgery 2005;57:382–391.
  17. Ji S, Roberts DW, Hartov A, Paulsen KD: Brain-skull contact boundary conditions in an inverse computational deformation model. Med Image Anal 2009;13:659–672.
  18. Pallatroni H, Hartov A, McInerney J, Platenik LA, Miga MI, Kennedy FE, Paulsen KD, Roberts DW: Coregistered ultrasound as a neurosurgical guide. Stereotact Funct Neurosurg 1999;73:143–147.
  19. Hartov A, Roberts DW, Paulsen KD: A comparative analysis of coregistered ultrasound and magnetic resonance imaging in neurosurgery. Neurosurgery 2008;62:91–99.
  20. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P: The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97–109.
  21. 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: A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001;95:190–198.
  22. Barker FG 2nd, Prados MD, Chang SM, Gutin PH, Lamborn KR, Larson DA, Malec MK, McDermott MW, Sneed PK, Wara WM, Wilson CB: Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 1996;84:442–448.
  23. Albert FK, Forsting M, Sartor K, Adams HP, Kunze S: Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 1994;34:45–60.
  24. Black PM, Moriarty T, Alexander E 3rd, Stieg P, Woodard EJ, Gleason PL, Martin CH, Kikinis R, Schwartz RB, Jolesz FA: Development and implementation of intraoperative magnetic resonance imaging and its neurosurgical applications. Neurosurgery 1997;41:831–842.
  25. Gronningsaeter A, Kleven A, Ommedal S, Aarseth TE, Lie T, Lindseth F, Lango T, Unsgard G: Sonowand, an ultrasound based neuronavigation system. Neurosurgery 2000;47:1373–1379.
  26. Grunert P, Muller-Forell W, Darabi K, Reisch R, Busert C, Hopf N, Perneczky A: Basic principles and clinical applications of neuronavigation and intraoperative computed tomography. Comput Aided Surg 1998;3:166–173.
  27. Keles GE, Lamborn KR, Berger MS: Coregistration accuracy and detection of brain shift using intraoperative sononavigation during resection of hemispheric tumors. Neurosurgery 2003;53:556–562.
  28. Letteboer MM, Willems PW, Viergever MA, Niessen WJ: Brain shift estimation in image-guided neurosurgery using 3-D ultrasound. IEEE Trans Biomed Eng 2005;52:268–276.
  29. Matula C, Rossler K, Reddy M, Schindler E, Koos WT: Intraoperative computed tomography guided neuronavigation: concepts, efficiency, and work flow. Comput Aided Surg 1998;3:174–182.
  30. 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: Serial intraoperative magnetic resonance imaging of brain shift. Neurosurgery 2001;48:787–797.
  31. Nakao N, Nakai K, Itakura T: Updating of neuronavigation based on images intraoperatively acquired with a mobile computerized tomographic scanner: technical note. Minim Invasive Neurosurg 2003;46:117–120.
  32. Uhl E, Zausinger S, Morhard D, Heigl T, Scheder B, Rachinger W, Schichor C, Tonn JC: Intraoperative computed tomography with integrated navigation system in a multidisciplinary operating suite. Neurosurgery 2009;64:231–239.
  33. Roberts DW, Miga MI, Hartov A, Eisner S, Lemery JM, Kennedy FE, Paulsen KD: Intraoperatively updated neuroimaging using brain modeling and sparse data. Neurosurgery 1999;45:1199–1206.
  34. Wu Z, Paulsen KD, Sullivan JM Jr: Adaptive model initialization and deformation for automatic segmentation of T1-weighted brain MRI data. IEEE Trans Biomed Eng 2005;52:1128–1131.
  35. Ji S, Hartov A, Roberts DW, Paulsen KD: Data assimilation using a gradient descent method for estimation of intraoperative brain deformation. Med Image Anal 2009;13:744–756.

  

Author Contacts

David W. Roberts, MD
Section of Neurosurgery, Dartmouth-Hitchcock Medical Center
One Medical Center Drive
Lebanon, NH 03756 (USA)
Tel. +1 603 650 8734, Fax +1 603 650 7911, E-Mail David.W.Roberts@dartmouth.edu

  

Article Information

This study was presented in part at the 77th Annual Meeting of the American Association of Neurological Surgeons, San Diego, Calif., USA, May 5, 2009.

Received: July 16, 2009
Accepted after revision: August 28, 2009
Published online: November 12, 2009
Number of Print Pages : 10
Number of Figures : 5, Number of Tables : 3, Number of References : 35

  

Publication Details

Stereotactic and Functional Neurosurgery

Vol. 88, No. 1, Year 2010 (Cover Date: January 2010)

Journal Editor: Roberts D.W. (Lebanon, N.H.)
ISSN: 1011-6125 (Print), eISSN: 1423-0372 (Online)

For additional information: http://www.karger.com/SFN


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Introduction: Fluorescence-guided resection (FGR) of brain tumors is an intuitive, practical and emerging technology for visually delineating neoplastic tissue exposed intraoperatively. Image guidance is the standard technique for producing 3-dimensional spatially coregistered information for surgical decision making. Both technologies together are synergistic: the former detects surface fluorescence as a biomarker of the current surgical margin while the latter shows coregistered volumetric neuroanatomy but can be degraded by intraoperative brain shift. We present the implementation of deformation modeling for brain shift compensation in protoporphyrin IX FGR, integrating these two sources of information for maximum surgical benefit. Methods: Two patients underwent FGR coregistered with conventional image guidance. Histopathological analysis, intraoperative fluorescence and image space coordinates were recorded for biopsy specimens acquired during surgery. A biomechanical brain deformation model driven by intraoperative ultrasound data was used to generate updated MR images. Results: Combined use of fluorescence signatures and updated MR image information showed substantially improved accuracy compared to fluorescence or the original (i.e., nonupdated) MR images, detecting only true positives and true negatives, and no instances of false positives or false negatives. Conclusion: Implementation of brain deformation modeling in FGR shows promise for increasing the accuracy of neurosurgical guidance in the delineation and resection of brain tumors.

© 2009 S. Karger AG, Basel


  

Author Contacts

David W. Roberts, MD
Section of Neurosurgery, Dartmouth-Hitchcock Medical Center
One Medical Center Drive
Lebanon, NH 03756 (USA)
Tel. +1 603 650 8734, Fax +1 603 650 7911, E-Mail David.W.Roberts@dartmouth.edu

  

Article Information

This study was presented in part at the 77th Annual Meeting of the American Association of Neurological Surgeons, San Diego, Calif., USA, May 5, 2009.

Received: July 16, 2009
Accepted after revision: August 28, 2009
Published online: November 12, 2009
Number of Print Pages : 10
Number of Figures : 5, Number of Tables : 3, Number of References : 35

  

Publication Details

Stereotactic and Functional Neurosurgery

Vol. 88, No. 1, Year 2010 (Cover Date: January 2010)

Journal Editor: Roberts D.W. (Lebanon, N.H.)
ISSN: 1011-6125 (Print), eISSN: 1423-0372 (Online)

For additional information: http://www.karger.com/SFN


Article / Publication Details

First-Page Preview
Abstract of Technology Report

Received: 7/16/2009
Accepted: 8/28/2009
Published online: 11/12/2009
Issue release date: January 2010

Number of Print Pages: 10
Number of Figures: 5
Number of Tables: 3

ISSN: 1011-6125 (Print)
eISSN: 1423-0372 (Online)

For additional information: http://www.karger.com/SFN


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Utsuki S, Miyoshi N, Oka H, Miyajima Y, Shimizu S, Suzuki S, Fujii K: Fluorescence-guided resection of metastatic brain tumors using a 5-aminolevulinic acid-induced protoporphyrin IX: pathological study. Brain Tumor Pathol 2007;24:53–55.
  2. Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, Goetz AE, Kiefmann R, Reulen HJ: Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 1998;42:518–525.
  3. Stummer W, Stepp H, Moller G, Ehrhardt A, Leonhard M, Reulen HJ: Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue. Acta Neurochir (Wien) 1998;140:995–1000.
  4. Stummer W, Reulen HJ, Novotny A, Stepp H, Tonn JC: Fluorescence-guided resections of malignant gliomas – An overview. Acta Neurochir Suppl 2003;88:9–12.
  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: Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 2008;62:564–576.
  6. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ: Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 2006;7:392–401.
  7. Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ: Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 2000;93:1003–1013.
  8. Pichlmeier U, Bink A, Schackert G, Stummer W: Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients. Neuro Oncol 2008;10:1025–1034.
  9. Hefti M, von Campe G, Moschopulos M, Siegner A, Looser H, Landolt H: 5-Aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: a one-year experience at a single institution. Swiss Med Wkly 2008;138:180–185.
  10. Sun H, Roberts DW, Farid H, Wu Z, Hartov A, Paulsen KD: Cortical surface tracking using a stereoscopic operating microscope. Neurosurgery 2005;56:86–97.
  11. Sun H, Lunn KE, Farid H, Wu Z, Roberts DW, Hartov A, Paulsen KD: Stereopsis-guided brain shift compensation. IEEE Trans Med Imaging 2005;24:1039–1052.
  12. Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R: Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 2000;47:1070–1079.
  13. Lunn KE, Paulsen KD, Liu F, Kennedy FE, Hartov A, Roberts DW: Data-guided brain deformation modeling: evaluation of a 3-D adjoint inversion method in porcine studies. IEEE Trans Biomed Eng 2006;53:1893–1900.
  14. Hill DL, Maurer CR Jr, Maciunas RJ, Barwise JA, Fitzpatrick JM, Wang MY: Measurement of intraoperative brain surface deformation under a craniotomy. Neurosurgery 1998;43:514–526.
  15. Utsuki S, Oka H, Sato S, Shimizu S, Suzuki S, Tanizaki Y, Kondo K, Miyajima Y, Fujii K: Histological examination of false positive tissue resection using 5-aminolevulinic acid-induced fluorescence guidance. Neurol Med Chir (Tokyo) 2007;47:210–213.
  16. Toms SA, Lin WC, Weil RJ, Johnson MD, Jansen ED, Mahadevan-Jansen A: Intraoperative optical spectroscopy identifies infiltrating glioma margins with high sensitivity. Neurosurgery 2005;57:382–391.
  17. Ji S, Roberts DW, Hartov A, Paulsen KD: Brain-skull contact boundary conditions in an inverse computational deformation model. Med Image Anal 2009;13:659–672.
  18. Pallatroni H, Hartov A, McInerney J, Platenik LA, Miga MI, Kennedy FE, Paulsen KD, Roberts DW: Coregistered ultrasound as a neurosurgical guide. Stereotact Funct Neurosurg 1999;73:143–147.
  19. Hartov A, Roberts DW, Paulsen KD: A comparative analysis of coregistered ultrasound and magnetic resonance imaging in neurosurgery. Neurosurgery 2008;62:91–99.
  20. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P: The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97–109.
  21. 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: A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001;95:190–198.
  22. Barker FG 2nd, Prados MD, Chang SM, Gutin PH, Lamborn KR, Larson DA, Malec MK, McDermott MW, Sneed PK, Wara WM, Wilson CB: Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 1996;84:442–448.
  23. Albert FK, Forsting M, Sartor K, Adams HP, Kunze S: Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 1994;34:45–60.
  24. Black PM, Moriarty T, Alexander E 3rd, Stieg P, Woodard EJ, Gleason PL, Martin CH, Kikinis R, Schwartz RB, Jolesz FA: Development and implementation of intraoperative magnetic resonance imaging and its neurosurgical applications. Neurosurgery 1997;41:831–842.
  25. Gronningsaeter A, Kleven A, Ommedal S, Aarseth TE, Lie T, Lindseth F, Lango T, Unsgard G: Sonowand, an ultrasound based neuronavigation system. Neurosurgery 2000;47:1373–1379.
  26. Grunert P, Muller-Forell W, Darabi K, Reisch R, Busert C, Hopf N, Perneczky A: Basic principles and clinical applications of neuronavigation and intraoperative computed tomography. Comput Aided Surg 1998;3:166–173.
  27. Keles GE, Lamborn KR, Berger MS: Coregistration accuracy and detection of brain shift using intraoperative sononavigation during resection of hemispheric tumors. Neurosurgery 2003;53:556–562.
  28. Letteboer MM, Willems PW, Viergever MA, Niessen WJ: Brain shift estimation in image-guided neurosurgery using 3-D ultrasound. IEEE Trans Biomed Eng 2005;52:268–276.
  29. Matula C, Rossler K, Reddy M, Schindler E, Koos WT: Intraoperative computed tomography guided neuronavigation: concepts, efficiency, and work flow. Comput Aided Surg 1998;3:174–182.
  30. 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: Serial intraoperative magnetic resonance imaging of brain shift. Neurosurgery 2001;48:787–797.
  31. Nakao N, Nakai K, Itakura T: Updating of neuronavigation based on images intraoperatively acquired with a mobile computerized tomographic scanner: technical note. Minim Invasive Neurosurg 2003;46:117–120.
  32. Uhl E, Zausinger S, Morhard D, Heigl T, Scheder B, Rachinger W, Schichor C, Tonn JC: Intraoperative computed tomography with integrated navigation system in a multidisciplinary operating suite. Neurosurgery 2009;64:231–239.
  33. Roberts DW, Miga MI, Hartov A, Eisner S, Lemery JM, Kennedy FE, Paulsen KD: Intraoperatively updated neuroimaging using brain modeling and sparse data. Neurosurgery 1999;45:1199–1206.
  34. Wu Z, Paulsen KD, Sullivan JM Jr: Adaptive model initialization and deformation for automatic segmentation of T1-weighted brain MRI data. IEEE Trans Biomed Eng 2005;52:1128–1131.
  35. Ji S, Hartov A, Roberts DW, Paulsen KD: Data assimilation using a gradient descent method for estimation of intraoperative brain deformation. Med Image Anal 2009;13:744–756.